Evaluating soil microbial carbon use efficiency explicitly as a function of cellular processes: implications for measurements and models

Carbon use efficiency (CUE), the proportion of carbon (C) consumed by microbes that is converted into biomass, is an important parameter for soil C models with explicit microbial controls. While often considered as a single parameter, CUE is an emergent property of multiple microbial processes, including assimilation efficiency, biomass-specific respiration, enzyme production, and respiratory costs of enzyme production. These processes occur over variable time scales and imply different fates for C, and the same emergent CUE value can result when C is allocated in fundamentally different ways (e.g. a high investment in enzyme production vs. a high assimilation cost). We developed a model that represents the individual processes underlying emergent CUE to test how shifts in microbial allocation alter equilibrium soil C pool sizes. We found that an increase in emergent CUE that results from a change in assimilation efficiency, biomass specific respiration, or respiration costs from enzyme production causes soil organic C (SOC) to decline, while the same change in emergent CUE resulting from a change in enzyme production causes SOC to increase. We also used the model to test the sensitivity of CUE from isotopic C tracer estimates to changes in microbial allocation processes. We found that these estimates do not account for the same microbial processes represented by emergent CUE in models. We propose that considering microbial processes explicitly rather than representing CUE as a single parameter can improve data-model integration. In addition, modeling microbial processes explicitly will account for a wider range of possible outcomes from shifts in microbial C allocation, such as when increased SOC results from increasing CUE.     

Does declining carbon‐use efficiency explain thermal acclimation of soil respiration with warming?

Enhanced soil respiration in response to global warming may substantially increase atmospheric CO₂ concentrations above the anthropogenic contribution, depending on the mechanisms underlying the temperature sensitivity of soil respiration. Here, we compared short‐term and seasonal responses of soil respiration to a shifting thermal environment and variable substrate availability via laboratory incubations. To analyze the data from incubations, we implemented a novel process‐based model of soil respiration in a hierarchical Bayesian framework. Our process model combined a Michaelis–Menten‐type equation of substrate availability and microbial biomass with an Arrhenius‐type nonlinear temperature response function. We tested the competing hypotheses that apparent thermal acclimation of soil respiration can be explained by depletion of labile substrates in warmed soils, or that physiological acclimation reduces respiration rates. We demonstrated that short‐term apparent acclimation can be induced by substrate depletion, but that decreasing microbial biomass carbon (MBC) is also important, and lower MBC at warmer temperatures is likely due to decreased carbon‐use efficiency (CUE). Observed seasonal acclimation of soil respiration was associated with higher CUE and lower basal respiration for summer‐ vs. winter‐collected soils. Whether the observed short‐term decrease in CUE or the seasonal acclimation of CUE with increased temperatures dominates the response to long‐term warming will have important consequences for soil organic carbon storage.     

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.     

Microbial Growth and Carbon Use Efficiency in the Rhizosphere and Root-Free Soil

Plant-microbial interactions alter C and N balance in the rhizosphere and affect the microbial carbon use efficiency (CUE)–the fundamental characteristic of microbial metabolism. Estimation of CUE in microbial hotspots with high dynamics of activity and changes of microbial physiological state from dormancy to activity is a challenge in soil microbiology. We analyzed respiratory activity, microbial DNA content and CUE by manipulation the C and nutrients availability in the soil under Beta vulgaris. All measurements were done in root-free and rhizosphere soil under steady-state conditions and during microbial growth induced by addition of glucose. Microorganisms in the rhizosphere and root-free soil differed in their CUE dynamics due to varying time delays between respiration burst and DNA increase. Constant CUE in an exponentially-growing microbial community in rhizosphere demonstrated the balanced growth. In contrast, the CUE in the root-free soil increased more than three times at the end of exponential growth and was 1.5 times higher than in the rhizosphere. Plants alter the dynamics of microbial CUE by balancing the catabolic and anabolic processes, which were decoupled in the root-free soil. The effects of N and C availability on CUE in rhizosphere and root-free soil are discussed.     

