Short-term variation in leaf-level water use efficiency in a tropical forest.

The representation of stomatal regulation of transpiration and CO2 assimilation is key to forecasting terrestrial ecosystem responses to global change. Given its importance in determining the relationship between forest productivity and climate, accurate and mechanistic model representation of the relationship between stomatal conductance (gs ) and assimilation is crucial. We assess possible physiological and mechanistic controls on the estimation of the g1 (stomatal slope, inversely proportional to water use efficiency) and g0 (stomatal intercept) parameters, using diurnal gas exchange surveys and leaf-level response curves of six tropical broadleaf evergreen tree species. g1 estimated from ex situ response curves averaged 50% less than g1 estimated from survey data. While g0 and g1 varied between leaves of different phenological stages, the trend was not consistent among species. We identified a diurnal trend associated with g1 and g0 that significantly improved model projections of diurnal trends in transpiration. The accuracy of modeled gs can be improved by accounting for variation in stomatal behavior across diurnal periods, and between measurement approaches, rather than focusing on phenological variation in stomatal behavior. Additional investigation into the primary mechanisms responsible for diurnal variation in g1 will be required to account for this phenomenon in land-surface models.

The influence of increasing atmospheric CO2 , temperature, and vapor pressure deficit on seawater-induced tree mortality.

Increasing seawater exposure is killing coastal trees globally, with expectations of accelerating mortality with rising sea levels. However, the impact of concomitant changes in atmospheric CO2 concentration, temperature, and vapor pressure deficit (VPD) on seawater-induced tree mortality is uncertain. We examined the mechanisms of seawater-induced mortality under varying climate scenarios using a photosynthetic gain and hydraulic cost optimization model validated against observations in a mature stand of Sitka spruce (Picea sitchensis) trees in the Pacific Northwest, USA, that were dying from recent seawater exposure. The simulations matched well with observations of photosynthesis, transpiration, nonstructural carbohydrates concentrations, leaf water potential, the percentage loss of xylem conductivity, and stand-level mortality rates. The simulations suggest that seawater-induced mortality could decrease by c. 16.7% with increasing atmospheric CO2 levels due to reduced risk of carbon starvation. Conversely, rising VPD could increase mortality by c. 5.6% because of increasing risk of hydraulic failure. Across all scenarios, seawater-induced mortality was driven by hydraulic failure in the first 2 yr after seawater exposure began, with carbon starvation becoming more important in subsequent years. Changing CO2 and climate appear unlikely to have a significant impact on coastal tree mortality under rising sea levels.

Declining carbohydrate content of Sitka-spruce treesdying from seawater exposure.

Increasing sea levels associated with climate change threaten the survival of coastal forests, yet the mechanisms by which seawater exposure causes tree death remain poorly understood. Despite the potentially crucial role of nonstructural carbohydrate (NSC) reserves in tree survival, their dynamics in the process of death under seawater exposure are unknown. Here we monitored progressive tree mortality and associated NSC storage in Sitka-spruce (Picea sitchensis) trees dying under ecosystem-scale increases in seawater exposure in western Washington, USA. All trees exposed to seawater, because of monthly tidal intrusion, experienced declining crown foliage during the sampling period, and individuals with a lower percentage of live foliated crown (PLFC) died faster. Tree PLFC was strongly correlated with subsurface salinity and needle ion contents. Total NSC concentrations in trees declined remarkably with crown decline, and reached extremely low levels at tree death (2.4% and 1.6% in leaves and branches, respectively, and 0.4% in stems and roots). Starch in all tissues was almost completely consumed, while sugars remained at a homeostatic level in foliage. The decreasing NSC with closer proximity to death and near zero starch at death are evidences that carbon starvation occurred during Sitka-spruce mortality during seawater exposure. Our results highlight the importance of carbon storage as an indicator of tree mortality risks under seawater exposure.

Seawater exposure causes hydraulic damage in dying Sitka-spruce trees.

