Thermal acclimation of shoot respiration in an Arctic woody plant species subjected to 22 years of warming and altered nutrient supply

Despite concern about the status of carbon (C) in the Arctic tundra, there is currently little information on how plant respiration varies in response to environmental change in this region. We quantified the impact of long‐term nitrogen (N) and phosphorus (P) treatments and greenhouse warming on the short‐term temperature (T) response and sensitivity of leaf respiration (R), the high‐T threshold of R, and associated traits in shoots of the Arctic shrub Betula nana in experimental plots at Toolik Lake, Alaska. Respiration only acclimated to greenhouse warming in plots provided with both N and P (resulting in a ~30% reduction in carbon efflux in shoots measured at 10 and 20 °C), suggesting a nutrient dependence of metabolic adjustment. Neither greenhouse nor N+P treatments impacted on the respiratory sensitivity to T (Q₁₀); overall, Q₁₀ values decreased with increasing measuring T, from ~3.0 at 5 °C to ~1.5 at 35 °C. New high‐resolution measurements of R across a range of measuring Ts (25–70 °C) yielded insights into the T at which maximal rates of R occurred (T_max). Although growth temperature did not affect T_max, N+P fertilization increased T_max values ~5 °C, from 53 to 58 °C. N+P fertilized shoots exhibited greater rates of R than nonfertilized shoots, with this effect diminishing under greenhouse warming. Collectively, our results highlight the nutrient dependence of thermal acclimation of leaf R in B. nana, suggesting that the metabolic efficiency allowed via thermal acclimation may be impaired at current levels of soil nutrient availability. This finding has important implications for predicting carbon fluxes in Arctic ecosystems, particularly if soil N and P become more abundant in the future as the tundra warms.     

Differential physiological responses to environmental change promote woody shrub expansion

Direct and indirect effects of warming are increasingly modifying the carbon-rich vegetation and soils of the Arctic tundra, with important implications for the terrestrial carbon cycle. Understanding the biological and environmental influences on the processes that regulate foliar carbon cycling in tundra species is essential for predicting the future terrestrial carbon balance in this region. To determine the effect of climate change impacts on gas exchange in tundra, we quantified foliar photosynthesis (A_net), respiration in the dark and light (R_D and R_L, determined using the Kok method), photorespiration (PR), carbon gain efficiency (CGE, the ratio of photosynthetic CO₂ uptake to total CO₂ exchange of photosynthesis, PR, and respiration), and leaf traits of three dominant species – Betula nana, a woody shrub; Eriophorum vaginatum, a graminoid; and Rubus chamaemorus, a forb – grown under long-term warming and fertilization treatments since 1989 at Toolik Lake, Alaska. Under warming, B. nana exhibited the highest rates of A_net and strongest light inhibition of respiration, increasing CGE nearly 50% compared with leaves grown in ambient conditions, which corresponded to a 52% increase in relative abundance. Gas exchange did not shift under fertilization in B. nana despite increases in leaf N and P and near-complete dominance at the community scale, suggesting a morphological rather than physiological response. Rubus chamaemorus, exhibited minimal shifts in foliar gas exchange, and responded similarly to B. nana under treatment conditions. By contrast, E. vaginatum, did not significantly alter its gas exchange physiology under treatments and exhibited dramatic decreases in relative cover (warming: −19.7%; fertilization: −79.7%; warming with fertilization: −91.1%). Our findings suggest a foliar physiological advantage in the woody shrub B. nana that is further mediated by warming and increased soil nutrient availability, which may facilitate shrub expansion and in turn alter the terrestrial carbon cycle in future tundra environments.     

