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Forests are increasingly affected by heatwaves, often co-occurring with drought, with consequences for water and carbon (C) cycling. However, our ability to project tree resilience to more intense hot droughts remains limited. Here, we used single tree chambers (n = 18) to investigate transpiration (E), net assimilation (Anet), root respiration (Rroot) and stem diameter change in Scots pine seedlings in a control treatment and during gradually intensifying heat or drought-heat stress (max. 42 °C), including recovery. Alongside this, we assessed indicators of stress impacts and recovery capacities. In the heat treatment, excessive leaf heating was mitigated via increased E, while under drought-heat, E ceased and leaf temperatures reached 46 °C. However, leaf electrolyte leakage was negligible, while light-adapted quantum yield of photosystem II (F′v/F′m) declined alongside Anet moderately in heat, but strongly in drought-heat seedlings, in which respiration exceeded C uptake. Drought-heat largely affected the hydraulic system as apparent in stem diameter shrinkage, declining relative needle water content (RWCNeedle) and water potential (ΨNeedle) reaching −2.7 MPa, alongside a 90% decline of leaf hydraulic conductance (KLeaf). Heat alone resulted in low functional impairment and all measured parameters recovered quickly. Contrary, following drought-heat, the recovery of KLeaf was incomplete and stem hydraulic conductivity (KS) was 25% lower than the control. However, F′v/F′m recovered and the tree net C balance reached control values 2 days post-stress, with stem increment rates accelerating during the second recovery week. This indicates a new equilibrium of C uptake and release in drought-heat seedlings independent of hydraulic impairment, which may slowly contribute to the repair of damaged tissues. In summary, Scots pine recovered rapidly following moderate heat stress, while combined with drought, hydraulic and thermal stress intensified, resulting in functional damage and slow recovery of hydraulic conductance. This incomplete hydraulic recovery could critically limit evaporative cooling capacities and C uptake under repeated heatwaves.

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 (CO2)-C-13 pulse labeling to naturally dry control and long-term irrigated trees and tracked the fate of the label in aboveand 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.

Heatwaves combined with drought affect tree functioning with as yet undetermined legacy effects on carbon (C) and nitrogen (N) allocation. - We continuously monitored shoot and root gas exchange, δ13CO2 of respiration and stem growth in well-watered and drought-treated Pinus sylvestris (Scots pine) seedlings exposed to increasing daytime temperatures (max. 42°C) and evaporative demand. Following stress release, we used 13CO2 canopy pulse-labeling, supplemented by soil-applied 15N, to determine allocation to plant compartments, respiration and soil microbial biomass (SMB) over 2.5 wk. - Previously heat-treated seedlings rapidly translocated 13C along the long-distance transport path, to root respiration (Rroot; 7.1 h) and SMB (3 d). Furthermore, 13C accumulated in branch cellulose, suggesting secondary growth enhancement. However, in recovering drought-heat seedlings, the mean residence time of 13C in needles increased, whereas C translocation to Rroot was delayed (13.8 h) and 13C incorporated into starch rather than cellulose. Concurrently, we observed stress-induced low N uptake and aboveground allocation. - C and N allocation during early recovery were affected by stress type and impact. Although C uptake increased quickly in both treatments, drought-heat in combination reduced the above–belowground coupling and starch accumulated in leaves at the expense of growth. Accordingly, C allocation during recovery depends on phloem translocation capacity., New Phytologist, 233 (2), ISSN:0028-646X, ISSN:1469-8137

After drought events, tree recovery depends on sufficient carbon (C) allocation to the sink organs. The present study aimed to elucidate dynamics of tree-level C sink activity and allocation of recent photoassimilates (C$_{new}$) and stored C in c. 70-year-old Norway spruce (Picea abies) trees during a 4-week period after drought release. We conducted a continuous, whole-tree $^{13}$C labeling in parallel with controlled watering after 5 years of experimental summer drought. The fate of C$_{new}$ to growth and CO$_{2}$ efflux was tracked along branches, stems, coarse- and fine roots, ectomycorrhizae and root exudates to soil CO$_{2}$ efflux after drought release. Compared with control trees, drought recovering trees showed an overall 6% lower C sink activity and 19% less allocation of C$_{new}$ to aboveground sinks, indicating a low priority for aboveground sinks during recovery. In contrast, fine-root growth in recovering trees was seven times greater than that of controls. However, only half of the C used for new fine-root growth was comprised of C$_{new}$ while the other half was supplied by stored C. For drought recovery of mature spruce trees, in addition to C$_{new}$, stored C appears to be critical for the regeneration of the fine-root system and the associated water uptake capacity.