Sea-level rise is one of the most critical challenges facing coastal ecosystems under climate change. Observations of elevated tree mortality in global coastal forests are increasing, but important knowledge gaps persist concerning the mechanism of salinity stress-induced nonhalophytic tree mortality. We monitored progressive mortality and associated gas exchange and hydraulic shifts in Sitka-spruce (Picea sitchensis) trees located within a salinity gradient under an ecosystem-scale change of seawater exposure in Washington State, USA. Percentage of live foliated crown (PLFC) decreased and tree mortality increased with increasing soil salinity during the study period. A strong reduction in gas exchange and xylem hydraulic conductivity (Ks) occurred during tree death, with an increase in the percentage loss of conductivity (PLC) and turgor loss point (πtlp). Hydraulic and osmotic shifts reflected that hydraulic function declined from seawater exposure, and dying trees were unable to support osmotic adjustment. Constrained gas exchange was strongly related to hydraulic damage at both stem and leaf levels. Significant correlations between foliar sodium (Na+) concentration and gas exchange and key hydraulic parameters (Ks, PLC, and πtlp) suggest that cellular injury related to the toxic effects of ion accumulation impacted the physiology of these dying trees. This study provides evidence of toxic effects on the cellular function that manifests in all aspects of plant functioning, leading to unfavourable osmotic and hydraulic conditions.

Increasing temperature and vapour pressure deficit lead to hydraulic damages in the absence of soil drought.

Temperature (T) and vapour pressure deficit (VPD) are important drivers of plant hydraulic conductivity, growth, mortality, and ecosystem productivity, independently of soil water availability. Our goal was to disentangle the effects of T and VPD on plant hydraulic responses. Young trees of Fagus sylvatica L., Quercus pubescens Willd. and Quercus ilex L. were exposed to a cross-combination of a T and VPD manipulation under unlimited soil water availability. Stem hydraulic conductivity and leaf-level hydraulic traits (e.g., gas exchange and osmotic adjustment) were tracked over a full growing season. Significant loss of xylem conductive area (PLA) was found in F. sylvatica and Q. pubescens due to rising VPD and T, but not in Q. ilex. Increasing T aggravated the effects of high VPD in F. sylvatica only. PLA was driven by maximum hydraulic conductivity and minimum leaf conductance, suggesting that high transpiration and water loss after stomatal closure contributed to plant hydraulic stress. This study shows for the first time that rising VPD and T lead to losses of stem conductivity even when soil water is not limiting, highlighting their rising importance in plant mortality mechanisms in the future.

Stability of tropical forest tree carbon-water relations in a rainfall exclusion treatment through shifts in effective water uptake depth.

Increasing severity and frequency of drought is predicted for large portions of the terrestrial biosphere, with major impacts already documented in wet tropical forests. Using a 4-year rainfall exclusion experiment in the Daintree Rainforest in northeast Australia, we examined canopy tree responses to reduced precipitation and soil water availability by quantifying seasonal changes in plant hydraulic and carbon traits for 11 tree species between control and drought treatments. Even with reduced soil volumetric water content in the upper 1 m of soil in the drought treatment, we found no significant difference between treatments for predawn and midday leaf water potential, photosynthesis, stomatal conductance, foliar stable carbon isotope composition, leaf mass per area, turgor loss point, xylem vessel anatomy, or leaf and stem nonstructural carbohydrates. While empirical measurements of aboveground traits revealed homeostatic maintenance of plant water status and traits in response to reduced soil moisture, modeled belowground dynamics revealed that trees in the drought treatment shifted the depth from which water was acquired to deeper soil layers. These findings reveal that belowground acclimation of tree water uptake depth may buffer tropical rainforests from more severe droughts that may arise in future with climate change.

Stomatal behaviour and stem xylem traits are coordinated for woody plant species under exceptional drought conditions.

