Decadal warming causes a consistent and persistent shift from heterotrophic to autotrophic respiration in contrasting permafrost ecosystems

Soil carbon in permafrost ecosystems has the potential to become a major positive feedback to climate change if permafrost thaw increases heterotrophic decomposition. However, warming can also stimulate autotrophic production leading to increased ecosystem carbon storage—a negative climate change feedback. Few studies partitioning ecosystem respiration examine decadal warming effects or compare responses among ecosystems. Here, we first examined how 11 years of warming during different seasons affected autotrophic and heterotrophic respiration in a bryophyte‐dominated peatland in Abisko, Sweden. We used natural abundance radiocarbon to partition ecosystem respiration into autotrophic respiration, associated with production, and heterotrophic decomposition. Summertime warming decreased the age of carbon respired by the ecosystem due to increased proportional contributions from autotrophic and young soil respiration and decreased proportional contributions from old soil. Summertime warming's large effect was due to not only warmer air temperatures during the growing season, but also to warmer deep soils year‐round. Second, we compared ecosystem respiration responses between two contrasting ecosystems, the Abisko peatland and a tussock‐dominated tundra in Healy, Alaska. Each ecosystem had two different timescales of warming (<5 years and over a decade). Despite the Abisko peatland having greater ecosystem respiration and larger contributions from heterotrophic respiration than the Healy tundra, both systems responded consistently to short‐ and long‐term warming with increased respiration, increased autotrophic contributions to ecosystem respiration, and increased ratios of autotrophic to heterotrophic respiration. We did not detect an increase in old soil carbon losses with warming at either site. If increased autotrophic respiration is balanced by increased primary production, as is the case in the Healy tundra, warming will not cause these ecosystems to become growing season carbon sources. Warming instead causes a persistent shift from heterotrophic to more autotrophic control of the growing season carbon cycle in these carbon‐rich permafrost ecosystems.     

Plant community structure regulates responses of prairie soil respiration to decadal experimental warming

Soil respiration is recognized to be influenced by temperature, moisture, and ecosystem production. However, little is known about how plant community structure regulates responses of soil respiration to climate change. Here, we used a 13‐year field warming experiment to explore the mechanisms underlying plant community regulation on feedbacks of soil respiration to climate change in a tallgrass prairie in Oklahoma, USA. Infrared heaters were used to elevate temperature about 2 °C since November 1999. Annual clipping was used to mimic hay harvest. Our results showed that experimental warming significantly increased soil respiration approximately from 10% in the first 7 years (2000–2006) to 30% in the next 6 years (2007–2012). The two‐stage warming stimulation of soil respiration was closely related to warming‐induced increases in ecosystem production over the years. Moreover, we found that across the 13 years, warming‐induced increases in soil respiration were positively affected by the proportion of aboveground net primary production (ANPP) contributed by C₃ forbs. Functional composition of the plant community regulated warming‐induced increases in soil respiration through the quantity and quality of organic matter inputs to soil and the amount of photosynthetic carbon (C) allocated belowground. Clipping, the interaction of clipping with warming, and warming‐induced changes in soil temperature and moisture all had little effect on soil respiration over the years (all P > 0.05). Our results suggest that climate warming may drive an increase in soil respiration through altering composition of plant communities in grassland ecosystems.     

Soil respiration response to climate change in Pacific Northwest prairies is mediated by a regional Mediterranean climate gradient