Under ongoing global climate change, drought periods are predicted to increase in frequency and intensity in the future. Under these circumstances, it is crucial for tree's survival to recover their restricted functionalities quickly after drought release. To elucidate the recovery of carbon (C) transport rates in c. 70-year-old Norway spruce (Picea abies [L.] KARST.) after 5 years of recurrent summer droughts, we conducted a continuous whole-tree $^{13}$C labeling experiment in parallel with watering. We determined the arrival time of current photoassimilates in major C sinks by tracing the $^{13}$C label in stem and soil CO$_{2}$ efflux, and tips of living fine roots. In the first week after watering, aboveground C transport rates (CTR) from crown to trunk base were still 50% lower in previously drought-stressed trees (0.16 ± 0.01 m h$^{-1}$) compared to controls (0.30 ± 0.06 m h$^{-1}$). Conversely, CTR below ground, that is, from the trunk base to soil CO$_{2}$ efflux were already similar between treatments (c. 0.03 m h$^{-1}$). Two weeks after watering, aboveground C transport of previously drought-stressed trees recovered to the level of the controls. Furthermore, regrowth of water-absorbing fine roots upon watering was supported by faster incorporation of $^{13}$C label in previously drought-stressed (within 12 ± 10 h upon arrival at trunk base) compared to control trees (73 ± 10 h). Thus, the whole-tree C transport system from the crown to soil CO$_{2}$ efflux fully recovered within 2 weeks after drought release, and hence showed high resilience to recurrent summer droughts in mature Norway spruce forests. This high resilience of the C transport system is an important prerequisite for the recovery of other tree functionalities and productivity.

Carbon (C) exuded via roots is proposed to increase under drought and facilitate important ecosystem functions. However, it is unknown how exudate quantities relate to the total C budget of a drought-stressed tree, that is, how much of net-C assimilation is allocated to exudation at the tree level. - We calculated the proportion of daily C assimilation allocated to root exudation during early summer by collecting root exudates from mature Fagus sylvatica and Picea abies exposed to experimental drought, and combining above- and belowground C fluxes with leaf, stem and fine-root surface area. - Exudation from individual roots increased exponentially with decreasing soil moisture, with the highest increase at the wilting point. Despite c. 50% reduced C assimilation under drought, exudation from fine-root systems was maintained and trees exuded 1.0% (F. sylvatica) to 2.5% (P. abies) of net C into the rhizosphere, increasing the proportion of C allocation to exudates two- to three-fold. Water-limited P. abies released two-thirds of its exudate C into the surface soil, whereas in droughted F. sylvatica it was only one-third. - Across the entire root system, droughted trees maintained exudation similar to controls, suggesting drought-imposed belowground C investment, which could be beneficial for ecosystem resilience.

Forests are increasingly affected by heatwaves, often co-occurring with drought, with consequences for water and carbon (C) cycling. However, our ability to project the resilience of trees to an intensification of hot droughts remains limited. Here, we used single tree cuvettes (n=18) allowing us to investigate transpiration (E), net assimilation (Anet), root respiration (Rroot) and stem diameter change in Scots pine seedlings during gradually intensifying heat or drought-heat stress (max. 42°C), and post-stress. Further, we assessed indicators of stress impacts and recovery capacities.Under heat stress, well-watered seedlings prevented overheating of leaves effectively via increased E, while under drought-heat leaf temperatures increased to 46°C. However, leaf electrolyte leakage was negligible, but F’v/F’m declined alongside Anet moderately in heat but strongly in drought-heat seedlings, in which respiration exceeded C uptake. Further, the decrease of needle water potential (ψNeedle) to −2.7 MPa and relative needle water content (RWCNeedle) under drought-heat reflected a decline of leaf hydraulic conductance (KLeaf) by 90% and stem hydraulic conductivity (KS) by 25%. Alongside, we observed pronounced stem diameter shrinkage.Heat stress alone resulted in low functional impairment and all measured parameters recovered fast. In contrast, larger impacts following combined heat and drought led to the incomplete recovery of KLeaf and KS. Despite Anet tended to be reduced albeit F’v/F’m had recovered, the seedlings’ net C balance reached control values 2 d after stress release and stem growth rates exceeded control rates in the 2nd week post-stress. This indicates that a new equilibrium of C uptake and release was maintained at the tree level, slowly supporting regaining of stress-induced losses.In summary, we highlight that under moderate heatwaves with low functional impairment, recovery is fast in Scots pine, while in combination with drought hydraulic and thermal stress are intensified, resulting in functional damage and delayed recovery processes. The incomplete recovery of hydraulic conductance indicates limited water transport capacities that could become critical under repeated heat events.