Atmospheric CO2 mole fraction affects stand‐scale carbon use efficiency of sunflower by stimulating respiration in light

Plant carbon‐use‐efficiency (CUE), a key parameter in carbon cycle and plant growth models, quantifies the fraction of fixed carbon that is converted into net primary production rather than respired. CUE has not been directly measured, partly because of the difficulty of measuring respiration in light. Here, we explore if CUE is affected by atmospheric CO₂. Sunflower stands were grown at low (200 μmol mol^?1) or high CO₂ (1000 μmol mol^?1) in controlled environment mesocosms. CUE of stands was measured by dynamic stand‐scale ¹³C labelling and partitioning of photosynthesis and respiration. At the same plant age, growth at high CO₂ (compared with low CO₂) led to 91% higher rates of apparent photosynthesis, 97% higher respiration in the dark, yet 143% higher respiration in light. Thus, CUE was significantly lower at high (0.65) than at low CO₂ (0.71). Compartmental analysis of isotopic tracer kinetics demonstrated a greater commitment of carbon reserves in stand‐scale respiratory metabolism at high CO₂. Two main processes contributed to the reduction of CUE at high CO₂: a reduced inhibition of leaf respiration by light and a diminished leaf mass ratio. This work highlights the relevance of measuring respiration in light and assessment of the CUE response to environment conditions.     

植物与微生物碳利用效率及影响因子研究进展

陆地生态系统碳循环是生物地球化学循环的关键过程之一。碳利用效率（carbon use efficiency,CUE）是描述生物用于形成生物量的碳占其所吸收总碳比例的一个定量指标,反映了生物的碳同化能力和固碳潜力,是研究生态系统碳循环中碳通量和碳分配模式的重要参数,能有效预测生物与周围环境之间的碳流通和碳反馈。目前,关于CUE的研究还不充分,尤其是对CUE及其影响因子的系统性综合论述还较少。为此,本文综述了国内外有关碳利用效率（植物碳利用效率（CUE_a）和微生物碳利用效率（CUE_h））的研究方法和研究进展,分析了CUE_a和CUE_h的异同、内在联系及作用机理。基于分析对今后的研究提出几点展望：（1）优化测量手段和计算方法,适当地调整参数,将模型方法与实测数据结合,使CUE的定量描述结果更准确;（2）结合不同尺度的研究结果,探究个体、种群、群落、生态系统等不同空间尺度和时间尺度上CUE的联系及变化规律,为碳循环和碳流通的时空变化规律提供新证据;（3）研究CUE对全球变化（如高温、干旱、CO₂浓度增加等）的响应,探讨CUE对未来气候情景的响应和适应机制;（4）开展有关物种丰富度或生物多样性的梯度变化对CUE的影响研究,阐释物种多样性减少或物种灭绝等现象对碳循环过程的影响,将生态系统物种多样性与生态系统功能相联系;（5）加强对CUE_h的研究,定量探究其与CUE_a的异同,并将二者结合起来,更全面地解释地上-地下生态系统碳的分配特征。同时适当开展动物CUE的研究,目前该类研究还缺乏系统性。     

Impacts of elevated temperature on the growth and functioning of decomposer fungi are influenced by grazing collembola

