Chronic warming and dry soils limit carbon uptake and growth despite a longer growing season in beech and oak.

Progressively warmer and drier climatic conditions impact tree phenology and carbon cycling with large consequences for forest carbon balance. However, it remains unclear how individual impacts of warming and drier soils differ from their combined effects and how species interactions modulate tree responses. Using mesocosms, we assessed the multiyear impact of continuous air warming and lower soil moisture alone or in combination on phenology, leaf-level photosynthesis, nonstructural carbohydrate concentrations, and aboveground growth of young European beech (Fagus sylvatica L.) and Downy oak (Quercus pubescens Willd.) trees. We further tested how species interactions (in monocultures and in mixtures) modulated these effects. Warming prolonged the growing season of both species but reduced growth in oak. In contrast, lower moisture did not impact phenology but reduced carbon assimilation and growth in both species. Combined impacts of warming and drier soils did not differ from their single effects. Under warmer and drier conditions, performances of both species were enhanced in mixtures compared to monocultures. Our work revealed that higher temperature and lower soil moisture have contrasting impacts on phenology vs. leaf-level assimilation and growth, with the former being driven by temperature and the latter by moisture. Furthermore, we showed a compensation in the negative impacts of chronic heat and drought by tree species interactions.

Drought resistance and resilience of rhizosphere communities in forest soils from the cellular to ecosystem scale - insights from 13C pulse labeling.

The link between above- and belowground communities is a key uncertainty in drought and rewetting effects on forest carbon (C) cycle. In young beech model ecosystems and mature naturally dry pine forest exposed to 15-yr-long irrigation, we performed 13C pulse labeling experiments, one during drought and one 2 wk after rewetting, tracing tree assimilates into rhizosphere communities. The 13C pulses applied in tree crowns reached soil microbial communities of the young and mature forests one and 4 d later, respectively. Drought decreased the transfer of labeled assimilates relative to the irrigation treatment. The 13C label in phospholipid fatty acids (PLFAs) indicated greater drought reduction of assimilate incorporation by fungi (-85%) than by gram-positive (-43%) and gram-negative bacteria (-58%). 13C label incorporation was more strongly reduced for PLFAs (cell membrane) than for microbial cytoplasm extracted by chloroform. This suggests that fresh rhizodeposits are predominantly used for osmoregulation or storage under drought, at the expense of new cell formation. Two weeks after rewetting, 13C enrichment in PLFAs was greater in previously dry than in continuously moist soils. Drought and rewetting effects were greater in beech systems than in pine forest. Belowground C allocation and rhizosphere communities are highly resilient to drought.

Twenty years of irrigation acclimation is driven by denser canopies and not by plasticity in twig- and needle-level hydraulics in a Pinus sylvestris forest.

Climate change is predicted to increase atmospheric vapor pressure deficit, exacerbating soil drought, and thus enhancing tree evaporative demand and mortality. Yet, few studies have addressed the longer-term drought acclimation strategy of trees, particularly the importance of morphological versus hydraulic plasticity. Using a long-term (20 years) irrigation experiment in a natural forest, we investigated the acclimation of Scots pine (Pinus sylvestris) morpho-anatomical traits (stomatal anatomy and crown density) and hydraulic traits (leaf water potential, vulnerability to cavitation (Ψ50), specific hydraulic conductivity (Ks), and tree water deficit) to prolonged changes in soil moisture. We found that low water availability reduced twig water potential and increased tree water deficit during the growing season. Still, the trees showed limited adjustments in most branch-level hydraulic traits (Ψ50 and Ks) and needle anatomy. In contrast, trees acclimated to prolonged irrigation by increasing their crown density and hence the canopy water demand. This study demonstrates that despite substantial canopy adjustments, P. sylvestris may be vulnerable to extreme droughts because of limited adjustment potential in its hydraulic system. While sparser canopies reduce water demand, such shifts take decades to occur under chronic water deficits and might not mitigate short-term extreme drought events.

Finding balance: Tree-ring isotopes differentiate between acclimation and stress-induced imbalance in a long-term irrigation experiment.