Soil respiration is expected to increase with rising global temperatures but the degree of response may depend on soil moisture and other local factors. Experimental climate change studies from single sites cannot discern whether an observed response is site‐dependent or generalizable. To deconvolve site‐specific vs. regional climatic controls, we examined soil respiration for 18 months along a 520 km climate gradient in three Pacific Northwest, USA prairies that represents increasingly severe Mediterranean conditions from north to south. At each site we implemented a fully factorial combination of 2.5–3 °C warming and 20% added precipitation intensity. The response of soil respiration to warming was driven primarily by the latitudinal climate gradient and not site‐specific factors. Warming increased respiration at all sites during months when soil moisture was not limiting. However, these gains were offset by reductions in respiration during seasonal transitions and summer drought due to lengthened periods of soil moisture limitation. The degree of this offset varied along the north–south climate gradient such that in 2011 warming increased cumulative annual soil respiration 28.6% in the northern site, 13.5% in the central site, and not at all in the southern site. Precipitation also stimulated soil respiration more frequently in the south, consistent with an increased duration of moisture limitation. The best predictors of soil respiration in nonlinear models were the Normalized Difference Vegetation Index (NDVI), antecedent soil moisture, and temperature but these models provided biased results at high and low soil respiration. NDVI was an effective integrator of climate and site differences in plant productivity in terms of their combined effects on soil respiration. Our results suggest that soil moisture limitation can offset the effect of warming on soil respiration, and that greater growing‐season moisture limitation would constrain cumulative annual responses to warming.     

Contrasting responses of heterotrophic and autotrophic respiration to experimental warming in a winter annual‐dominated prairie

Understanding how soil respiration (Rs) and its source components respond to climate warming is crucial to improve model prediction of climate‐carbon (C) feedback. We conducted a manipulation experiment by warming and clipping in a prairie dominated by invasive winter annual Bromus japonicas in Southern Great Plains, USA. Infrared radiators were used to simulate climate warming by 3 °C and clipping was used to mimic yearly hay mowing. Heterotrophic respiration (Rh) was measured inside deep collars (70 cm deep) that excluded root growth, while total soil respiration (Rs) was measured inside surface collars (2–3 cm deep). Autotrophic respiration (Ra) was calculated by subtracting Rh from Rs. During 3 years of experiment from January 2010 to December 2012, warming had no significant effect on Rs. The neutral response of Rs to warming was due to compensatory effects of warming on Rh and Ra. Warming significantly (P < 0.05) stimulated Rh but decreased Ra. Clipping only marginally (P < 0.1) increased Ra in 2010 but had no effect on Rh. There were no significant interactive effects of warming and clipping on Rs or its components. Warming stimulated annual Rh by 22.0%, but decreased annual Ra by 29.0% across the 3 years. The decreased Ra was primarily associated with the warming‐induced decline of the winter annual productivity. Across the 3 years, warming increased Rh/Rs by 29.1% but clipping did not affect Rh/Rs. Our study highlights that climate warming may have contrasting effects on Rh and Ra in association with responses of plant productivity to warming.     

增温和刈割对高寒草甸土壤呼吸及其组分的影响

评估土壤呼吸及其组分对增温等全球变化的响应对于预测陆地生态系统碳循环至关重要。本研究利用红外线辐射加热器(Infrared heater)装置在青藏高原高寒草甸生态系统设置增温和刈割野外控制实验。通过测定2018年生长季(5—9月)土壤呼吸和异养呼吸,探究增温和刈割对土壤呼吸及其组分的影响。研究结果表明：(1) 单独增温使土壤呼吸显著增加31.65% (P<0.05),异养呼吸显著增加27.12% (P<0.05),土壤自养呼吸没有显著改变(P>0.05);单独刈割对土壤呼吸和自养呼吸没有显著影响(P>0.05),单独刈割刺激异养呼吸增加32.54% (P<0.05);(2) 增温和刈割之间的交互作用对土壤呼吸和异养呼吸没有显著影响(P>0.05),但是对自养呼吸的影响是显著的(P<0.05),土壤呼吸和异养呼吸的季节效应显著(P<0.05);(3)土壤呼吸及其组分与土壤温度均成显著指数关系,与土壤湿度呈显著的正相关关系(P<0.05),处理影响它们的响应敏感性。本研究表明青藏高原东缘高寒草甸土壤碳排放与气候变暖存在正反馈。     

Contrasting mechanisms underlie short‐ and longer‐term soil respiration responses to experimental warming in a dryland ecosystem