Elevated temperature has potential to influence the biological mechanisms regulating ecosystem–atmosphere carbon exchange. The relationship between warming and heterotrophic microbial respiration remains poorly understood, not least in terms of the differential sensitivity of microbial groups to temperature and the complexity of interactions with other biota. Cord‐forming basidiomycete fungi are dominant primary decomposers in temperate woodland. Decomposition rates are determined by the composition of the decomposer community, ecophysiological relationships between these fungi and abiotic variables and interactions with other organisms. Amongst the latter, a major determinant is the balance between mycelial growth and removal by soil invertebrate grazers, which can themselves be affected by elevated temperature. We investigated the impact of elevated temperature on fungal foraging and decomposition of beech (Fagus sylvatica) wood in soil microcosms to which the invertebrate grazers, Folsomia candida and Protophorura armata (Collembola), were added in factorial combinations with five basidiomycete fungi. Species‐specific impacts on mycelial development and function resulted from differential sensitivity of fungi to warming and grazing. Temperature impacts on collembola abundance were resource‐specific, causing increased grazing pressure by both species, but on different fungi. Grazing often counteracted warming‐induced stimulation of mycelial growth, but occasionally amplified the temperature effect, with implications for colonization rates of new resources. High grazing pressure did not prevent increased fungal‐mediated decomposition of colonized wood, as fungi utilized more resource‐derived energy to maintain explorative growth. Impacts of elevated temperature on decomposition are likely to depend on local composition of the fungal and invertebrate decomposer community.     

Forest carbon use efficiency: is respiration a constant fraction of gross primary production?

Carbon‐use efficiency (CUE), the ratio of net primary production (NPP) to gross primary production (GPP), describes the capacity of forests to transfer carbon (C) from the atmosphere to terrestrial biomass. It is widely assumed in many landscape‐scale carbon‐cycling models that CUE for forests is a constant value of ∼0.5. To achieve a constant CUE, tree respiration must be a constant fraction of canopy photosynthesis. We conducted a literature survey to test the hypothesis that CUE is constant and universal among forest ecosystems. Of the 60 data points obtained from 26 papers published since 1975, more than half reported values of GPP that were not estimated independently from NPP; values of CUE calculated from independent estimates of GPP were greater than those calculated from estimates of GPP derived from NPP. The slope of the relationship between NPP and GPP for all forests was 0.53, but values of CUE varied from 0.23 to 0.83 for different forest types. CUE decreased with increasing age, and a substantial portion of the variation among forest types was caused by differences in stand age. When corrected for age the mean value of CUE was greatest for temperate deciduous forests and lowest for boreal forests. CUE also increased as the ratio of leaf mass‐to‐total mass increased. Contrary to the assumption of constancy, substantial variation in CUE has been reported in the literature. It may be inappropriate to assume that respiration is a constant fraction of GPP as adhering to this assumption may contribute to incorrect estimates of C cycles. A 20% error in current estimates of CUE used in landscape models (i.e. ranging from 0.4 to 0.6) could misrepresent an amount of C equal to total anthropogenic emissions of CO₂ when scaled to the terrestrial biosphere.     

Carbon use efficiency of microbial communities: stoichiometry,methodology and modelling

Carbon use efficiency (CUE) is a fundamental parameter for ecological models based on the physiology of microorganisms. CUE determines energy and material flows to higher trophic levels, conversion of plant‐produced carbon into microbial products and rates of ecosystem carbon storage. Thermodynamic calculations support a maximum CUE value of ~ 0.60 (CUE _max). Kinetic and stoichiometric constraints on microbial growth suggest that CUE in multi‐resource limited natural systems should approach ~ 0.3 (CUE _max/2). However, the mean CUE values reported for aquatic and terrestrial ecosystems differ by twofold (~ 0.26 vs. ~ 0.55) because the methods used to estimate CUE in aquatic and terrestrial systems generally differ and soil estimates are less likely to capture the full maintenance costs of community metabolism given the difficulty of measurements in water‐limited environments. Moreover, many simulation models lack adequate representation of energy spilling pathways and stoichiometric constraints on metabolism, which can also lead to overestimates of CUE. We recommend that broad‐scale models use a CUE value of 0.30, unless there is evidence for lower values as a result of pervasive nutrient limitations. Ecosystem models operating at finer scales should consider resource composition, stoichiometric constraints and biomass composition, as well as environmental drivers, to predict the CUE of microbial communities.     