Climate change will have a considerable impact on forest productivity worldwide. Forecasting the magnitude of such impact, with multiple environmental stressors changing simultaneously, is only possible with the help of process-based models. In order to assess their performance, such models require careful evaluation against measurements. However, direct comparison of model outputs against observational data is often not reliable, as models may provide the right answers due to the wrong reasons. This would severely hinder forecasting abilities under unprecedented climate conditions. Here, we present a methodology for model assessment, which supplements the traditional output-to-observation model validation. It evaluates model performance through its ability to reproduce observed seasonal changes of the most limiting environmental driver (MLED) for a given process, here daily gross primary productivity (GPP). We analyzed seasonal changes of the MLED for GPP in two contrasting pine forests, the Mediterranean Pinus halepensis Mill. Yatir (Israel) and the boreal Pinus sylvestris L. Hyytiälä (Finland) from three years of eddy-covariance flux data. Then, we simulated the same period with a state-of-the-art process-based simulation model (LandscapeDNDC). Finally, we assessed if the model was able to reproduce both GPP observations and MLED seasonality. We found that the model reproduced the seasonality of GPP in both stands, but it was slightly overestimated without site-specific fine-tuning. Interestingly, although LandscapeDNDC properly captured the main MLED in Hyytiälä (temperature) and in Yatir (soil water availability), it failed to reproduce high-temperature and high-vapor pressure limitations of GPP in Yatir during spring and summer. We deduced that the most likely reason for this divergence is an incomplete description of stomatal behavior. In summary, this study validates the MLED approach as a model evaluation tool, and opens up new possibilities for model improvement.

Plant responses to drought and heat stress have been extensively studied, whereas post-stress recovery, which is fundamental to understanding stress resilience, has received much less attention. Here, we present a conceptual stress-recovery framework with respect to hydraulic and metabolic functioning in woody plants. We further synthesize results from controlled experimental studies following heat or drought events and highlight underlying mechanisms that drive post-stress recovery. We find that the pace of recovery differs among physiological processes. Leaf water potential and abscisic acid concentration typically recover within few days upon rewetting, while leaf gas exchange-related variables lag behind. Under increased drought severity as indicated by a loss in xylem hydraulic conductance, the time for stomatal conductance recovery increases markedly. Following heat stress release, a similar delay in leaf gas exchange recovery has been observed, but the reasons are most likely a slow reversal of photosynthetic impairment and other temperature-related leaf damages, which typically manifest at temperatures above 40 °C. Based thereon, we suggest that recovery of gas exchange is fast following mild stress, while recovery is slow and reliant on the efficiency of repair and regrowth when stress results in functional impairment and damage to critical plant processes. We further propose that increasing stress severity, particular after critical stress levels have been reached, increases the carbon cost involved in reestablishing functionality. This concept can guide future experimental research and provides a base for modeling post-stress recovery of carbon and water relations in trees.

This contribution presents the result of a free-air 13C labeling experiment on mature Norway spruce (P. abies [L.] KARST.) upon watering after five years of recurrent summer drought in southern Germany, focusing on whole tree allocation processes. Mature spruce trees had been exposed to recurrent summer drought from 2014 to 2018 through complete exclusion of precipitation throughfall from spring to late fall (i.e., March to November). In early summer 2019, the drought stressed spruce trees were watered to investigate their recovery processes. In parallel with the watering, we conducted a whole-tree 13C labeling in canopies and traced the signal in various C sinks, i.e. stem phloem and CO2 efflux, tree rings at different heights, coarse roots, fine root tips, mycorrhiza, root exudates, and soil CO2 efflux.We hypothesize that drought stressed spruce preferentially allocates newly assimilated C to belowground sinks upon drought release. Conversely to our expectations, allocation to belowground C sinks was not stimulated in drought stressed compared to control spruce. Likewise, the relative amount of recently fixed C allocated to aboveground sinks did not differ between treatments. Our findings suggest that the belowground C sinks are not of higher priority for the allocation of newly assimilated C upon watering after long-term drought. The observed allocation pattern is discussed taking total above- and belowground biomass as well as C source/sink relations into account.