Soil carbon losses to the atmosphere through soil respiration are expected to rise with ongoing temperature increases, but available evidence from mesic biomes suggests that such response disappears after a few years of experimental warming. However, there is lack of empirical basis for these temporal dynamics in soil respiration responses, and for the mechanisms underlying them, in drylands, which collectively form the largest biome on Earth and store 32% of the global soil organic carbon pool. We coupled data from a 10 year warming experiment in a biocrust‐dominated dryland ecosystem with laboratory incubations to confront 0–2 years (short‐term hereafter) versus 8–10 years (longer‐term hereafter) soil respiration responses to warming. Our results showed that increased soil respiration rates with short‐term warming observed in areas with high biocrust cover returned to control levels in the longer‐term. Warming‐induced increases in soil temperature were the main drivers of the short‐term soil respiration responses, whereas longer‐term soil respiration responses to warming were primarily driven by thermal acclimation and warming‐induced reductions in biocrust cover. Our results highlight the importance of evaluating short‐ and longer‐term soil respiration responses to warming as a mean to reduce the uncertainty in predicting the soil carbon–climate feedback in drylands.     

Adenylate control contributes to thermal acclimation of sugar maple fine‐root respiration in experimentally warmed soil

We investigated the occurrence of and mechanisms responsible for acclimation of fine‐root respiration of mature sugar maple (Acer saccharum) after 3+ years of experimental soil warming (+4 to 5 °C) in a factorial combination with soil moisture addition. Potential mechanisms for thermal respiratory acclimation included changes in enzymatic capacity, as indicated by root N concentration; substrate limitation, assessed by examining nonstructural carbohydrates and effects of exogenous sugar additions; and adenylate control, examined as responses of root respiration to a respiratory uncoupling agent. Partial acclimation of fine‐root respiration occurred in response to soil warming, causing specific root respiration to increase to a much lesser degree (14% to 26%) than would be expected for a 4 to 5 °C temperature increase (approximately 55%). Acclimation was greatest when ambient soil temperature was warmer or soil moisture availability was low. We found no evidence that enzyme or substrate limitation caused acclimation but did find evidence supporting adenylate control. The uncoupling agent caused a 1.4 times greater stimulation of respiration in roots from warmed soil. Sugar maple fine‐root respiration in warmed soil was at least partially constrained by adenylate use, helping constrain respiration to that needed to support work being performed by the roots.     

Increased soil release of greenhouse gases shrinks terrestrial carbon uptake enhancement under warming

Warming can accelerate the decomposition of soil organic matter and stimulate the release of soil greenhouse gases (GHGs), but to what extent soil release of methane (CH₄) and nitrous oxide (N₂O) may contribute to soil C loss for driving climate change under warming remains unresolved. By synthesizing 1,845 measurements from 164 peer‐reviewed publications, we show that around 1.5°C (1.16–2.01°C) of experimental warming significantly stimulates soil respiration by 12.9%, N₂O emissions by 35.2%, CH₄ emissions by 23.4% from rice paddies, and by 37.5% from natural wetlands. Rising temperature increases CH₄ uptake of upland soils by 13.8%. Warming‐enhanced emission of soil CH₄ and N₂O corresponds to an overall source strength of 1.19, 1.84, and 3.12 Pg CO₂‐equivalent/year under 1°C, 1.5°C, and 2°C warming scenarios, respectively, interacting with soil C loss of 1.60 Pg CO₂/year in terms of contribution to climate change. The warming‐induced rise in soil CH₄ and N₂O emissions (1.84 Pg CO₂‐equivalent/year) could reduce mitigation potential of terrestrial net ecosystem production by 8.3% (NEP, 22.25 Pg CO₂/year) under warming. Soil respiration and CH₄ release are intensified following the mean warming threshold of 1.5°C scenario, as compared to soil CH₄ uptake and N₂O release with a reduced and less positive response, respectively. Soil C loss increases to a larger extent under soil warming than under canopy air warming. Warming‐raised emission of soil GHG increases with the intensity of temperature rise but decreases with the extension of experimental duration. This synthesis takes the lead to quantify the ecosystem C and N cycling in response to warming and advances our capacity to predict terrestrial feedback to climate change under projected warming scenarios.     