Trends in seedling growth and carbon‐use efficiency vary among broadleaf tree species along a latitudinal transect in eastern North America

Factors constraining the geographic ranges of broadleaf tree species in eastern North America were examined in common gardens along a ~1500 km latitudinal transect travers in grange boundaries of four target species: trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera) to the north vs. eastern cottonwood (Populus deltoides) and sweet gum (Liquidambar styraciflua) to the south. In 2006 and 2007, carbon‐use efficiency (CUE), the proportion of assimilated carbon retained in biomass, was estimated for seedlings of the four species as the quotient of relative growth rate (RGR) and photosynthesis per unit tree mass (A_tree). In aspen and birch, CUE and RGR declined significantly with increasing growth temperature, which spanned 9 °C across gardens and years. The 37% (relative) CUE decrease from coolest to warmest garden correlated with increases in leaf nighttime respiration (R_leaf) and the ratio of R_leaf to leaf photosynthesis (R_%A). For cottonwood and sweet gum, however, similar increases in R_leaf and R_%A accompanied modest CUE declines, implying that processes other than R_leaf were responsible for species differences in CUE's temperature response. Our findings illustrate marked taxonomic variation, at least among young trees, in the thermal sensitivity of CUE, and point to potentially negative consequences of climate warming for the carbon balance, competitive ability, and persistence of two foundation species in northern temperate and boreal forests.     

Increased microbial growth,biomass, and turnover drive soil organic carbon accumulation at higher plant diversity

Species‐rich plant communities have been shown to be more productive and to exhibit increased long‐term soil organic carbon (SOC) storage. Soil microorganisms are central to the conversion of plant organic matter into SOC, yet the relationship between plant diversity, soil microbial growth, turnover as well as carbon use efficiency (CUE) and SOC accumulation is unknown. As heterotrophic soil microbes are primarily carbon limited, it is important to understand how they respond to increased plant‐derived carbon inputs at higher plant species richness (PSR). We used the long‐term grassland biodiversity experiment in Jena, Germany, to examine how microbial physiology responds to changes in plant diversity and how this affects SOC content. The Jena Experiment considers different numbers of species (1–60), functional groups (1–4) as well as functional identity (small herbs, tall herbs, grasses, and legumes). We found that PSR accelerated microbial growth and turnover and increased microbial biomass and necromass. PSR also accelerated microbial respiration, but this effect was less strong than for microbial growth. In contrast, PSR did not affect microbial CUE or biomass‐specific respiration. Structural equation models revealed that PSR had direct positive effects on root biomass, and thereby on microbial growth and microbial biomass carbon. Finally, PSR increased SOC content via its positive influence on microbial biomass carbon. We suggest that PSR favors faster rates of microbial growth and turnover, likely due to greater plant productivity, resulting in higher amounts of microbial biomass and necromass that translate into the observed increase in SOC. We thus identify the microbial mechanism linking species‐rich plant communities to a carbon cycle process of importance to Earth's climate system.     

Reduced carbon use efficiency and increased microbial turnover with soil warming

Global soil carbon (C) stocks are expected to decline with warming, and changes in microbial processes are key to this projection. However, warming responses of critical microbial parameters such as carbon use efficiency (CUE) and biomass turnover (rB) are not well understood. Here, we determine these parameters using a probabilistic inversion approach that integrates a microbial‐enzyme model with 22 years of carbon cycling measurements at Harvard Forest. We find that increasing temperature reduces CUE but increases rB, and that two decades of soil warming increases the temperature sensitivities of CUE and rB. These temperature sensitivities, which are derived from decades‐long field observations, contrast with values obtained from short‐term laboratory experiments. We also show that long‐term soil C flux and pool changes in response to warming are more dependent on the temperature sensitivity of CUE than that of rB. Using the inversion‐derived parameters, we project that chronic soil warming at Harvard Forest over six decades will result in soil C gain of <1.0% on average (1st and 3rd quartiles: 3.0% loss and 10.5% gain) in the surface mineral horizon. Our results demonstrate that estimates of temperature sensitivity of microbial CUE and rB can be obtained and evaluated rigorously by integrating multidecadal datasets. This approach can potentially be applied in broader spatiotemporal scales to improve long‐term projections of soil C feedbacks to climate warming.     