Contrasting thermal acclimation of leaf dark respiration and photosynthesis of Antarctic vascular plant species exposed to nocturnal warming

Leaf respiration and photosynthesis will respond differently to an increase in temperature during night, which can be more relevant in sensitive ecosystems such as Antarctica. We postulate that the plant species able to colonize the Antarctic Peninsula – Colobanthus quitensis (Kunth) Bartl. and Deschampsia antarctica Desv. – are able to acclimate their foliar respiration and to maintain photosynthesis under nocturnal warming to sustain a positive foliar carbon balance. We conducted a laboratory experiment to evaluate the effect of time of day (day and night) and nocturnal warming on dark respiration. Short (E₀ and Q₁₀) and long‐term acclimation of respiration, leaf carbohydrates, photosynthesis (A_sat) and foliar carbon balance (R/A) were evaluated. The results suggest that the two species have differential thermal acclimation respiration, where D. antarctica showed more thermosensitivity to short‐term changes in temperature than C. quitensis. Experimental nocturnal warming affected respiration at daytime differentially between the two species, with a significant increase of R₁₀ and A_sat in D. antarctica, while no changes on respiration were observed in C. quitensis. Long thermal treatments of the plants indicated that nocturnal but not diurnal respiration could acclimate in both species, and to a greater extent in C. quitensis. Non‐structural carbohydrates were related with respiration in C. quitensis but not in D. antarctica, suggesting that respiration in the former species is likely controlled by total soluble sugars and starch during day and night, respectively. Finally, foliar carbon balance was differentially improved under warming conditions in Antarctic plants by different mechanisms, with C. quitensis deploying respiratory acclimation, while D. antarctica increased its A_sat.     

Thermal acclimation of leaf and root respiration: an investigation comparing inherently fast- and slow-growing plant species

We investigated the extent to which leaf and root respiration (R) differ in their response to short‐ and long‐term changes in temperature in several contrasting plant species (herbs, grasses, shrubs and trees) that differ in inherent relative growth rate (RGR, increase in mass per unit starting mass and time). Two experiments were conducted using hydroponically grown plants. In the long‐term (LT) acclimation experiment, 16 species were grown at constant 18, 23 and 28 °C. In the short‐term (ST) acclimation experiment, 9 of those species were grown at 25/20 °C (day/night) and then shifted to a 15/10 °C for 7 days. Short‐term Q₁₀ values (proportional change in R per 10 °C) and the degree of acclimation to longer‐term changes in temperature were compared. The effect of growth temperature on root and leaf soluble sugar and nitrogen concentrations was examined. Light‐saturated photosynthesis (A_sat) was also measured in the LT acclimation experiment. Our results show that Q₁₀ values and the degree of acclimation are highly variable amongst species and that roots exhibit lower Q₁₀ values than leaves over the 15–25 °C measurement temperature range. Differences in RGR or concentrations of soluble sugars/nitrogen could not account for the inter‐specific differences in the Q₁₀ or degree of acclimation. There were no systematic differences in the ability of roots and leaves to acclimate when plants developed under contrasting temperatures (LT acclimation). However, acclimation was greater in both leaves and roots that developed at the growth temperature (LT acclimation) than in pre‐existing leaves and roots shifted from one temperature to another (ST acclimation). The balance between leaf R and A_sat was maintained in plants grown at different temperatures, regardless of their inherent relative growth rate. We conclude that there is tight coupling between the respiratory acclimation and the temperature under which leaves and roots developed and that acclimation plays an important role in determining the relationship between respiration and photosynthesis.     

Coupling of respiration, nitrogen, and sugars underlies convergent temperature acclimation in Pinus banksiana across wide-ranging sites and populations