Scots pine (Pinus sylvestris L.) is a common European tree species, and understanding its acclimation to the rapidly changing climate through physiological, biochemical or structural adjustments is vital for predicting future growth. We investigated a long-term irrigation experiment at a naturally dry forest in Switzerland, comparing Scots pine trees that have been continuously irrigated for 17 years (irrigated) with those for which irrigation was interrupted after 10 years (stop) and non-irrigated trees (control), using tree growth, xylogenesis, wood anatomy, and carbon, oxygen and hydrogen stable isotope measurements in the water, sugars and cellulose of plant tissues. The dendrochronological analyses highlighted three distinct acclimation phases to the treatments: irrigated trees experienced (i) a significant growth increase in the first 4 years of treatment, (ii) high growth rates but with a declining trend in the following 8 years and finally (iii) a regression to pre-irrigation growth rates, suggesting the development of a new growth limitation (i.e. acclimation). The introduction of the stop treatment resulted in further growth reductions to below-control levels during the third phase. Irrigated trees showed longer growth periods and lower tree-ring δ13 C values, reflecting lower stomatal restrictions than control trees. Their strong tree-ring δ18 O and δ2 H (O-H) relationship reflected the hydrological signature similarly to the control. On the contrary, the stop trees had lower growth rates, conservative wood anatomical traits, and a weak O-H relationship, indicating a physiological imbalance. Tree vitality (identified by crown transparency) significantly modulated growth, wood anatomical traits and tree-ring δ13 C, with low-vitality trees of all treatments performing similarly regardless of water availability. We thus provide quantitative indicators for assessing physiological imbalance and tree acclimation after environmental stresses. We also show that tree vitality is crucial in shaping such responses. These findings are fundamental for the early assessment of ecosystem imbalances and decline under climate change.

Author Correction: Environment and host as large-scale controls of ectomycorrhizal fungi.

Change history: In the HTML version of this Article, author 'Filipa Cox' had no affiliation in the author list, although she was correctly associated with affiliation 3 in the PDF. In addition, the blue circles for 'oak' were missing from Extended Data Fig. 1. These errors have been corrected online.

Environment and host as large-scale controls of ectomycorrhizal fungi.

Explaining the large-scale diversity of soil organisms that drive biogeochemical processes-and their responses to environmental change-is critical. However, identifying consistent drivers of belowground diversity and abundance for some soil organisms at large spatial scales remains problematic. Here we investigate a major guild, the ectomycorrhizal fungi, across European forests at a spatial scale and resolution that is-to our knowledge-unprecedented, to explore key biotic and abiotic predictors of ectomycorrhizal diversity and to identify dominant responses and thresholds for change across complex environmental gradients. We show the effect of 38 host, environment, climate and geographical variables on ectomycorrhizal diversity, and define thresholds of community change for key variables. We quantify host specificity and reveal plasticity in functional traits involved in soil foraging across gradients. We conclude that environmental and host factors explain most of the variation in ectomycorrhizal diversity, that the environmental thresholds used as major ecosystem assessment tools need adjustment and that the importance of belowground specificity and plasticity has previously been underappreciated.

Absence of canopy temperature variation despite stomatal adjustment in Pinus sylvestris under multidecadal soil moisture manipulation.

Global warming and droughts push forests closer to their thermal limits, altering tree carbon uptake and growth. To prevent critical overheating, trees can adjust their thermotolerance (Tcrit ), temperature and photosynthetic optima (Topt and Aopt ), and canopy temperature (Tcan ) to stay below damaging thresholds. However, we lack an understanding of how soil droughts affect photosynthetic thermal plasticity and Tcan regulation. In this study, we measured the effect of soil moisture on the seasonal and diurnal dynamics of net photosynthesis (A), stomatal conductance (gs ), and Tcan , as well as the thermal plasticity of photosynthesis (Tcrit , Topt , and Aopt ), over the course of 1 yr using a long-term irrigation experiment in a drought-prone Pinus sylvestris forest in Switzerland. Irrigation resulted in higher needle-level A, gs , Topt , and Aopt compared with naturally drought-exposed trees. No daily or seasonal differences in Tcan were observed between treatments. Trees operated below their thermal thresholds (Tcrit ), independently of soil moisture content. Despite strong Tcan and Tair coupling, we provide evidence that drought reduces trees' temperature optimum due to a substantial reduction of gs during warm and dry periods of the year. These findings provide important insights regarding the effects of soil drought on the thermal tolerance of P. sylvestris.

