Stomatal regulation by microclimate and tree water relations: interpreting ecophysiological field data with a hydraulic plant model

Dynamics in microclimate and physiological plant traits were studied for Pubescent oak and Scots pine in a dry inner-alpine valley in Switzerland, at a 10 min resolution for three consecutive years (2001-2003). As expected, stomata tended to close with increasing drought in air and soil. However, stomatal aperture in oak was smaller than in pine under relatively wet conditions, but larger under dry conditions. To explore underlying mechanisms, a model was applied that (i) quantifies water relations within trees from physical principles (mechanistic part) and (ii) assumes that signals from light, stomatal aperture, crown water potential, and tree water deficit in storage pools control stomata (systemic part). The stomata of pine showed a more sensitive response to increasing drought because both factors, the slowly changing tree water deficit and the rapidly changing crown water potential, closed the stomata. By contrast, the stomata of oak became less drought-sensitive as the closing signal of crown water potential was opposed by the opening signal of tree water deficit. Moreover, parameter optimization suggests that oak withdrew more water from the storage pools and reduced leaf water potentials to lower levels, without risking serious damage by cavitation. The new model thus suggests how the hydraulic water flow and storage system determines the responses in stomatal aperture and transpiration to drought at time scales ranging from hours to multiple years, and why pine and oak might differ in such responses. These differences explain why oaks are more efficient competitors during drought periods, although this was not the case in the extremely dry year 2003, which provoked massive leaf loss and, from July onwards, physiological activity almost cease

Pine and mistletoes: how to live with a leak in the water flow and storage system?

The mistletoe, Viscum album, living on Scots pine (Pinus sylvestris) has been reported barely to regulate its transpiration and thus heavily to affect the gas exchange of its host. The extent of this mistletoe effect and its underlying mechanism has, so far, only been partially analysed. In this study, pine branches with different mistletoe infestation levels were investigated by sap flow gauges and analysed with a modelling approach to identify the mistletoe-induced stomatal regulation of pine and its consequences for the water and carbon balances of the tree. It was found that Viscum album barely regulates its stomata and that pines consequently compensate for the additional water loss of mistletoes by closing their own stomata. Despite the reduced stomatal aperture of the needles, the total water loss of branches with mistletoes increased. Furthermore, the increasingly closed stomata reduced carbon assimilation for the pine. Such a negative effect of the mistletoes on pine's stomatal conductance and carbon gain was particularly strong during dry periods. Our study therefore suggests that mistletoe-induced stomatal closure is a successful mechanism against dying from hydraulic failure in the short term but increases the risk of carbon starvation in the long term. With the current conditions in Valais, Switzerland, a tree with more than about 10-20% of its total leaf area attributable to mistletoes is at the threshold of keeping a positive carbon balance. The currently increasing mistletoe abundance, due to increasing mean annual temperatures, is therefore accelerating the ongoing pine decline in many dry inner-Alpine valley

Intra-annual radial growth and water relations of trees: implications towards a growth mechanism

There is a missing link between tree physiological and wood-anatomical knowledge which makes it impossible mechanistically to explain and predict the radial growth of individual trees from climate data. Empirical data of microclimatic factors, intra-annual growth rates, and tree-specific ratios between actual and potential transpiration (T PET−1) of trees of three species (Quercus pubescens, Pinus sylvestris, and Picea abies) at two dry sites in the central Wallis, Switzerland, were recorded from 2002 to 2004 at a 10 min resolution. This included the exceptionally hot and dry summer of 2003. These data were analysed in terms of direct (current conditions) and indirect impacts (predispositions of the past year) on growth. Rain was found to be the only factor which, to a large extent, consistently explained the radial increment for all three tree species at both sites and in the short term as well. Other factors had some explanatory power on the seasonal time-scale only. Quercus pubescens built up much of its tree ring before bud break. Pinus sylvestris and Picea abies started radial growth 1-2 weeks after Quercus pubescens and this was despite the fact that they had a high T PET−1 before budburst and radial growth started. A high T PET−1 was assumed to be related to open stomata, a very high net CO2 assimilation rate, and thus a potential carbon (C)-income for the tree. The main period of radial growth covered about 30-70% of the productive days of a year. In terms of C-allocation, these results mean that Quercus pubescens depended entirely on internal C-stores in the early phase of radial growth and that for all three species there was a long time period of C-assimilation which was not used for radial growth in above-ground wood. The results further suggest a strong dependence of radial growth on the current tree water relations and only secondarily on the C-balance. A concept is discussed which links radial growth over a feedback loop to actual tree water-relations and long-term affected C-storage to microclimat