The resistance of trees to stress events has been studied intensively, however we know little on underlying processes affecting the recovery of trees following stress release. Hence, this clearly impairs our ability to project the resilience of trees and forests to an intensification of heatwaves and drought spells.Here we studied the legacy effects of heat and heat-drought stress on carbon (C) allocation dynamics in Scots pine. We were particularly interested in how C allocation changes post heat and heat-drought stress and how this change in allocation affects tree growth. We exposed Pinus sylvestris seedlings to increasing temperatures from 30 to 40°C within 18 days either under well-watered or drought conditions and measured stem growth, leaf water potential and above- and belowground gas exchange. Two days after stress release, we conducted a 13CO2 pulse-labelling experiment in custom build single tree cuvettes (n=18) allowing us to continuously monitor 13CO2 shoot and root gas exchange. We then chased the fate of the newly assimilated C from leaves to roots via soluble sugars, starch and cellulose.Our results showed that Pinus sylvestris is able to recover gas exchange following heat release immediately in the well-watered trees, while drought-treated trees recovered slightly slower. We found indications for a stress compensatory response of the previously heat-treated trees, which tended to translocate recent assimilates faster compared to the control trees as identified in the dynamics of water-soluble carbon in the phloem and root 13CO2 efflux. In addition, we found larger stem growth rates in the heat-treated trees which was also reflected by a larger investment of new assimilates to cellulose. In the trees that experienced both, heat and drought stress, C allocation differed strongly from the control trees as apparent in a half as fast C translocation from leaves to root respiration and large investments of new assimilates into starch. This delayed translocation but enhanced allocation towards C storage in needle tissues was reflected in a delayed recovery of stem growth and very low detection of the 13C signal in twig, root and stem cellulose. We can conclude that heatwaves of 40°C have relatively moderate responses on C allocation post-stress, whereas hot drought stress clearly affects C allocation as indicated by a delayed C transport capacity and a preferential allocation towards C storage in needle tissues. This could indicate that C allocation following hot drought stress is affected by an impaired phloem functionality, which only slowly recovers post-stress.

Trees are increasingly exposed to hot droughts due to CO

Forest leaf area has enormous leverage on the carbon cycle because it mediates both forest productivity and resilience to climate extremes. Despite widespread evidence that trees are capable of adjusting to changes in environment across both space and time through modifying carbon allocation to leaves, many vegetation models use fixed carbon allocation schemes independent of environment, which introduces large uncertainties into predictions of future forest responses to atmospheric CO2 fertilization and anthropogenic climate change. Here, we develop an optimization-based model, whereby tree carbon allocation to leaves is an emergent property of environment and plant hydraulic traits. Using a combination of meta-analysis, observational datasets, and model predictions, we find strong evidence that optimal hydraulic-carbon coupling explains observed patterns in leaf allocation across large environmental and CO2 concentration gradients. Furthermore, testing the sensitivity of leaf allocation strategy to a diversity in hydraulic and economic spectrum physiological traits, we show that plant hydraulic traits in particular have an enormous impact on the global change response of forest leaf area. Our results provide a rigorous theoretical underpinning for improving carbon cycle predictions through advancing model predictions of leaf area, and underscore that tree-level carbon allocation to leaves should be derived from first principles using mechanistic plant hydraulic processes in the next generation of vegetation models.

The frequency and intensity of climatic extremes, such as heat waves, are predicted to increase globally, with severe implications for terrestrial carbon and water cycling. Temperatures may rise above critical thresholds that allow trees to function optimally, with unknown long-term consequences for forest ecosystems. In this context, we investigated how photosynthetic traits and the water balance in Douglas-fir are affected by exposure to three heat waves with temperatures about 12 degrees C above ambient. Photosynthetic carboxylation efficiency (V-cmax) was mostly unaffected, but electron transport (J(max)) and photosynthetic rates under saturating light (A(sat)) were strongly influenced by the heat waves, with lagging limitations on photosynthesis still being observed six weeks after the last heat wave. We also observed lingering heat-induced inhibitions on transpiration, minimum stomatal conductance, and night-time stomatal conductance (g(s-night)). Results from the stomatal models used to calculate minimum stomatal conductance were similar to g(s-night) and indicated changes in leaf morphology, e.g. stomatal occlusions and alterations in epicuticular wax. Our results show Douglas-fir's ability to restrict water loss following heat stress, but at the price of reduced photosynthetic performance. Such limitations indicate potential long-term restrictions that heat waves can impose on tree development and functioning under extreme climatic conditions. (C) 2016 Elsevier GmbH. All rights reserved.