Patterns and mechanisms of short‐term temperature acclimation and long‐term climatic adaptation of respiration among intraspecific populations are poorly understood, but both are potentially important in constraining respiratory carbon flux to climate warming across large geographic scales, as well as influencing the metabolic fitness of populations. Herein we report on leaf dark respiration of 33‐year‐old trees of jack pine (Pinus banksiana Lamb.) grown in three contrasting North American common gardens (0.9, 4.6, and 7.9 °C, mean annual temperature) comprised of identical populations of wide‐ranging geographic origins. We tested whether respiration rates in this evergreen conifer acclimate to prevailing ambient air temperatures and differ among populations. At each of the common gardens, observed population differences in respiration rates measured at a standard temperature (20 °C) were comparatively small and largely unrelated to climate of seed‐source origin. In contrast, respiration in all populations exhibited seasonal acclimation at all sites. Specific respiration rates at 20 °C inversely tracked seasonal variation in ambient air temperature, increasing with cooler temperatures in fall and declining with warmer temperatures in spring and summer. Such responses were similar among populations and sites, thus providing a general predictive equation regarding temperature acclimation of respiration for the species. Temperature acclimation was associated with variation in nitrogen (N) and soluble carbohydrate concentrations, supporting a joint enzyme and substrate‐based model of respiratory acclimation. Regression analyses revealed convergent relationships between respiration and the combination of needle N and soluble carbohydrate concentrations and between N‐based respiration (R_N, μmol mol N^{? 1} s^{? 1}) and soluble carbohydrate concentrations, providing evidence for general predictive relationships across geographically diverse populations, seasons, and sites. Overall, these findings demonstrate that seasonal acclimation of respiration modulates rates of foliar respiratory carbon flux in a widely distributed evergreen species, and does so in a predictable way. Genetic differences in specific respiration rate appear less important than temperature acclimation in downregulating respiratory carbon fluxes with climate warming across wide‐ranging sites.     

Long‐term experimental manipulation of climate alters the ectomycorrhizal community of Betula nana in Arctic tundra

Climate warming is leading to shrub expansion in Arctic tundra. Shrubs form ectomycorrhizal (ECM) associations with soil fungi that are central to ecosystem carbon balance as determinants of plant community structure and as decomposers of soil organic matter. To assess potential climate change impacts on ECM communities, we analysed fungal internal transcribed spacer sequences from ECM root tips of the dominant tundra shrub Betula nana growing in treatments plots that had received long‐term warming by greenhouses and/or fertilization as part of the Arctic Long‐Term Ecological Research experiment at Toolik Lake Alaska, USA. We demonstrate opposing effects of long‐term warming and fertilization treatments on ECM fungal diversity; with warming increasing and fertilization reducing the diversity of ECM communities. We show that warming leads to a significant increase in high biomass fungi with proteolytic capacity, especially Cortinarius spp., and a reduction of fungi with high affinities for labile N, especially Russula spp. In contrast, fertilization treatments led to relatively small changes in the composition of the ECM community, but increased the abundance of saprotrophs. Our data suggest that warming profoundly alters nutrient cycling in tundra, and may facilitate the expansion of B. nana through the formation of mycorrhizal networks of larger size.     

Plastic and genetic responses of a common sedge to warming have contrasting effects on carbon cycle processes

Climate warming affects plant physiology through genetic adaptation and phenotypic plasticity, but little is known about how these mechanisms influence ecosystem processes. We used three elevation gradients and a reciprocal transplant experiment to show that temperature causes genetic change in the sedge Eriophorum vaginatum. We demonstrate that plants originating from warmer climate produce fewer secondary compounds, grow faster and accelerate carbon dioxide (CO₂) release to the atmosphere. However, warmer climate also caused plasticity in E. vaginatum, inhibiting nitrogen metabolism, photosynthesis and growth and slowing CO₂ release into the atmosphere. Genetic differentiation and plasticity in E. vaginatum thus had opposing effects on CO₂ fluxes, suggesting that warming over many generations may buffer, or reverse, the short‐term influence of this species over carbon cycle processes. Our findings demonstrate the capacity for plant evolution to impact ecosystem processes, and reveal a further mechanism through which plants will shape ecosystem responses to climate change.     