Isohydry (maintenance of plant water potential at the cost of carbon gain) and anisohydry (gas exchange maintenance at the cost of declining plant water status) make up two ends of a stomatal drought response strategy continuum. However, few studies have merged measures of stomatal regulation with xylem hydraulic safety strategies based on in situ field measurements. The goal of this study was to characterize the stomatal and xylem hydraulic safety strategies of woody species in the biodiverse Mediterranean-type ecosystem region of California. Measurements were conducted in situ when California was experiencing the most severe drought conditions in the past 1,200 years. We found coordination among stomatal, hydraulic, and standard leaf functional traits. For example, stem xylem vulnerability to cavitation (P50 ) was correlated with the water potential at stomatal closure (Pclose ); more resistant species had a more negative water potential at stomatal closure. The degree of isohydry-anisohydry, defined at Pclose -P50 , was correlated with the hydraulic safety margin across species; more isohydric species had a larger hydraulic safety margin. In addition, we report for the first time Pclose values below -10 MPa. Measuring these traits in a biodiverse region under exceptional drought conditions contributes to our understanding of plant drought responses.

Plant hydraulic responses to long-term dry season nitrogen deposition alter drought tolerance in a Mediterranean-type ecosystem.

Anthropogenic nitrogen (N) deposition represents a significant N input for many terrestrial ecosystems. N deposition can affect plants on scales ranging from photosynthesis to community composition, yet few studies have investigated how changes in N availability affect plant water relations. We tested the effects of N addition on plant water relations, hydraulic traits, functional traits, gas exchange, and leaf chemistry in a semi-arid ecosystem in Southern California using long-term experimental plots fertilized with N for over a decade. The dominant species were Artemisia california and Salvia mellifera at Santa Margarita Ecological Reserve and Adenostoma fasciculatum and Ceanothus greggii at Sky Oaks Field Station. All species, except Ceanothus, showed increased leaf N concentration, decreased foliar carbon to N ratio, and increased foliar N isotopic composition with fertilization, indicating that added N was taken up by study species, yet each species had a differing physiological response to long-term N addition. Dry season predawn water potentials were less negative with N addition for all species except Adenostoma, but there were no differences in midday water potentials, or wet season water potentials. Artemisia was particularly responsive, as N addition increased stem hydraulic conductivity, stomatal conductance, and leaf carbon isotopic composition, and decreased wood density. The alteration of water relations and drought resistance parameters with N addition in Artemisia, as well as Adenostoma, Ceanothus, and Salvia, indicate that N deposition can affect the ability of native Southern California shrubs to respond to drought.

Coordination of stem and leaf hydraulic conductance in southern California shrubs: a test of the hydraulic segmentation hypothesis.

Coordination of water movement among plant organs is important for understanding plant water use strategies. The hydraulic segmentation hypothesis (HSH) proposes that hydraulic conductance in shorter lived, 'expendable' organs such as leaves and longer lived, more 'expensive' organs such as stems may be decoupled, with resistance in leaves acting as a bottleneck or 'safety valve'. We tested the HSH in woody species from a Mediterranean-type ecosystem by measuring leaf hydraulic conductance (Kleaf) and stem hydraulic conductivity (KS). We also investigated whether leaves function as safety valves by relating Kleaf and the hydraulic safety margin (stem water potential minus the water potential at which 50% of conductivity is lost (Ψstem-Ψ50)). We also examined related plant traits including the operating range of water potentials, wood density, leaf mass per area, and leaf area to sapwood area ratio to provide insight into whole-plant water use strategies. For hydrated shoots, Kleaf was negatively correlated with KS , supporting the HSH. Additionally, Kleaf was positively correlated with the hydraulic safety margin and negatively correlated with the leaf area to sapwood area ratio. Consistent with the HSH, our data indicate that leaves may act as control valves for species with high KS , or a low safety margin. This critical role of leaves appears to contribute importantly to plant ecological specialization in a drought-prone environment.

Responses of functional traits to seven-year nitrogen addition in two tree species: coordination of hydraulics, gas exchange and carbon reserves.