Carbon losses due to soil warming: Do autotrophic and heterotrophic soil respiration respond equally?

Global warming has the potential to increase soil respiration (R_S), one of the major fluxes in the global carbon (C) cycle. R_S consists of an autotrophic (R_A) and a heterotrophic (R_H) component. We combined a soil warming experiment with a trenching experiment to assess how R_S, R_A, and R_H are affected. The experiment was conducted in a mature forest dominated by Norway spruce. The site is located in the Austrian Alps on dolomitic bedrock. We warmed the soil of undisturbed and trenched plots by means of heating cables 4 °C above ambient during the snow‐free seasons of 2005 and 2006. Soil warming increased the CO₂ efflux from control plots (R_S) by ∼45% during 2005 and ∼47% during 2006. The CO₂ efflux from trenched plots (R_H) increased by ∼39% during 2005 and ∼45% during 2006. Similar responses of R_S and R_H indicated that the autotrophic and heterotrophic components of R_S responded equally to the temperature increase. Thirty‐five to forty percent or 1 t C ha⁻¹ yr⁻¹ of the overall annual increase in R_S (2.8 t C ha⁻¹ yr⁻¹) was autotrophic. The remaining, heterotrophic part of soil respiration (1.8 t C ha⁻¹ yr⁻¹), represented the warming‐induced C loss from the soil. The autotrophic component showed a distinct seasonal pattern. Contribution of R_A to R_S was highest during summer. Seasonally derived Q₁₀ values reflected this pattern and were correspondingly high (5.3–9.3). The autotrophic CO₂ efflux increase due to the 4 °C warming implied a Q₁₀ of 2.9. Hence, seasonally derived Q₁₀ of R_A did not solely reflect the seasonal soil temperature development.     

Thermal acclimation of leaf respiration of tropical trees and lianas: response to experimental canopy warming,and consequences for tropical forest carbon balance

Climate warming is expected to increase respiration rates of tropical forest trees and lianas, which may negatively affect the carbon balance of tropical forests. Thermal acclimation could mitigate the expected respiration increase, but the thermal acclimation potential of tropical forests remains largely unknown. In a tropical forest in Panama, we experimentally increased nighttime temperatures of upper canopy leaves of three tree and two liana species by on average 3  ° C for 1 week, and quantified temperature responses of leaf dark respiration. Respiration at 25  ° C (R₂₅) decreased with increasing leaf temperature, but acclimation did not result in perfect homeostasis of respiration across temperatures. In contrast, Q₁₀ of treatment and control leaves exhibited similarly high values (range 2.5–3.0) without evidence of acclimation. The decrease in R₂₅ was not caused by respiratory substrate depletion, as warming did not reduce leaf carbohydrate concentration. To evaluate the wider implications of our experimental results, we simulated the carbon cycle of tropical latitudes (24 ° S–24 ° N) from 2000 to 2100 using a dynamic global vegetation model (LM3VN) modified to account for acclimation. Acclimation reduced the degree to which respiration increases with climate warming in the model relative to a no‐acclimation scenario, leading to 21% greater increase in net primary productivity and 18% greater increase in biomass carbon storage over the 21st century. We conclude that leaf respiration of tropical forest plants can acclimate to nighttime warming, thereby reducing the magnitude of the positive feedback between climate change and the carbon cycle.     