Effect of growth temperature on photosynthetic capacity and respiration in three ecotypes of Eriophorum vaginatum

Ecotypic differentiation in the tussock‐forming sedge Eriophorum vaginatum has led to the development of populations that are locally adapted to climate in Alaska's moist tussock tundra. As a foundation species, E. vaginatum plays a central role in providing topographic and microclimatic variation essential to these ecosystems, but a changing climate could diminish the importance of this species. As Arctic temperatures have increased, there is evidence of adaptational lag in E. vaginatum, as locally adapted ecotypes now exhibit reduced population growth rates. Whether there is a physiological underpinning to adaptational lag is unknown. Accordingly, this possibility was investigated in reciprocal transplant gardens. Tussocks of E. vaginatum from sites separated by ~1° latitude (Coldfoot: 67°15′N, Toolik Lake: 68°37′, Sagwon: 69°25′) were transplanted into the Toolik Lake and Sagwon sites and exposed to either an ambient or an experimental warming treatment. Five tussocks pertreatment combination were measured at each garden to determine photosynthetic capacity (i.e., V_cmax and J_max) and dark respiration rate (R_d) at measurement temperatures of 15, 20, and 25°C. Photosynthetic enhancements or homeostasis were observed for all ecotypes at both gardens under increased growth temperature, indicating no negative effect of elevated temperature on photosynthetic capacity. Further, no evidence of thermal acclimation in R_d was observed for any ecotype, and there was little evidence of ecotypic variation in R_d. As such, no physiological contribution to adaptational lag was observed given the increase in growth temperature (up to ~2°C) provided by this study. Despite neutral to positive effects of increased growth temperature on photosynthesis in E. vaginatum, it appears to confer no lasting advantage to the species.     

Response of dark respiration to temperature in Eriophorum vaginatum from a 30-year-old transplant experiment in Alaska

Background: In the Arctic region, temperature increases are expected to be greater under anticipated climate change than the global average. Understanding how dark respiration (R_d) of common Arctic plant species acclimates to changes in the environment is therefore important for predicting changes to the Arctic carbon balance.

Aims: The aim of this study is to investigate the influence of genotype and growing environment on R_d, the temperature response (Q₁₀) of R_d, and foliar N (N_leaf) of the Arctic sedge Eriophorum vaginatum.

Methods: We measured R_d, and determined its Q₁₀ and N_leaf of E. vaginatum populations that were reciprocally transplanted 30 years previously along a latitudinal transect of 370 km in northern Alaska.

Results: R_d and Q₁₀ did not differ among populations (ecotypes) of E. vaginatum, but the local environment had a significant effect on both variables. R_d as well as N_leaf was higher in northern, colder sites, while Q₁₀ was lower there.

Conclusions: R_d in the different populations of E. vaginatum is a very plastic trait and controlled by growing environment, as is N_leaf. The lower Q₁₀ values in the northern sites were most likely a consequence of substrate inhibition of R_d at higher temperatures.     

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.     

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.     

Climate change alters leaf anatomy,but has no effects on volatile emissions from arctic plants

Biogenic volatile organic compound (BVOC) emissions are expected to change substantially because of the rapid advancement of climate change in the Arctic. BVOC emission changes can feed back both positively and negatively on climate warming. We investigated the effects of elevated temperature and shading on BVOC emissions from arctic plant species Empetrum hermaphroditum, Cassiope tetragona, Betula nana and Salix arctica. Measurements were performed in situ in long‐term field experiments in subarctic and high Arctic using a dynamic enclosure system and collection of BVOCs into adsorbent cartridges analysed by gas chromatography‐mass spectrometry. In order to assess whether the treatments had resulted in anatomical adaptations, we additionally examined leaf anatomy using light microscopy and scanning electron microscopy. Against expectations based on the known temperature and light‐dependency of BVOC emissions, the emissions were barely affected by the treatments. In contrast, leaf anatomy of the studied plants was significantly altered in response to the treatments, and these responses appear to differ from species found at lower latitudes. We suggest that leaf anatomical acclimation may partially explain the lacking treatment effects on BVOC emissions at plant shoot‐level. However, more studies are needed to unravel why BVOC emission responses in arctic plants differ from temperate species.     

