Sap flow through partially embolized xylem vessel networks.

Sap is transported through numerous conduits in the xylem of woody plants along the path from the soil to the leaves. When all conduits are functional, vessel lumen diameter is a strong predictor of hydraulic conductivity. As vessels become embolized, sap movement becomes increasingly affected by factors operating at scales beyond individual conduits, creating resistances that result in hydraulic conductivity diverging from diameter-based estimates. These effects include pit resistances, connectivity, path length, network topology, and vessel or sector isolation. The impact of these factors varies with the level and distribution of emboli within the network, and manifest as alterations in the relationship between the number and diameter of embolized vessels with measured declines in hydraulic conductivity across vulnerability to embolism curves. Divergences between measured conductivity and diameter-based estimates reveal functional differences that arise because of species- and tissue-specific vessel network structures. Such divergences are not uniform, and xylem tissues may diverge in different ways and to differing degrees. Plants regularly operate under nonoptimal conditions and contain numerous embolized conduits. Understanding the hydraulic implications of emboli within a network and the function of partially embolized networks are critical gaps in our understanding of plants occurring within natural environments.

The impact of rising CO2 and acclimation on the response of US forests to global warming.

The response of forests to climate change depends in part on whether the photosynthetic benefit from increased atmospheric CO2 (∆Ca = future minus historic CO2) compensates for increased physiological stresses from higher temperature (∆T). We predicted the outcome of these competing responses by using optimization theory and a mechanistic model of tree water transport and photosynthesis. We simulated current and future productivity, stress, and mortality in mature monospecific stands with soil, species, and climate sampled from 20 continental US locations. We modeled stands with and without acclimation to ∆Ca and ∆T, where acclimated forests adjusted leaf area, photosynthetic capacity, and stand density to maximize productivity while avoiding stress. Without acclimation, the ∆Ca-driven boost in net primary productivity (NPP) was compromised by ∆T-driven stress and mortality associated with vascular failure. With acclimation, the ∆Ca-driven boost in NPP and stand biomass (C storage) was accentuated for cooler futures but negated for warmer futures by a ∆T-driven reduction in NPP and biomass. Thus, hotter futures reduced forest biomass through either mortality or acclimation. Forest outcomes depended on whether projected climatic ∆Ca/∆T ratios were above or below physiological thresholds that neutralized the negative impacts of warming. Critically, if forests do not acclimate, the ∆Ca/∆T must be above ca 89 ppm⋅°C-1 to avoid chronic stress, a threshold met by 55% of climate projections. If forests do acclimate, the ∆Ca/∆T must rise above ca 67 ppm⋅°C-1 for NPP and biomass to increase, a lower threshold met by 71% of projections.

Optimization theory explains nighttime stomatal responses.

Nocturnal transpiration is widely observed across species and biomes, and may significantly impact global water, carbon, and energy budgets. However, it remains elusive why plants lose water at night and how to model it at large scales. We hypothesized that plants optimize nighttime leaf diffusive conductance (gwn ) to balance potential daytime photosynthetic benefits and nocturnal transpiration benefits. We quantified nighttime benefits from respiratory reductions due to evaporative leaf cooling. We described nighttime costs in terms of a reduced carbon gain during the day because of water use at night. We measured nighttime stomatal responses and tested our model with water birch (Betula occidentalis) saplings grown in a glasshouse. The gwn of water birch decreased with drier soil, higher atmospheric CO2 , wetter air, lower leaf temperature, and lower leaf respiration rate. Our model predicted all these responses correctly, except for the response of gwn to air humidity. Our results also suggested that the slow decrease in gwn after sunset could be associated with decreasing leaf respiration. The optimality-based nocturnal transpiration model smoothly integrates with daytime stomatal optimization approaches, and thus has the potential to quantitatively predict nocturnal transpiration across space and time.

Understanding and predicting forest mortality in the western United States using long-term forest inventory data and modeled hydraulic damage.