Thawing permafrost increases old soil and autotrophic respiration in tundra: Partitioning ecosystem respiration using δ13C and ∆14C

Ecosystem respiration (R_eco) is one of the largest terrestrial carbon (C) fluxes. The effect of climate change on R_eco depends on the responses of its autotrophic and heterotrophic components. How autotrophic and heterotrophic respiration sources respond to climate change is especially important in ecosystems underlain by permafrost. Permafrost ecosystems contain vast stores of soil C (1672 Pg) and are located in northern latitudes where climate change is accelerated. Warming will cause a positive feedback to climate change if heterotrophic respiration increases without corresponding increases in primary production. We quantified the response of autotrophic and heterotrophic respiration to permafrost thaw across the 2008 and 2009 growing seasons. We partitioned R_eco using Δ¹⁴C and δ¹³C into four sources–two autotrophic (above – and belowground plant structures) and two heterotrophic (young and old soil). We sampled the Δ¹⁴C and δ¹³C of sources using incubations and the Δ¹⁴C and δ¹³C of R_eco using field measurements. We then used a Bayesian mixing model to solve for the most likely contributions of each source to R_eco. Autotrophic respiration ranged from 40 to 70% of R_eco and was greatest at the height of the growing season. Old soil heterotrophic respiration ranged from 6 to 18% of R_eco and was greatest where permafrost thaw was deepest. Overall, growing season fluxes of autotrophic and old soil heterotrophic respiration increased as permafrost thaw deepened. Areas with greater thaw also had the greatest primary production. Warming in permafrost ecosystems therefore leads to increased plant and old soil respiration that is initially compensated by increased net primary productivity. However, barring large shifts in plant community composition, future increases in old soil respiration will likely outpace productivity, resulting in a positive feedback to climate change.     

Phenological responses of Icelandic subarctic grasslands to short‐term and long‐term natural soil warming

The phenology of vegetation, particularly the length of the growing season (LOS; i.e., the period from greenup to senescence), is highly sensitive to climate change, which could imply potent feedbacks to the climate system, for example, by altering the ecosystem carbon (C) balance. In recent decades, the largest extensions of LOS have been reported at high northern latitudes, but further warming‐induced LOS extensions may be constrained by too short photoperiod or unfulfilled chilling requirements. Here, we studied subarctic grasslands, which cover a vast area and contain large C stocks, but for which LOS changes under further warming are highly uncertain. We measured LOS extensions of Icelandic subarctic grasslands along natural geothermal soil warming gradients of different age (short term, where the measurements started after 5 years of warming and long term, i.e., warmed since ≥50 years) using ground‐level measurements of normalized difference vegetation index. We found that LOS linearly extended with on average 2.1 days per °C soil warming up to the highest soil warming levels (ca. +10°C) and that LOS had the potential to extend at least 1 month. This indicates that the warming impact on LOS in these subarctic grasslands will likely not saturate in the near future. A similar response to short‐ and long‐term warming indicated a strong physiological control of the phenological response of the subarctic grasslands to warming and suggested that genetic adaptations and community changes were likely of minor importance. We conclude that the warming‐driven extension of the LOSs of these subarctic grasslands did not saturate up to +10°C warming, and hence that growing seasons of high‐latitude grasslands are likely to continue lengthening with future warming (unless genetic adaptations or species shifts do occur). This persistence of the warming‐induced extension of LOS has important implications for the C‐sink potential of subarctic grasslands under climate change.     

Pathways regulating decreased soil respiration with warming in a biocrust‐dominated dryland

A positive soil carbon (C)‐climate feedback is embedded into the climatic models of the IPCC. However, recent global syntheses indicate that the temperature sensitivity of soil respiration (R_S) in drylands, the largest biome on Earth, is actually lower in warmed than in control plots. Consequently, soil C losses with future warming are expected to be low compared with other biomes. Nevertheless, the empirical basis for these global extrapolations is still poor in drylands, due to the low number of field experiments testing the pathways behind the long‐term responses of soil respiration (R_S) to warming. Importantly, global drylands are covered with biocrusts (communities formed by bryophytes, lichens, cyanobacteria, fungi, and bacteria), and thus, R_S responses to warming may be driven by both autotrophic and heterotrophic pathways. Here, we evaluated the effects of 8‐year experimental warming on R_S, and the different pathways involved, in a biocrust‐dominated dryland in southern Spain. We also assessed the overall impacts on soil organic C (SOC) accumulation over time. Across the years and biocrust cover levels, warming reduced R_S by 0.30 μmol CO₂ m^?2 s^?1 (95% CI = ?0.24 to 0.84), although the negative warming effects were only significant after 3 years of elevated temperatures in areas with low initial biocrust cover. We found support for different pathways regulating the warming‐induced reduction in R_S at areas with low (microbial thermal acclimation via reduced soil mass‐specific respiration and β‐glucosidase enzymatic activity) vs. high (microbial thermal acclimation jointly with a reduction in autotrophic respiration from decreased lichen cover) initial biocrust cover. Our 8‐year experimental study shows a reduction in soil respiration with warming and highlights that biocrusts should be explicitly included in modeling efforts aimed to quantify the soil C–climate feedback in drylands.     