Evergreen leaf respiration acclimates to long-term nocturnal warming under field conditions

Acclimation of plant respiration rates (R) to climate warming is highly variable and many results appear contradictory. We tested the recently suggested hypotheses that pre‐existing, long‐lived leaves should exhibit a relatively limited ability for R to acclimate to climate warming, and that acclimation would occur via changes in the short‐term temperature sensitivity of respiration. Seedlings of a subalpine, evergreen tree species (Eucalyptus pauciflora) were grown under naturally fluctuating conditions within its natural distribution. We used a free air temperature increase (FATI) system of infra‐red ceramic lamps to raise night‐time leaf temperatures by 0.3±0.1, 1.3±0.1, and 2.2±0.1 °C above ambient for 1 year. Light‐saturated assimilation rates and plant growth did not change with nocturnal FATI treatments. Leaf R measured at prevailing temperatures did not differ between FATI treatments. Within each FATI treatment, nocturnal leaf R was highly sensitive to artificial temperature changes within minutes, and also correlated strongly with natural nocturnal and seasonal temperature variation. The corresponding values of Q₁₀ of R varied according to time scale of measurements, but did not vary between FATI treatments. Instead, acclimation of R to nocturnal FATI occurred through changes in the base rate of respiration.     

Stomatal acclimation to vapour pressure deficit doubles transpiration of small tree seedlings with warming

Future climate change is expected to increase temperature (T) and atmospheric vapour pressure deficit (VPD) in many regions, but the effect of persistent warming on plant stomatal behaviour is highly uncertain. We investigated the effect of experimental warming of 1.9–5.1 °C and increased VPD of 0.5–1.3 kPa on transpiration and stomatal conductance (g_s) of tree seedlings in the temperate forest understory (Duke Forest, North Carolina, USA). We observed peaked responses of transpiration to VPD in all seedlings, and the optimum VPD for transpiration (D_opt) shifted proportionally with increasing chamber VPD. Warming increased mean water use of Carya by 140% and Quercus by 150%, but had no significant effect on water use of Acer. Increased water use of ring‐porous species was attributed to (1) higher air T and (2) stomatal acclimation to VPD resulting in higher g_s and more sensitive stomata, and thereby less efficient water use. Stomatal acclimation maintained homeostasis of leaf T and carbon gain despite increased VPD, revealing that short‐term stomatal responses to VPD may not be representative of long‐term exposure. Acclimation responses differ from expectations of decreasing g_s with increasing VPD and may necessitate revision of current models based on this assumption.     

Short‐term acclimation to warmer temperatures accelerates leaf carbon exchange processes across plant types

While temperature responses of photosynthesis and plant respiration are known to acclimate over time in many species, few studies have been designed to directly compare process‐level differences in acclimation capacity among plant types. We assessed short‐term (7 day) temperature acclimation of the maximum rate of Rubisco carboxylation (V_cmax), the maximum rate of electron transport (J_max), the maximum rate of phosphoenolpyruvate carboxylase carboxylation (V_pmax), and foliar dark respiration (R_d) in 22 plant species that varied in lifespan (annual and perennial), photosynthetic pathway (C₃ and C₄), and climate of origin (tropical and nontropical) grown under fertilized, well‐watered conditions. In general, acclimation to warmer temperatures increased the rate of each process. The relative increase in different photosynthetic processes varied by plant type, with C₃ species tending to preferentially accelerate CO₂‐limited photosynthetic processes and respiration and C₄ species tending to preferentially accelerate light‐limited photosynthetic processes under warmer conditions. R_d acclimation to warmer temperatures caused a reduction in temperature sensitivity that resulted in slower rates at high leaf temperatures. R_d acclimation was similar across plant types. These results suggest that temperature acclimation of the biochemical processes that underlie plant carbon exchange is common across different plant types, but that acclimation to warmer temperatures tends to have a relatively greater positive effect on the processes most limiting to carbon assimilation, which differ by plant type. The acclimation responses observed here suggest that warmer conditions should lead to increased rates of carbon assimilation when water and nutrients are not limiting.     