Temperate tree species show identical response in tree water deficit but different sensitivities in sap flow to summer soil drying

Temperate forests are expected to be particularly vulnerable to drought and soil drying because they are not adapted to such conditions and perform best in mesic environments. Here we ask (i) how sensitively four common temperate tree species (Fagus sylvatica, Picea abies, Acer pseudoplatanus and Fraxinus excelsior) respond in their water relations to summer soil drying and seek to determine (ii) if species-specific responses to summer soil drying are related to the onset of declining water status across the four species. Throughout 2012 and 2013 we determined tree water deficit (TWD) as a proxy for tree water status from recorded stem radius changes and monitored sap flow rates with sensors on 16 mature trees studied in the field at Lägeren, Switzerland. All tree species responded equally in their relative maximum TWD to the onset of declining soil moisture. This implies that the water supply of all tree species was affected by declining soil moisture and that none of the four species was able to fully maintain its water status, e.g., by access to alternative water sources in the soil. In contrast we found strong and highly species-specific responses of sap flow to declining soil moisture with the strongest decline in P. abies (92%), followed by F. sylvatica (53%) and A. pseudoplatanus (48%). F. excelsior did not significantly reduce sap flow. We hypothesize the species-specific responses in sap flow to declining soil moisture that occur despite a simultaneous increase in relative TWD in all species reflect how fast these species approach critical levels of their water status, which is most likely influenced by species-specific traits determining the hydraulic properties of the species tree

Drought alters timing, quantity, and quality of wood formation in Scots pine

Drought has been frequently discussed as a trigger for forest decline. Today, large-scale Scots pine decline is observed in many dry inner-Alpine valleys, with drought discussed as the main causative factor. This study aimed to analyse the impact of drought on wood formation and wood structure. To study tree growth under contrasting water supply, an irrigation experiment was installed in a mature Scots pine (Pinus sylvestris L.) forest at a xeric site in a dry inner-Alpine valley. Inter- and intra-annual radial increments as well as intra-annual variations in wood structure of pine trees were studied. It was found that non-irrigated trees had a noticeably shorter period of wood formation and showed a significantly lower increment. The water conduction cells were significantly enlarged and had significantly thinner cell walls compared with irrigated trees. It is concluded that pine trees under drought stress build a more effective water-conducting system (larger tracheids) at the cost of a probably higher vulnerability to cavitation (larger tracheids with thinner cell walls) but without losing their capability to recover. The significant shortening of the growth period in control trees indicated that the period where wood formation actually takes place can be much shorter under drought than the ‘potential' period, meaning the phenological growth perio

A lifetime perspective of biomass allocation in Quercus pubescens trees in a dry, alpine valley

Plasticity of biomass allocation is a key to growth and survival of trees exposed to variable levels of stress in their lifetime. Most of our understanding of dynamic biomass allocation comes from seedling studies, but plasticity may be different in mature trees. We used stem analysis to reconstruct whole-tree growth and biomass allocation patterns in Quercus pubescens trees harvested from a dry woodland in Valais, Switzerland. We identified three distinct growth phases. In phase I, a primary root developed but the aboveground structure did not persist. In phase II, height growth occurred and secondary roots developed. In phase III, height growth ceased and stems and roots only grew radially. Reference trees harvested from a less dry site nearby only showed phase II-type growth. In line with our hypothesis, drought-stressed trees maintained more biomass in roots and less in aboveground woody parts than reference trees. Contrary to our expectation, stressed trees allocated proportionally more resources to leaves and less to roots in the growing season before harvest than reference trees. It appears that sub-seasonal wood anatomical adjustments to water availability minimize hydraulic failure, thus enabling these dry woodland trees to invest preferentially in leaves. Wet years did not see preferential investment in aboveground tissues, suggesting more restricted plasticity in biomass allocation in these mature trees than in seedlings. It is concluded that trees beyond seedling stage show different responses to variation in drought than the better-studied seedling

The Carbon Balance of Two Contrasting Mountain Forest Ecosystems in Switzerland: Similar Annual Trends, but Seasonal Differences