Offsetting global warming‐induced elevated greenhouse gas emissions from an arable soil by biochar application

Global warming will likely enhance greenhouse gas (GHG) emissions from soils. Due to its slow decomposability, biochar is widely recognized as effective in long‐term soil carbon (C) sequestration and in mitigation of soil GHG emissions. In a long‐term soil warming experiment (+2.5 °C, since July 2008) we studied the effect of applying high‐temperature Miscanthus biochar (0, 30 t/ha, since August 2013) on GHG emissions and their global warming potential (GWP) during 2 years in a temperate agroecosystem. Crop growth, physical and chemical soil properties, temperature sensitivity of soil respiration (R_s), and metabolic quotient (qCO₂) were investigated to yield further information about single effects of soil warming and biochar as well as on their interactions. Soil warming increased total CO₂ emissions by 28% over 2 years. The effect of warming on soil respiration did not level off as has often been observed in less intensively managed ecosystems. However, the temperature sensitivity of soil respiration was not affected by warming. Overall, biochar had no effect on most of the measured parameters, suggesting its high degradation stability and its low influence on microbial C cycling even under elevated soil temperatures. In contrast, biochar × warming interactions led to higher total N₂O emissions, possibly due to accelerated N‐cycling at elevated soil temperature and to biochar‐induced changes in soil properties and environmental conditions. Methane uptake was not affected by soil warming or biochar. The incorporation of biochar‐C into soil was estimated to offset warming‐induced elevated GHG emissions for 25 years. Our results highlight the suitability of biochar for C sequestration in cultivated temperate agricultural soil under a future elevated temperature. However, the increased N₂O emissions under warming limit the GHG mitigation potential of biochar.     

Tree root and soil heterotrophic respiration as revealed by girdling of boreal Scots pine forest: extending observations beyond the first year

Limitations in available techniques to separate autotrophic (root) and soil heterotrophic respiration have hampered the understanding of forest C cycling. The former is here defined as respiration by roots, their associated mycorrhizal fungi and other micro‐organisms in the rhizosphere directly dependent on labile C compounds leaked from roots. In order to separate the autotrophic and heterotrophic components of soil respiration, all Scots pine trees in 900 m² plots were girdled to instantaneously terminate the supply of current photosynthates from the tree canopy to roots. Högberg et al. (Nature 411, 789–792, 2001) reported that autotrophic activity contributed up to 56% of total soil respiration during the first summer of this experiment. They also found that mobilization of stored starch (and likely also sugars) in roots after girdling caused an increased apparent heterotrophic respiration on girdled plots. Herein a transient increase in the δ¹³C of soil CO₂ efflux after girdling, thought to be due to decomposition of ¹³C‐enriched ectomycorrhizal mycelium and root starch and sugar reserves, is reported. In the second year after girdling, when starch reserves of girdled tree roots were exhausted, calculated root respiration increased up to 65% of total soil CO₂ efflux. It is suggested that this estimate of its contribution to soil respiration is more precise than the previous based on one year of observation. Heterotrophic respiration declined in response to a 20‐day‐long 6 °C decline in soil temperature during the second summer, whereas root respiration did not decline. This did not support the idea that root respiration should be more sensitive to variations in soil temperature. It is suggested that above‐ground photosynthetic activity and allocation patterns of recent photosynthates to roots should be considered in models of responses of forest C balances to global climate change.     