The response of heterotrophic CO2 flux to soil warming

In a forest ecosystem at steady state, net carbon (C) assimilation by plants and C loss through soil and litter decomposition by heterotrophic organisms are balanced. However, a perturbation to the system, such as increased mean soil temperature, will lead to faster decay, enhancing CO₂ release from decomposers, and thus upsetting the balance. Recent in situ experiments have indicated that the stimulation of soil respiration following a step increase in annual average soil temperature declines over time. One possible explanation for this decline may be changes in substrate availability. This hypothesis is examined by using the ecosystem model G'DAY, which simulates C and nitrogen (N) dynamics in plants and soil. We applied the model to observations from a soil‐warming experiment in a Norway spruce (Picea abies (L.) Karst.) stand by simulating a step increase of soil temperature. The model provided a good qualitative reproduction of the observed reduction of heterotrophic respiration (R_h) under sustained warming. The simulations showed how the combined effects of faster turnover and reduced substrate availability lead to a transient increase of R_h. The simulated annual increase in R_h from soil was 60% in the first year after perturbation but decreased to 30% after a decade. One conclusion from the analysis of the simulations is that R_h can decrease even though the temperature response function for decomposition remains unchanged. G'DAY suggests that acclimation of R_h to soil warming is partly an effect of substrate depletion of labile C pools during the first decade of warming as a result of accelerated rates of mineralization. The response is attributed mainly to changing levels of C in pools with short time constants, reflecting the importance of high‐quality soil C fractions. Changes of the structure or physiology of the decomposer community were not invoked. Therefore, it becomes a question of definition whether the simulated dynamics of the declining response of CO₂ release to the warming should be named acclimation or seen as a natural part of the system dynamics.     

Contrasting effects of long term versus short-term nitrogen addition on photosynthesis and respiration in the Arctic

We examined the effects of short (<1–4 years) and long-term (22 years) nitrogen (N) and/or phosphorus (P) addition on the foliar CO₂ exchange parameters of the Arctic species Betula nana and Eriophorum vaginatum in northern Alaska. Measured variables included: the carboxylation efficiency of Rubisco (V_cmax), electron transport capacity (J_max), dark respiration (R_d), chlorophyll a and b content (Chl), and total foliar N (N). For both B. nana and E. vaginatum, foliar N increased by 20–50 % as a consequence of 1–22 years of fertilisation, respectively, and for B. nana foliar N increase was consistent throughout the whole canopy. However, despite this large increase in foliar N, no significant changes in V_cmax and J_max were observed. In contrast, R_d was significantly higher (>25 %) in both species after 22 years of N addition, but not in the shorter-term treatments. Surprisingly, Chl only increased in both species the first year of fertilisation (i.e. the first season of nutrients applied), but not in the longer-term treatments. These results imply that: (1) under current (low) N availability, these Arctic species either already optimize their photosynthetic capacity per leaf area, or are limited by other nutrients; (2) observed increases in Arctic NEE and GPP with increased nutrient availability are caused by structural changes like increased leaf area index, rather than increased foliar photosynthetic capacity and (3) short-term effects (1–4 years) of nutrient addition cannot always be extrapolated to a larger time scale, which emphasizes the importance of long-term ecological experiments.     

Apparent thermal acclimation of soil heterotrophic respiration mainly mediated by substrate availability

Multiple lines of existing evidence suggest that increasing CO₂ emission from soils in response to rising temperature could accelerate global warming. However, in experimental studies, the initial positive response of soil heterotrophic respiration (R_H) to warming often weakens over time (referred to apparent thermal acclimation). If the decreased R_H is driven by thermal adaptation of soil microbial community, the potential for soil carbon (C) losses would be reduced substantially. In the meanwhile, the response could equally be caused by substrate depletion, and would then reflect the gradual loss of soil C. To address uncertainties regarding the causes of apparent thermal acclimation, we carried out sterilization and inoculation experiments using the soil samples from an alpine meadow with 6 years of warming and nitrogen (N) addition. We demonstrate that substrate depletion, rather than microbial adaptation, determined the response of R_H to long-term warming. Furthermore, N addition appeared to alleviate the apparent acclimation of R_H to warming. Our study provides strong empirical support for substrate availability being the cause of the apparent acclimation of soil microbial respiration to temperature. Thus, these mechanistic insights could facilitate efforts of biogeochemical modeling to accurately project soil C stocks in the future climate.     

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.