Rhizosphere activity in an old-growth forest reacts rapidly to changes in soil moisture and shapes whole-tree carbon allocation.

Drought alters carbon (C) allocation within trees, thereby impairing tree growth. Recovery of root and leaf functioning and prioritized C supply to sink tissues after drought may compensate for drought-induced reduction of assimilation and growth. It remains unclear if C allocation to sink tissues during and following drought is controlled by altered sink metabolic activities or by the availability of new assimilates. Understanding such mechanisms is required to predict forests' resilience to a changing climate. We investigated the impact of drought and drought release on C allocation in a 100-y-old Scots pine forest. We applied 13CO2 pulse labeling to naturally dry control and long-term irrigated trees and tracked the fate of the label in above- and belowground C pools and fluxes. Allocation of new assimilates belowground was ca. 53% lower under nonirrigated conditions. A short rainfall event, which led to a temporary increase in the soil water content (SWC) in the topsoil, strongly increased the amounts of C transported belowground in the nonirrigated plots to values comparable to those in the irrigated plots. This switch in allocation patterns was congruent with a tipping point at around 15% SWC in the response of the respiratory activity of soil microbes. These results indicate that the metabolic sink activity in the rhizosphere and its modulation by soil moisture can drive C allocation within adult trees and ecosystems. Even a subtle increase in soil moisture can lead to a rapid recovery of belowground functions that in turn affects the direction of C transport in trees.

Impact of warmer and drier conditions on tree photosynthetic properties and the role of species interactions.

Increased temperature and prolonged soil moisture reduction have distinct impacts on tree photosynthetic properties. Yet, our knowledge of their combined effect is limited. Moreover, how species interactions alter photosynthetic responses to warming and drought remains unclear. Using mesocosms, we studied how photosynthetic properties of European beech and downy oak were impacted by multi-year warming and soil moisture reduction alone or combined, and how species interactions (intra- vs inter-specific interactions) modulated these effects. Warming of +5°C enhanced photosynthetic properties in oak but not beech, while moisture reduction decreased them in both species. Combined warming and moisture reduction reduced photosynthetic properties for both species, but no exacerbated effects were observed. Oak was less impacted by combined warming and limited moisture when interacting with beech than in intra-specific stands. For beech, species interactions had no impact on the photosynthetic responses to warming and moisture reduction, alone or combined. Warming had either no or beneficial effects on the photosynthetic properties, while moisture reduction and their combined effects strongly reduced photosynthetic responses. However, inter-specific interactions mitigated the adverse impacts of combined warming and drought in oak, thereby highlighting the need to deepen our understanding of the role of species interactions under climate change.

Drought reduces water uptake in beech from the drying topsoil, but no compensatory uptake occurs from deeper soil layers.

The intensity and frequency of droughts events are projected to increase in future with expected adverse effects for forests. Thus, information on the dynamics of tree water uptake from different soil layers during and after drought is crucial. We applied an in situ water isotopologue monitoring system to determine the oxygen isotope composition in soil and xylem water of European beech with a 2-h resolution together with measurements of soil water content, transpiration and tree water deficit. Using a Bayesian isotope mixing model, we inferred the relative and absolute contribution of water from four different soil layers to tree water use. Beech took up more than 50% of its water from the uppermost 5 cm soil layer at the beginning of the 2018 drought, but then reduced absolute water uptake from the drying topsoil by 84%. The trees were not able to quantitatively compensate for restricted topsoil water availability by additional uptake from deeper soil layers, which is related to the fine root depth distribution. Absolute water uptake from the topsoil was restored to pre-drought levels within 3 wk after rewetting. These uptake patterns help to explain both the drought sensitivity of beech and its high recovery potential after drought release.

