Acclimation of mature spruce and beech to five years of repeated summer drought - The role of stomatal conductance and leaf area adjustment for water use.

Forests globally are experiencing severe droughts, leading to significant reductions in growth, crown dieback and even tree mortality. The ability of forest ecosystems to acclimate to prolonged and repeated droughts is critical for their survival with ongoing climate change. In a five-year throughfall exclusion experiment, we investigated the long-term physiological and morphological acclimation of mature Norway spruce (Picea abies [L.] KARST.) and European beech (Fagus sylvatica L.) to repeated summer drought at the leaf, shoot and whole tree level. Throughout the drought period, spruce reduced their total water use by 70 % to only 4-9 L per day and tree, while beech was less affected with about 30 % reduction of water use. During the first two summers, spruce achieved this by closing their stomata by up to 80 %. Additionally, from the second drought summer onwards, spruce produced shorter shoots and needles, resulting in a stepwise reduction of total leaf area of over 50 % by the end of the experiment. Surprisingly, no premature leaf loss was observed. This reduction in leaf area allowed a gradual increase in stomatal conductance. After the five-year drought experiment, water consumption per leaf area was the same as in the controls, while the total water consumption of spruce was still reduced. In contrast, beech showed no significant reduction in whole-tree leaf area, but nevertheless reduced water use by up to 50 % by stomatal closure. If the restriction of transpiration by stomatal closure is sufficient to ensure survival of Norway spruce during the first drought summers, then the slow but steady reduction in leaf area will ensure successful acclimation of water use, leading to reduced physiological drought stress and long-term survival. Neighboring beech appeared to benefit from the water-saving strategy of spruce by using the excess water.

Repeated summer drought delays sugar export from the leaf and impairs phloem transport in mature beech.

Phloem sustains maintenance and growth processes through transport of sugars from source to sink organs. Under low water availability, tree functioning is impaired, i.e., growth/photosynthesis decline and phloem transport may be hindered. In a 3-year throughfall exclusion (TE) experiment on mature European beech (Fagus sylvatica L.) we conducted 13CO2 branch labeling to investigate translocation of recently fixed photoassimilates under experimental drought over 2 years (2015 and 2016). We hypothesized (H1) that mean residence time of photoassimilates in leaves (MRT) increases, whereas (H2) phloem transport velocity (Vphloem) decreases under drought. Transport of carbohydrates in the phloem was assessed via δ13C of CO2 efflux measured at two branch positions following 13CO2 labeling. Pre-dawn water potential (ΨPD) and time-integrated soil water deficit (iSWD) were used to quantify drought stress. The MRT increased by 46% from 32.1 ± 5.4 h in control (CO) to 46.9 ± 12.3 h in TE trees, supporting H1, and positively correlated (P < 0.001) with iSWD. Confirming H2, Vphloem in 2016 decreased by 47% from 20.7 ± 5.8 cm h-1 in CO to 11.0 ± 2.9 cm h-1 in TE trees and positively correlated with ΨPD (P = 0.001). We suggest that the positive correlation between MRT and iSWD is a result of the accumulation of osmolytes maintaining cell turgor in the leaves under longer drought periods. Furthermore, we propose that the positive correlation between Vphloem and ΨPD is due to a lower water uptake of phloem conduits from surrounding tissues under increasing drought leading to a higher phloem sap viscosity and lower Vphloem. The two mechanisms increasing MRT and reducing Vphloem respond differently to low water availability and impair trees' carbon translocation under drought.

Fate of recently fixed carbon in European beech (Fagus sylvatica) saplings during drought and subsequent recovery.

Drought reduces the carbon (C) assimilation of trees and decouples aboveground from belowground carbon fluxes, but little is known about the response of drought-stressed trees to rewetting. This study aims to assess dynamics and patterns of C allocation in beech saplings under dry and rewetted soil conditions. In October 2010, 5-year-old beech saplings from a forest site were transplanted into 20 l pots. In 2011, the saplings were subjected to different levels of soil drought ranging from non-limiting water supply (control) to severe water limitation with soil water potentials of less than -1.5 MPa. As a physiologically relevant measure of drought, the cumulated soil water potential (i.e., drought stress dose (DSD)) was calculated for the growing season. In late August, the saplings were transferred into a climate chamber and pulse-labeled with (13)C-depleted CO2 (δ(13)C of -47‰). Isotopic signatures in leaf and soil respiration were repeatedly measured. Five days after soil rewetting, a second label was applied using 99 atom% (13)CO2. After another 12 days, the fate of assimilated C in each sapling was assessed by calculating the (13)C mass balance. Photosynthesis decreased by 60% in saplings under severe drought. The mean residence time (MRT) of recent assimilates in leaf respiration was more than three times longer than under non-limited conditions and was positively correlated to DSD. Also, the appearance of the label in soil respiration was delayed. Within 5 days after rewetting, photosynthesis, MRT of recent assimilates in leaf respiration and appearance of the label in soil respiration recovered fully. Despite the fast recovery, less label was recovered in the biomass of the previously drought-stressed plants, which also allocated less C to the root compartment (45 vs 64% in the control). We conclude that beech saplings quickly recover from extreme soil drought, although transitional after-effects prevail in C allocation, possibly due to repair-driven respiratory processes.