Atmospheric nitrogen (N) deposition has been observed to impact plant structure and functional traits in terrestrial ecosystems. Although the effect of N deposition on plant water use has been well-evaluated in laboratories and in experimental forests, the linkages between water and carbon relations under N deposition are unclear. Here, we report on hydraulics, gas exchange and carbon reserves of two broad-leaved tree species (Quercus mongolica and Fraxinus mandshurica) in mature temperate forests after a seven-year experiment with different levels of N addition (control (CK), low (23 kg N ha-1 yr-1), medium (46 kg N ha-1 yr-1) and high (69 kg N ha-1 yr-1)). We investigated variation in hydraulic traits (xylem-specific hydraulic conductivity (Ks), native percentage loss of conductivity (PLC) and leaf water potential), xylem anatomy (vessel diameter and density), gas exchange (maximum net photosynthesis rate and stomatal conductance) and carbon reserves (soluble sugars, starch and total nonstructural carbohydrates (NSC)) with different N addition levels. We found that medium N addition significantly increased Ks and vessel diameter compared to control, but accompanied increasing PLC and decreasing leaf water potential, suggesting that N addition results in a greater hydraulic efficiency and higher risk of embolism. N addition promoted photosynthetic capacity via increasing foliar N concentration but did not change stomatal conductance. In addition, we found increase in foliar soluble sugar concentration and decrease in starch concentration with N addition, and positive correlations between hydraulic traits (vessel diameter and PLC) and soluble sugars. These coupled responses of tree hydraulics and carbon metabolism are consistent with a regulatory role of carbohydrates in maintaining hydraulic integrity. Our study provides an important insight into the relationship of plant water transport and carbon dynamics under increasing N deposition.

Testing the 'microbubble effect' using the Cavitron technique to measure xylem water extraction curves.

Plant resistance to xylem cavitation is a major drought adaptation trait and is essential to characterizing vulnerability to climate change. Cavitation resistance can be determined with vulnerability curves. In the past decade, new techniques have increased the ease and speed at which vulnerability curves are produced. However, these new techniques are also subject to new artefacts, especially as related to long-vesselled species. We tested the reliability of the 'flow rotor' centrifuge technique, the so-called Cavitron, and investigated one potential mechanism behind the open vessel artefact in centrifuge-based vulnerability curves: the microbubble effect. The microbubble effect hypothesizes that microbubbles introduced to open vessels, either through sample flushing or injection of solution, travel by buoyancy or mass flow towards the axis of rotation where they artefactually nucleate cavitation. To test the microbubble effect, we constructed vulnerability curves using three different rotor sizes for five species with varying maximum vessel length, as well as water extraction curves that are constructed without injection of solution into the rotor. We found that the Cavitron technique is robust to measure resistance to cavitation in tracheid-bearing and short-vesselled species, but not for long-vesselled ones. Moreover, our results support the microbubble effect hypothesis as the major cause for the open vessel artefact in long-vesselled species.

Can vessel dimension explain tolerance toward fungal vascular wilt diseases in woody plants? Lessons from Dutch elm disease and esca disease in grapevine.

This review illuminates key findings in our understanding of grapevine xylem resistance to fungal vascular wilt diseases. Grapevine (Vitis spp.) vascular diseases such as esca, botryosphaeria dieback, and eutypa dieback, are caused by a set of taxonomically unrelated ascomycete fungi. Fungal colonization of the vascular system leads to a decline of the plant host because of a loss of the xylem function and subsequent decrease in hydraulic conductivity. Fungal vascular pathogens use different colonization strategies to invade and kill their host. Vitis vinifera cultivars display different levels of tolerance toward vascular diseases caused by fungi, but the plant defense mechanisms underlying those observations have not been completely elucidated. In this review, we establish a parallel between two vascular diseases, grapevine esca disease and Dutch elm disease, and argue that the former should be viewed as a vascular wilt disease. Plant genotypes exhibit differences in xylem morphology and resistance to fungal pathogens causing vascular wilt diseases. We provide evidence that the susceptibility of three commercial V. vinifera cultivars to esca disease is correlated to large vessel diameter. Additionally, we explore how xylem morphological traits related to water transport are influenced by abiotic factors, and how these might impact host tolerance of vascular wilt fungi. Finally, we explore the utility of this concept for predicting which V. vinifera cultivars are most vulnerable of fungal vascular wilt diseases and propose new strategies for disease management.