罗浮栲林土壤微生物碳利用效率对短期氮添加的响应

作为调节土壤碳矿化过程的重要参数,微生物碳利用效率(CUE)对理解陆地生态系统中的碳循环至关重要。本研究在戴云山罗浮栲林设置对照(0 kg N·hm^-2·a^-1)、低氮(40 kg N·hm^-2·a^-1)和高氮(80 kg N·hm^-2·a^-1) 3个氮添加水平以模拟氮沉降,测定了表层(0～10 cm)土壤基本理化性质、有机碳组分、微生物生物量和酶活性;并利用¹⁸O标记水方法测定土壤微生物CUE,以更好地理解氮沉降加剧对微生物CUE的影响及其影响因素。结果表明: 短期氮添加显著降低了土壤微生物的呼吸速率、碳和氮获取酶活性,但显著增加了土壤微生物CUE。β-N-乙酰氨基酸葡糖苷酶(NAG)/微生物生物量碳(MBC)、微生物呼吸速率、β-葡萄糖苷酶(BG)/MBC、纤维素水解酶(CBH)/MBC和土壤有机碳含量是影响CUE的主要因素,且CUE与NAG/MBC、微生物呼吸速率、BG/MBC和CBH/MBC呈显著负相关,与土壤有机碳呈显著正相关。综上,短期氮添加导致土壤微生物获取碳和氮的成本降低,减少微生物呼吸,从而提高了土壤微生物CUE,这将有助于提高罗浮栲林土壤碳固存潜力。     

Rate of warming affects temperature sensitivity of anaerobic peat decomposition and greenhouse gas production

Temperature sensitivity of anaerobic carbon mineralization in wetlands remains poorly represented in most climate models and is especially unconstrained for warmer subtropical and tropical systems which account for a large proportion of global methane emissions. Several studies of experimental warming have documented thermal acclimation of soil respiration involving adjustments in microbial physiology or carbon use efficiency (CUE), with an initial decline in CUE with warming followed by a partial recovery in CUE at a later stage. The variable CUE implies that the rate of warming may impact microbial acclimation and the rate of carbon‐dioxide (CO₂) and methane (CH₄) production. Here, we assessed the effects of warming rate on the decomposition of subtropical peats, by applying either a large single‐step (10°C within a day) or a slow ramping (0.1°C/day for 100 days) temperature increase. The extent of thermal acclimation was tested by monitoring CO₂ and CH₄ production, CUE, and microbial biomass. Total gaseous C loss, CUE, and MBC were greater in the slow (ramp) warming treatment. However, greater values of CH₄–C:CO₂–C ratios lead to a greater global warming potential in the fast (step) warming treatment. The effect of gradual warming on decomposition was more pronounced in recalcitrant and nutrient‐limited soils. Stable carbon isotopes of CH₄ and CO₂ further indicated the possibility of different carbon processing pathways under the contrasting warming rates. Different responses in fast vs. slow warming treatment combined with different endpoints may indicate alternate pathways with long‐term consequences. Incorporations of experimental results into organic matter decomposition models suggest that parameter uncertainties in CUE and CH₄–C:CO₂–C ratios have a larger impact on long‐term soil organic carbon and global warming potential than uncertainty in model structure, and shows that particular rates of warming are central to understand the response of wetland soils to global climate change.     