Global warming is expected to exacerbate the duration and intensity of droughts in the western United States, which may lead to increased tree mortality. A prevailing proximal mechanism of drought-induced tree mortality is hydraulic damage, but predicting tree mortality from hydraulic theory and climate data still remains a major scientific challenge. We used forest inventory data and a plant hydraulic model (HM) to address three questions: can we capture regional patterns of drought-induced tree mortality with HM-predicted damage thresholds; do HM metrics improve predictions of mortality across broad spatial areas; and what are the dominant controls of forest mortality when considering stand characteristics, climate metrics, and simulated hydraulic stress? We found that the amount of variance explained by models predicting mortality was limited (R2 median = 0.10, R2 range: 0.00-0.52). HM outputs, including hydraulic damage and carbon assimilation diagnostics, moderately improve mortality prediction across the western US compared with models using stand and climate predictors alone. Among factors considered, metrics of stand density and tree size tended to be some of the most critical factors explaining mortality, probably highlighting the important roles of structural overshoot, stand development, and biotic agent host selection and outbreaks in mortality patterns.

Coupled whole-tree optimality and xylem hydraulics explain dynamic biomass partitioning.

Trees partition biomass in response to resource limitation and physiological activity. It is presumed that these strategies evolved to optimize some measure of fitness. If the optimization criterion can be specified, then allometry can be modeled from first principles without prescribed parameterization. We present the Tree Hydraulics and Optimal Resource Partitioning (THORP) model, which optimizes allometry by estimating allocation fractions to organs as proportional to their ratio of marginal gain to marginal cost, where gain is net canopy photosynthesis rate, and costs are senescence rates. Root total biomass and profile shape are predicted simultaneously by a unified optimization. Optimal partitioning is solved by a numerically efficient analytical solution. THORP's predictions agree with reported tree biomass partitioning in response to size, water limitations, elevated CO2 and pruning. Roots were sensitive to soil moisture profiles and grew down to the groundwater table when present. Groundwater buffered against water stress regardless of meteorology, stabilizing allometry and root profiles as deep as c. 30 m. Much of plant allometry can be explained by hydraulic considerations. However, nutrient limitations cannot be fully ignored. Rooting mass and profiles were synchronized with hydrological conditions and groundwater even at considerable depths, illustrating that the below ground shapes whole-tree allometry.

A theoretical and empirical assessment of stomatal optimization modeling.

Optimal stomatal control models have shown great potential in predicting stomatal behavior and improving carbon cycle modeling. Basic stomatal optimality theory posits that stomatal regulation maximizes the carbon gain relative to a penalty of stomatal opening. All models take a similar approach to calculate instantaneous carbon gain from stomatal opening (the gain function). Where the models diverge is in how they calculate the corresponding penalty (the penalty function). In this review, we compare and evaluate 10 different optimization models in how they quantify the penalty and how well they predict stomatal responses to the environment. We evaluate models in two ways. First, we compare their penalty functions against seven criteria that ensure a unique and qualitatively realistic solution. Second, we quantitatively test model against multiple leaf gas-exchange datasets. The optimization models with better predictive skills have penalty functions that meet our seven criteria and use fitting parameters that are both few in number and physiology based. The most skilled models are those with a penalty function based on stress-induced hydraulic failure. We conclude by proposing a new model that has a hydraulics-based penalty function that meets all seven criteria and demonstrates a highly predictive skill against our test datasets.

Use of hydraulic traits for modeling genotype-specific acclimation in cotton under drought.

Understanding the genetic and physiological basis of abiotic stress tolerance under field conditions is key to varietal crop improvement in the face of climate variability. Here, we investigate dynamic physiological responses to water stress in silico and their relationships to genotypic variation in hydraulic traits of cotton (Gossypium hirsutum), an economically important species for renewable textile fiber production. In conjunction with an ecophysiological process-based model, heterogeneous data (plant hydraulic traits, spatially-distributed soil texture, soil water content and canopy temperature) were used to examine hydraulic characteristics of cotton, evaluate their consequences on whole plant performance under drought, and explore potential genotype × environment effects. Cotton was found to have R-shaped hydraulic vulnerability curves (VCs), which were consistent under drought stress initiated at flowering. Stem VCs, expressed as percent loss of conductivity, differed across genotypes, whereas root VCs did not. Simulation results demonstrated how plant physiological stress can depend on the interaction between soil properties and irrigation management, which in turn affect genotypic rankings of transpiration in a time-dependent manner. Our study shows how a process-based modeling framework can be used to link genotypic variation in hydraulic traits to differential acclimating behaviors under drought.