Net ecosystem exchange (NEE) of two contrasting mountain forest types in Switzerland was measured by eddy covariance (EC) measurements at a montane mixed forest, the Lägeren forest, over 5 years (2005-2009), and at a subalpine coniferous forest, the Seehornwald in Davos, over 12years (1997-2009). NEE was validated against annual carbon (C) storage estimates, based on biometric and soil respiration measurements as well as soil C modeling. Three different approaches were used: (1) calculation of net ecosystem production by quantifying C pools and fluxes, (2) assessment of change in wood biomass and soil C storage (ΔC), and (3) application of biomass expansion factors. Although biometric estimates were sensitive to assumptions made for each method applied, they agreed well with measured NEE. Comparing 5years of EC measurements available at both sites during 2005 and 2009 revealed that NEE, gross primary production (GPP), and total ecosystem respiration (TER) were larger at the Lägeren forest compared to the Davos forest, whereas soil respiration and soil C sequestration were of similar magnitudes. Both sites showed similar annual trends for NEE, GPP and TER, but different seasonal courses, due to different responses to environmental conditions (temperature, soil moisture, and radiation). Differences in the magnitude as well as in the seasonality of ecosystem CO2 exchange could mainly be attributed to tree phenology, productivity, and carbon allocation patterns, which are combined effects of tree type (broad-leaved vs. coniferous trees) and site-specific climatic conditions. Flux differences between the two mountain sites highlight the importance of considering the role of altitude in ecological studies and modelin

An empirical method that separates irreversible stem radial growth from bark water content changes in trees : theory and case studies

Substantial uncertainty surrounds our knowledge of tree stem growth, with some of the most basic questions, such as when stem radial growth occurs through the daily cycle, still unanswered. We employed high-resolution point dendrometers, sap flow sensors, and developed theory and statistical approaches, to devise a novel method separating irreversible radial growth from elastic tension-driven and elastic osmotically driven changes in bark water content. We tested this method using data from five case study species. Experimental manipulations, namely a field irrigation experiment on Scots pine and a stem girdling experiment on red forest gum trees, were used to validate the theory. Time courses of stem radial growth following irrigation and stem girdling were consistent with a-priori predictions. Patterns of stem radial growth varied across case studies, with growth occurring during the day and/or night, consistent with the available literature. Importantly, our approach provides a valuable alternative to existing methods, as it can be approximated by a simple empirical interpolation routine that derives irreversible radial growth using standard regression techniques. Our novel method provides an improved understanding of the relative source-sink carbon dynamics of tree stems at a sub-daily time scale.Peer reviewe

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 (g(s)) and reduced g(s) sensitivity to increasing VPD and soil drying. Following irrigation-stop, gas exchange decreased only after 3 years. After 5 years, maximum carboxylation (V-cmax) and electron transport (J(max)) 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. Acclimation to irrigation increased gas exchange in Pinus sylvestris, but reduced the sensitivity to short-term changes. In addition, structural adjustments led to an attenuation of initially strong leaf-level acclimation.Peer reviewe

Manipulative experiments demonstrate how long-term soil moisture changes alter controls of plant water use

Tree transpiration depends on biotic and abiotic factors that might change in the future, including precipitation and soil moisture status. Although short-term sap flux responses to soil moisture and evaporative demand have been the subject of attention before, the relative sensitivity of sap flux to these two factors under long-term changes in soil moisture conditions has rarely been determined experimentally. We tested how long-term artificial change in soil moisture affects the sensitivity of tree-level sap flux to daily atmospheric vapor pressure deficit (VPD) and soil moisture variations, and the generality of these effects across forest types and environments using four manipulative sites in mature forests. Exposure to relatively long-term (two to six years) soil moisture reduction decreases tree sap flux sensitivity to daily VPD and relative extractable water (REW) variations, leading to lower sap flux even under high soil moisture and optimal VPD. Inversely, trees subjected to long-term irrigation showed a significant increase in their sensitivity to daily VPD and REW, but only at the most water-limited site. The ratio between the relative change in soil moisture manipulation and the relative change in sap flux sensitivity to VPD and REW variations was similar across sites suggesting common adjustment mechanisms to long-term soil moisture status across environments for evergreen tree species. Overall, our results show that long-term changes in soil water availability, and subsequent adjustments to these novel conditions, could play a critical and increasingly important role in controlling forest water use in the future.Peer reviewe