Do biotic interactions modulate ecosystem functioning along stress gradients? Insights from semi-arid plant and biological soil crust communities

Climate change will exacerbate the degree of abiotic stress experienced by semi-arid ecosystems. While abiotic stress profoundly affects biotic interactions, their potential role as modulators of ecosystem responses to climate change is largely unknown. Using plants and biological soil crusts, we tested the relative importance of facilitative–competitive interactions and other community attributes (cover, species richness and species evenness) as drivers of ecosystem functioning along stress gradients in semi-arid Mediterranean ecosystems. Biotic interactions shifted from facilitation to competition along stress gradients driven by water availability and temperature. These changes were, however, dependent on the spatial scale and the community considered. We found little evidence to suggest that biotic interactions are a major direct influence upon indicators of ecosystem functioning (soil respiration, organic carbon, water-holding capacity, compaction and the activity of enzymes related to the carbon, nitrogen and phosphorus cycles) along stress gradients. However, attributes such as cover and species richness showed a direct effect on ecosystem functioning. Our results do not agree with predictions emphasizing that the importance of plant–plant interactions will be increased under climate change in dry environments, and indicate that reductions in the cover of plant and biological soil crust communities will negatively impact ecosystems under future climatic conditions.     

Environmental and stoichiometric controls on microbial carbon-use efficiency in soils

Carbon (C) metabolism is at the core of ecosystem function. Decomposers play a critical role in this metabolism as they drive soil C cycle by mineralizing organic matter to CO(2) . Their growth depends on the carbon-use efficiency (CUE), defined as the ratio of growth over C uptake. By definition, high CUE promotes growth and possibly C stabilization in soils, while low CUE favors respiration. Despite the importance of this variable, flexibility in CUE for terrestrial decomposers is still poorly characterized and is not represented in most biogeochemical models. Here, we synthesize the theoretical and empirical basis of changes in CUE across aquatic and terrestrial ecosystems, highlighting common patterns and hypothesizing changes in CUE under future climates. Both theoretical considerations and empirical evidence from aquatic organisms indicate that CUE decreases as temperature increases and nutrient availability decreases. More limited evidence shows a similar sensitivity of CUE to temperature and nutrient availability in terrestrial decomposers. Increasing CUE with improved nutrient availability might explain observed declines in respiration from fertilized stands, while decreased CUE with increasing temperature and plant C?:?N ratios might decrease soil C storage. Current biogeochemical models could be improved by accounting for these CUE responses along environmental and stoichiometric gradients.     

土壤微生物碳素利用效率研究进展

土壤微生物碳素利用效率(CUE)是指微生物将吸收的碳(C)转化为自身生物量C的效率,也称为微生物的生长效率。土壤微生物CUE是生态系统C循环中的重要生理生态学参数,影响着生态系统的C固持、周转、土壤矿化以及温室气体排放等过程。在全球环境变化背景下,认识土壤微生物CUE的变异及其影响机制,对于更好的认识生态系统C循环过程及其对全球变化的响应具有重要意义。概述了CUE的定义及其测定方法,重点综述和分析土壤微生物CUE的变异及影响因素取得的研究进展。基于现有研究的分析得出,土壤微生物CUE通常表示为微生物的生长与吸收的比值,分为基于微生物生长速率、微生物生物量、底物吸收速率和底物浓度变化等方法进行测定。土壤微生物CUE在0.2—0.8的范围内变化,这种变异主要受到来自热力学、生态环境因子、底物养分质量和有效性、化学计量平衡以及微生物群落组成的影响。今后土壤微生物CUE的研究应加强对微量代谢组分的定量分析,生物和环境要素交互影响的调控机理解析,以及微生物动态生理响应过程的碳循环模型优化。     

Respiration acclimation contributes to high carbon-use efficiency in a seasonally dry pine forest