Direct comparison of four methods to construct xylem vulnerability curves: Differences among techniques are linked to vessel network characteristics.

During periods of dehydration, water transport through xylem conduits can become blocked by embolism formation. Xylem embolism compromises water supply to leaves and may lead to losses in productivity or plant death. Vulnerability curves (VCs) characterize plant losses in conductivity as xylem pressures decrease. VCs are widely used to characterize and predict plant water use at different levels of water availability. Several methodologies for constructing VCs exist and sometimes produce different results for the same plant material. We directly compared four VC construction methods on stems of black cottonwood (Populus trichocarpa), a model tree species: dehydration, centrifuge, X-ray-computed microtomography (microCT), and optical. MicroCT VC was the most resistant, dehydration and centrifuge VCs were intermediate, and optical VC was the most vulnerable. Differences among VCs were not associated with how cavitation was induced but were related to how losses in conductivity were evaluated: measured hydraulically (dehydration and centrifuge) versus evaluated from visual information (microCT and optical). Understanding how and why methods differ in estimating vulnerability to xylem embolism is important for advancing knowledge in plant ecophysiology, interpreting literature data, and using accurate VCs in water flux models for predicting plant responses to drought.

Wood structure and function change with maturity: Age of the vascular cambium is associated with xylem changes in current-year growth.

Xylem vessel structure changes as trees grow and mature. Age- and development-related changes in xylem structure are likely related to changes in hydraulic function. We examined whether hydraulic function, including hydraulic conductivity and vulnerability to water-stress-induced xylem embolism, changed over the course of cambial development in the stems of 17 tree species. We compared current-year growth of young (1-4 years), intermediate (2-7 years), and older (3-10 years) stems occurring in series along branches. Diffuse and ring porous species were examined, but nearly all species produced only diffuse porous xylem in the distal branches that were examined irrespective of their mature xylem porosity type. Vessel diameter and length increased with cambial age. Xylem became both more conductive and more cavitation resistant with cambial age. Ring porous species had longer and wider vessels and xylem that had higher conductivity and was more vulnerable to cavitation; however, these differences between porosity types were not present in young stem samples. Understanding plant hydraulic function and architecture requires the sampling of multiple-aged tissues because plants may vary considerably in their xylem structural and functional traits throughout the plant body, even over relatively short distances and closely aged tissues.

A stomatal control model based on optimization of carbon gain versus hydraulic risk predicts aspen sapling responses to drought.

Empirical models of plant drought responses rely on parameters that are difficult to specify a priori. We test a trait- and process-based model to predict environmental responses from an optimization of carbon gain vs hydraulic risk. We applied four drought treatments to aspen (Populus tremuloides) saplings in a research garden. First we tested the optimization algorithm by using predawn xylem pressure as an input. We then tested the full model which calculates root-zone water budget and xylem pressure hourly throughout the growing season. The optimization algorithm performed well when run from measured predawn pressures. The per cent mean absolute error (MAE) averaged 27.7% for midday xylem pressure, transpiration, net assimilation, leaf temperature, sapflow, diffusive conductance and soil-canopy hydraulic conductance. Average MAE was 31.2% for the same observations when the full model was run from irrigation and rain data. Saplings that died were projected to exceed 85% loss in soil-canopy hydraulic conductance, whereas surviving plants never reached this threshold. The model fit was equivalent to that of an empirical model, but with the advantage that all inputs are specific traits. Prediction is empowered because knowing these traits allows knowing the response to climatic stress.

Predicting stomatal responses to the environment from the optimization of photosynthetic gain and hydraulic cost.