Drought effects on volatile organic compound emissions from Scots pine stems.

Tree stems have been identified as sources of volatile organic compounds (VOCs) that play important roles in tree defence and atmospheric chemistry. Yet, we lack understanding on the magnitude and environmental drivers of stem VOC emissions in various forest ecosystems. Due to the increasing importance of extreme drought, we studied drought effects on the VOC emissions from mature Scots pine (Pinus sylvestris L.) stems. We measured monoterpenes, acetone, acetaldehyde and methanol emissions with custom-made stem chambers, online PTR-MS and adsorbent sampling in a drought-prone forest over the hot-dry summer of 2018 and compared the emission rates and dynamics between trees in naturally dry conditions and under long-term irrigation (drought release). The pine stems were significant monoterpene sources. The stem monoterpene emissions potentially originated from resin, based on their similar monoterpene spectra. The emission dynamics of all VOCs followed temperature at a daily scale, but monoterpene and acetaldehyde emission rates decreased nonlinearly with drought over the summer. Despite the dry conditions, large peaks of monoterpene, acetaldehyde and acetone emissions occurred in late summer potentially due to abiotic or biotic stressors. Our results highlight the potential importance of stem emissions in the ecosystem VOC budget, encouraging further studies in diverse environments.

Photosynthetic acclimation and sensitivity to short- and long-term environmental changes in a drought-prone forest.

Future climate will be characterized by an increase in frequency and duration of drought and warming that exacerbates atmospheric evaporative demand. How trees acclimate to long-term soil moisture changes and whether these long-term changes alter trees' sensitivity to short-term (day to months) variations of vapor pressure deficit (VPD) and soil moisture is largely unknown. Leaf gas exchange measurements were performed within a long-term (17 years) irrigation experiment in a drought-prone Scots pine-dominated forest in one of Switzerland's driest areas on trees in naturally dry (control), irrigated, and 'irrigation-stop' (after 11 years of irrigation) conditions. Seventeen years of irrigation increased photosynthesis (A) and stomatal conductance (gs) and reduced gs sensitivity to increasing VPD and soil drying. Following irrigation-stop, gas exchange decreased only after 3 years. After 5 years, maximum carboxylation (Vcmax) and electron transport (Jmax) rates in irrigation-stop recovered to similar levels as to before the irrigation-stop. These results suggest that long-term release from soil drought reduces the sensitivity to VPD and that atmospheric constraints may play an increasingly important role in combination with soil drought. Moreover, our study indicates that structural adjustments lead to an attenuation of initially strong leaf-level acclimation to strong multiple-year drought.

Soil fauna drives vertical redistribution of soil organic carbon in a long-term irrigated dry pine forest.

Summer droughts strongly affect soil organic carbon (SOC) cycling, but net effects on SOC storage are unclear as drought affects both C inputs and outputs from soils. Here, we explored the overlooked role of soil fauna on SOC storage in forests, hypothesizing that soil faunal activity is particularly drought-sensitive, thereby reducing litter incorporation into the mineral soil and, eventually, long-term SOC storage. In a drought-prone pine forest (Switzerland), we performed a large-scale irrigation experiment for 17 years and assessed its impact on vertical SOC distribution and composition. We also examined litter mass loss of dominant tree species using different mesh-size litterbags and determined soil fauna abundance and community composition. The 17-year-long irrigation resulted in a C loss in the organic layers (-1.0 kg C m-2 ) and a comparable C gain in the mineral soil (+0.8 kg C m-2 ) and thus did not affect total SOC stocks. Irrigation increased the mass loss of Quercus pubescens and Viburnum lantana leaf litter, with greater effect sizes when meso- and macrofauna were included (+215%) than when excluded (+44%). The enhanced faunal-mediated litter mass loss was paralleled by a many-fold increase in the abundance of meso- and macrofauna during irrigation. Moreover, Acari and Collembola community composition shifted, with a higher presence of drought-sensitive species in irrigated soils. In comparison, microbial SOC mineralization was less sensitive to soil moisture. Our results suggest that the vertical redistribution of SOC with irrigation was mainly driven by faunal-mediated litter incorporation, together with increased root C inputs. Our study shows that soil fauna is highly sensitive to natural drought, which leads to a reduced C transfer from organic layers to the mineral soil. In the longer term, this potentially affects SOC storage and, therefore, soil fauna plays a key but so far largely overlooked role in shaping SOC responses to drought.