Predictions of warming and drying in the Mediterranean and other regions require quantifying of such effects on ecosystem carbon dynamics and respiration. Long‐term effects can only be obtained from forests in which seasonal drought is a regular feature. We carried out measurements in a semiarid Pinus halepensis (Aleppo pine) forest of aboveground respiration rates of foliage, R_f, and stem, R_t over 3 years. Component respiration combined with ongoing biometric, net CO₂ flux [net ecosystem productivity (NEP)] and soil respiration measurements were scaled to the ecosystem level to estimate gross and net primary productivity (GPP, NPP) and carbon‐use efficiency (CUE=NPP/GPP) using 6 years data. GPP, NPP and NEP were, on average, 880, 350 and 211 g C m^?2 yr^?1, respectively. The above ground respiration made up half of total ecosystem respiration but CUE remained high at 0.4. Large seasonal variations in both R_f and R_t were not consistently correlated with seasonal temperature trends. Seasonal adjustments of respiration were observed in both the normalized rate (R₂₀) and short‐term temperature sensitivity (Q₁₀), resulting in low respiration rates during the hot, dry period. R_f in fully developed needles was highest over winter–spring, and foliage R₂₀ was correlated with photosynthesis over the year. Needle growth occurred over summer, with respiration rates in developing needles higher than the fully developed foliage at most times. R_t showed a distinct seasonal maximum in May irrespective of year, which was not correlated to the winter stem growth, but could be associated with phenological drivers such as carbohydrate re‐mobilization and cambial activity. We show that in a semiarid pine forest photosynthesis and stem growth peak in (wet) winter and leaf growth in (dry) summer, and associated adjustments of component respiration, dominated by those in R₂₀, minimize annual respiratory losses. This is likely a key for maintaining high CUE and ecosystem productivity similar to much wetter sites, and could lead to different predictions of the effect of warming and drying climate on productivity of pine forests than based on short‐term droughts.     

Interactive effects of warming and invertebrate grazing on the outcomes of competitive fungal interactions

Saprotrophic fungal community composition, determined by the outcomes of competitive mycelial interactions, represents a key determinant of woodland carbon and nutrient cycling. Atmospheric warming is predicted to drive changes in fungal community composition. Grazing by invertebrates can also exert selective pressures on fungal communities and alter the outcome of competitive fungal interactions; their potential to do so is determined by grazing intensity. Temperature regulates the abundance of soil collembola, but it remains unclear whether this will alter the top-down determination of fungal community composition. We use soil microcosms to explore the direct (via effects on interacting fungi) and indirect (by influencing top-down grazing pressures) effects of a 3 °C temperature increase on the outcomes of competitive interactions between cord-forming basidiomycete fungi. By differentially affecting the fungal growth rates, warming reversed the outcomes of specific competitive interactions. Collembola populations also increased at elevated temperature, and these larger, more active, populations exerted stronger grazing pressures. Consequently, grazing mitigated the effects of temperature on these interactions, restoring fungal communities to those recorded at ambient temperature. The interactive effects of biotic and abiotic factors are a key in determining the functional and ecological responses of microbial communities to climate change.     

Acclimation to temperature and temperature sensitivity of metabolism by ectomycorrhizal fungi

Ectomycorrhizal (ECM) fungi contribute significantly to ecosystem respiration, but little research has addressed the effect of temperature on ECM fungal respiration. Some plants have the ability to acclimate to temperature such that long‐term exposure to warmer conditions slows respiration at a given measurement temperature and long‐term exposure to cooler conditions increases respiration at a given measurement temperature. We examined acclimation to temperature and temperature sensitivity (Q₁₀) of respiration by ECM fungi by incubating them for a week at one of three temperatures and measuring respiration over a range of temperatures. Among the 12 ECM fungal isolates that were tested, Suillus intermedius, Cenococcum geophilum, and Lactarius cf. pubescens exhibited significant acclimation to temperature, exhibiting an average reduction in respiration of 20–45% when incubated at 23 °C compared with when incubated at 11 or 17 °C. The isolates differed significantly in their Q₁₀ values, which ranged from 1.67 to 2.56. We also found that half of the isolates significantly increased Q₁₀ with an increase in incubator temperature by an average of 15%. We conclude that substantial variation exists among ECM fungal isolates in their ability to acclimate to temperature and in their sensitivity to temperature. As soil temperatures increase, ECM fungi that acclimate may require less carbon from their host plants than fungi that do not acclimate. The ability of some ECM fungi to acclimate may partially ameliorate the anticipated positive feedback between soil respiration and temperature.