Increasing microbial carbon use efficiency with warming predicts soil heterotrophic respiration globally

The degree to which climate warming will stimulate soil organic carbon (SOC) losses via heterotrophic respiration remains uncertain, in part because different or even opposite microbial physiology and temperature relationships have been proposed in SOC models. We incorporated competing microbial carbon use efficiency (CUE)–mean annual temperature (MAT) and enzyme kinetic–MAT relationships into SOC models, and compared the simulated mass‐specific soil heterotrophic respiration rates with multiple published datasets of measured respiration. The measured data included 110 dryland soils globally distributed and two continental to global‐scale cross‐biome datasets. Model–data comparisons suggested that a positive CUE–MAT relationship best predicts the measured mass‐specific soil heterotrophic respiration rates in soils distributed globally. These results are robust when considering models of increasing complexity and competing mechanisms driving soil heterotrophic respiration–MAT relationships (e.g., carbon substrate availability). Our findings suggest that a warmer climate selects for microbial communities with higher CUE, as opposed to the often hypothesized reductions in CUE by warming based on soil laboratory assays. Our results help to build the impetus for, and confidence in, including microbial mechanisms in soil biogeochemical models used to forecast changes in global soil carbon stocks in response to warming.     

Age‐mediation of tree‐growth responses to experimental warming in the northeastern Tibetan Plateau

The trajectory of tree‐growth response to climate warming may be related to attributes like tree age. However, age‐mediation of temperature sensitivity of tree growth has received little attention. This study aimed to determine how age affects tree growth in a future warmer world. In a 2‐year ecosystem warming experiment in the northeastern Tibetan Plateau of China, we explored the response of Qinghai spruce saplings at two life stages to two warming levels. Our results indicated a significant interaction between warming and age for sapling growth of Qinghai spruce. In high‐level warming scenario, the experiment increased growing season air temperatures by approximately 1.0°C and annual growing degree‐days by 38%. In response, warmed saplings lengthened the growing season by 10 days on average and increased the final shoot length to a maximum of 104% compared to control groups. Comparison of age classes revealed that old saplings exhibited significantly higher temperature sensitivity than young saplings. This performance may be caused by the differences in adaptive strategy to the asymmetric warming occurring during the whole day. Increased daytime temperature was expected to significantly enhance leaf photosynthesis, whereas lack of obvious nighttime warming would effectively restrict autotrophic respiration, thus resulting in the higher growth rate of old saplings compared with young saplings. Moreover, lack of nighttime warming rendered young saplings to be still in high stresses of freezing injury at low temperatures. These findings highlight the need for additional research on the effects of further climate anomalies on tree species during their ontogenetic processes.     

Thermal adaptation of heterotrophic soil respiration in laboratory microcosms

Respiration of heterotrophic microorganisms decomposing soil organic carbon releases carbon dioxide from soils to the atmosphere. In the short term, soil microbial respiration is strongly dependent on temperature. In the long term, the response of heterotrophic soil respiration to temperature is uncertain. However, following established evolutionary trade‐offs, mass‐specific respiration (R_mass) rates of heterotrophic soil microbes should decrease in response to sustained increases in temperature (and vice‐versa). Using a laboratory microcosm approach, we tested the potential for the R_mass of the microbial biomass in six different soils to adapt to three, experimentally imposed, thermal regimes (constant 10, 20 or 30 °C). To determine R_mass rates of the heterotrophic soil microbial biomass across the temperature range of the imposed thermal regimes, we periodically assayed soil subsamples using similar approaches to those used in plant, animal and microbial thermal adaptation studies. As would be expected given trade‐offs between maximum catalytic rates and the stability of the binding structure of enzymes, after 77 days of incubation R_mass rates across the range of assay temperatures were greatest for the 10 °C experimentally incubated soils and lowest for the 30 °C soils, with the 20 °C incubated soils intermediate. The relative magnitude of the difference in R_mass rates between the different incubation temperature treatments was unaffected by assay temperature, suggesting that maximum activities and not Q₁₀ were the characteristics involved in thermal adaptation. The time taken for changes in R_mass to manifest (77 days) suggests they likely resulted from population or species shifts during the experimental incubations; we discuss alternate mechanistic explanations for those results we observed. A future research priority is to evaluate the role that thermal adaptation plays in regulating heterotrophic respiration rates from field soils in response to changing temperature, whether seasonally or through climate change.     