Pervasive decreases in living vegetation carbon turnover time across forest climate zones.

Forests play a major role in the global carbon cycle. Previous studies on the capacity of forests to sequester atmospheric CO2 have mostly focused on carbon uptake, but the roles of carbon turnover time and its spatiotemporal changes remain poorly understood. Here, we used long-term inventory data (1955 to 2018) from 695 mature forest plots to quantify temporal trends in living vegetation carbon turnover time across tropical, temperate, and cold climate zones, and compared plot data to 8 Earth system models (ESMs). Long-term plots consistently showed decreases in living vegetation carbon turnover time, likely driven by increased tree mortality across all major climate zones. Changes in living vegetation carbon turnover time were negatively correlated with CO2 enrichment in both forest plot data and ESM simulations. However, plot-based correlations between living vegetation carbon turnover time and climate drivers such as precipitation and temperature diverged from those of ESM simulations. Our analyses suggest that forest carbon sinks are likely to be constrained by a decrease in living vegetation carbon turnover time, and accurate projections of forest carbon sink dynamics will require an improved representation of tree mortality processes and their sensitivity to climate in ESMs.

Turgor - a limiting factor for radial growth in mature conifers along an elevational gradient.

A valid representation of intra-annual wood formation processes in global vegetation models is vital for assessing climate change impacts on the forest carbon stock. Yet, wood formation is generally modelled with photosynthesis, despite mounting evidence that cambial activity is rather directly constrained by limiting environmental factors. Here, we apply a state-of-the-art turgor-driven growth model to simulate 4 yr of hourly stem radial increment from Picea abies (L.) Karst. and Larix decidua Mill. growing along an elevational gradient. For the first time, wood formation observations were used to validate weekly to annual stem radial increment simulations, while environmental measurements were used to assess the climatic constraints on turgor-driven growth. Model simulations matched the observed timing and dynamics of wood formation. Using the detailed model outputs, we identified a strict environmental regulation on stem growth (air temperature > 2°C and soil water potential > -0.6 MPa). Warmer and drier summers reduced the growth rate as a result of turgor limitation despite warmer temperatures being favourable for cambial activity. These findings suggest that turgor is a central driver of the forest carbon sink and should be considered in next-generation vegetation models, particularly in the context of global warming and increasing frequency of droughts.

Drone-based physiological index reveals long-term acclimation and drought stress responses in trees.

Monitoring early tree physiological responses to drought is key to understanding progressive impacts of drought on forests and identifying resilient species. We combined drone-based multispectral remote sensing with measurements of tree physiology and environmental parameters over two growing seasons in a 100-y-old Pinus sylvestris forest subject to 17-y of precipitation manipulation. Our goal was to determine if drone-based photochemical reflectance index (PRI) captures tree drought stress responses and whether responses are affected by long-term acclimation. PRI detects changes in xanthophyll cycle pigment dynamics, which reflect increases in photoprotective non-photochemical quenching activity resulting from drought-induced photosynthesis downregulation. Here, PRI of never-irrigated trees was up to 10 times lower (higher stress) than PRI of irrigated trees. Long-term acclimation to experimental treatment, however, influenced the seasonal relationship between PRI and soil water availability. PRI also captured diurnal decreases in photochemical efficiency, driven by vapour pressure deficit. Interestingly, 5 years after irrigation was stopped for a subset of the irrigated trees, a positive legacy effect persisted, with lower stress responses (higher PRI) compared with never-irrigated trees. This study demonstrates the ability of remotely sensed PRI to scale tree physiological responses to an entire forest and the importance of long-term acclimation in determining current drought stress responses.

Determinants of legacy effects in pine trees - implications from an irrigation-stop experiment.

Tree responses to altered water availability range from immediate (e.g. stomatal regulation) to delayed (e.g. crown size adjustment). The interplay of the different response times and processes, and their effects on long-term whole-tree performance, however, is hardly understood. Here we investigated legacy effects on structures and functions of mature Scots pine in a dry inner-Alpine Swiss valley after stopping an 11-yr lasting irrigation treatment. Measured ecophysiological time series were analysed and interpreted with a system-analytic tree model. We found that the irrigation stop led to a cascade of downregulations of physiological and morphological processes with different response times. Biophysical processes responded within days, whereas needle and shoot lengths, crown transparency, and radial stem growth reached control levels after up to 4 yr only. Modelling suggested that organ and carbon reserve turnover rates play a key role for a tree's responsiveness to environmental changes. Needle turnover rate was found to be most important to accurately model stem growth dynamics. We conclude that leaf area and its adjustment time to new conditions is the main determinant for radial stem growth of pine trees as the transpiring area needs to be supported by a proportional amount of sapwood, despite the growth-inhibiting environmental conditions.

Assessing the response of forest productivity to climate extremes in Switzerland using model-data fusion.

The response of forest productivity to climate extremes strongly depends on ambient environmental and site conditions. To better understand these relationships at a regional scale, we used nearly 800 observation years from 271 permanent long-term forest monitoring plots across Switzerland, obtained between 1980 and 2017. We assimilated these data into the 3-PG forest ecosystem model using Bayesian inference, reducing the bias of model predictions from 14% to 5% for forest stem carbon stocks and from 45% to 9% for stem carbon stock changes. We then estimated the productivity of forests dominated by Picea abies and Fagus sylvatica for the period of 1960-2018, and tested for productivity shifts in response to climate along elevational gradient and in extreme years. Simulated net primary productivity (NPP) decreased with elevation (2.86 ± 0.006 Mg C ha-1  year-1  km-1 for P. abies and 0.93 ± 0.010 Mg C ha-1  year-1  km-1 for F. sylvatica). During warm-dry extremes, simulated NPP for both species increased at higher and decreased at lower elevations, with reductions in NPP of more than 25% for up to 21% of the potential species distribution range in Switzerland. Reduced plant water availability had a stronger effect on NPP than temperature during warm-dry extremes. Importantly, cold-dry extremes had negative impacts on regional forest NPP comparable to warm-dry extremes. Overall, our calibrated model suggests that the response of forest productivity to climate extremes is more complex than simple shift toward higher elevation. Such robust estimates of NPP are key for increasing our understanding of forests ecosystems carbon dynamics under climate extremes.

Homeostatic levels of nonstructural carbohydrates after 13 yr of drought and irrigation in Pinus sylvestris.

Nonstructural carbohydrates (NSCs) are important for the growth and survival of trees. Drought may lead to a decrease in tree growth and to NSC depletion, whereas increased soil moisture in otherwise dry ecosystems may increase growth and NSC concentrations. A long-term (13 yr) irrigation experiment was conducted in a Pinus sylvestris-dominated forest located at the dry margin of the species in southern Switzerland. We measured the relative leaf area, growth, NSCs, needle δ13 C, [N] and [P] in trees on control and irrigated plots. Irrigation resulted in higher growth rates and carbon isotope discrimination, but did not alter NSC levels. Growth and NSC decreased with decreasing leaf area in both treatments, but NSC did not correlate with leaf-level gas exchange indices, such as foliar δ13 C, [N] or [P]. A legacy effect was shown, as trees with initially low leaf area had limited ability to respond to prolonged irrigation. The NSC constancy across treatments provides evidence that carbohydrate storage may stay constant when climate changes are sufficiently slow to allow acclimation. Moreover, we speculate that total leaf area, rather than leaf gas exchange per unit leaf area, drives the variation in whole-tree carbohydrate dynamics in this system.