Experimental fire increases soil carbon dioxide efflux in a grassland long‐term multifactor global change experiment

Numerous studies have demonstrated that soil respiration rates increase under experimental warming, although the long‐term, multiyear dynamics of this feedback are not well constrained. Less is known about the effects of single, punctuated events in combination with other longer‐duration anthropogenic influences on the dynamics of soil carbon (C) loss. In 2012 and 2013, we assessed the effects of decadal‐scale anthropogenic global change – warming, increased nitrogen (N) deposition, elevated carbon dioxide (CO₂), and increased precipitation – on soil respiration rates in an annual‐dominated Mediterranean grassland. We also investigated how controlled fire and an artificial wet‐up event, in combination with exposure to the longer‐duration anthropogenic global change factors, influenced the dynamics of C cycling in this system. Decade‐duration surface soil warming (1–2 °C) had no effect on soil respiration rates, while +N addition and elevated CO₂ concentrations increased growing‐season soil CO₂ efflux rates by increasing annual aboveground net primary production (NPP) and belowground fine root production, respectively. Low‐intensity experimental fire significantly elevated soil CO₂ efflux rates in the next growing season. Based on mixed‐effects modeling and structural equation modeling, low‐intensity fire increased growing‐season soil respiration rates through a combination of three mechanisms: large increases in soil temperature (3–5 °C), significant increases in fine root production, and elevated aboveground NPP. Our study shows that in ecosystems where soil respiration has acclimated to moderate warming, further increases in soil temperature can stimulate greater soil CO₂ efflux. We also demonstrate that punctuated short‐duration events such as fire can influence soil C dynamics with implications for both the parameterization of earth system models (ESMs) and the implementation of climate change mitigation policies that involve land‐sector C accounting.     

Soil respiration under climate change: prolonged summer drought offsets soil warming effects

Climate change may considerably impact the carbon (C) dynamics and C stocks of forest soils. To assess the combined effects of warming and reduced precipitation on soil CO₂ efflux, we conducted a two‐way factorial manipulation experiment (4 °C soil warming + throughfall exclusion) in a temperate spruce forest from 2008 until 2010. Soil was warmed by heating cables throughout the growing seasons. Soil drought was simulated by throughfall exclusions with three 100 m² roofs during 25 days in July/August 2008 and 2009. Soil warming permanently increased the CO₂ efflux from soil, whereas throughfall exclusion led to a sharp decrease in soil CO₂ efflux (45% and 50% reduction during roof installation in 2008 and 2009, respectively). In 2008, CO₂ efflux did not recover after natural rewetting and remained lowered until autumn. In 2009, CO₂ efflux recovered shortly after rewetting, but relapsed again for several weeks. Drought offset the increase in soil CO₂ efflux by warming in 2008 (growing season CO₂ efflux in t C ha^?1: control: 7.1 ± 1.0; warmed: 9.5 ± 1.7; warmed + roof: 7.4 ± 0.3; roof: 5.9 ± 0.4) and in 2009 (control: 7.6 ± 0.8; warmed + roof: 8.3 ± 1.0). Throughfall exclusion mainly affected the organic layer and the top 5 cm of the mineral soil. Radiocarbon data suggest that heterotrophic and autotrophic respiration were affected to the same extent by soil warming and drying. Microbial biomass in the mineral soil (0–5 cm) was not affected by the treatments. Our results suggest that warming causes significant C losses from the soil as long as precipitation patterns remain steady at our site. If summer droughts become more severe in the future, warming induced C losses will likely be offset by reduced soil CO₂ efflux during and after summer drought.