Stomatal regulation presumably evolved to optimize CO2 for H2 O exchange in response to changing conditions. If the optimization criterion can be readily measured or calculated, then stomatal responses can be efficiently modelled without recourse to empirical models or underlying mechanism. Previous efforts have been challenged by the lack of a transparent index for the cost of losing water. Yet it is accepted that stomata control water loss to avoid excessive loss of hydraulic conductance from cavitation and soil drying. Proximity to hydraulic failure and desiccation can represent the cost of water loss. If at any given instant, the stomatal aperture adjusts to maximize the instantaneous difference between photosynthetic gain and hydraulic cost, then a model can predict the trajectory of stomatal responses to changes in environment across time. Results of this optimization model are consistent with the widely used Ball-Berry-Leuning empirical model (r2 > 0.99) across a wide range of vapour pressure deficits and ambient CO2 concentrations for wet soil. The advantage of the optimization approach is the absence of empirical coefficients, applicability to dry as well as wet soil and prediction of plant hydraulic status along with gas exchange.

Plant xylem hydraulics: What we understand, current research, and future challenges.

Herein we review the current state-of-the-art of plant hydraulics in the context of plant physiology, ecology, and evolution, focusing on current and future research opportunities. We explain the physics of water transport in plants and the limits of this transport system, highlighting the relationships between xylem structure and function. We describe the great variety of techniques existing for evaluating xylem resistance to cavitation. We address several methodological issues and their connection with current debates on conduit refilling and exponentially shaped vulnerability curves. We analyze the trade-offs existing between water transport safety and efficiency. We also stress how little information is available on molecular biology of cavitation and the potential role of aquaporins in conduit refilling. Finally, we draw attention to how plant hydraulic traits can be used for modeling stomatal responses to environmental variables and climate change, including drought mortality.

The standard centrifuge method accurately measures vulnerability curves of long-vesselled olive stems.

The standard centrifuge method has been frequently used to measure vulnerability to xylem cavitation. This method has recently been questioned. It was hypothesized that open vessels lead to exponential vulnerability curves, which were thought to be indicative of measurement artifact. We tested this hypothesis in stems of olive (Olea europea) because its long vessels were recently claimed to produce a centrifuge artifact. We evaluated three predictions that followed from the open vessel artifact hypothesis: shorter stems, with more open vessels, would be more vulnerable than longer stems; standard centrifuge-based curves would be more vulnerable than dehydration-based curves; and open vessels would cause an exponential shape of centrifuge-based curves. Experimental evidence did not support these predictions. Centrifuge curves did not vary when the proportion of open vessels was altered. Centrifuge and dehydration curves were similar. At highly negative xylem pressure, centrifuge-based curves slightly overestimated vulnerability compared to the dehydration curve. This divergence was eliminated by centrifuging each stem only once. The standard centrifuge method produced accurate curves of samples containing open vessels, supporting the validity of this technique and confirming its utility in understanding plant hydraulics. Seven recommendations for avoiding artefacts and standardizing vulnerability curve methodology are provided.

Excising stem samples underwater at native tension does not induce xylem cavitation.

Xylem resistance to water stress-induced cavitation is an important trait that is associated with drought tolerance of plants. The level of xylem cavitation experienced by a plant is often assessed as the percentage loss in conductivity (PLC) at different water potentials. Such measurements are constructed with samples that are excised underwater at native tensions. However, a recent study concluded that cutting conduits under significant tension induced cavitation, even when samples were held underwater during cutting. This resulted in artificially increased PLC because of what we have termed a 'tension-cutting artefact'. We tested the hypothesized tension-cutting artefact on five species by measuring PLC at native tension compared with after xylem tensions had been relaxed. Our results did not support the tension-cutting artefact hypothesis, as no differences were observed between native and relaxed samples in four of five species. In a fifth species (Laurus nobilis), differences between native and relaxed samples appear to be due to vessel refilling rather than a tension-cutting effect. We avoided the tension-cutting artefact by cutting samples to slightly longer than their measurement length and subsequent trimming of at least 0.5 cm of sample ends prior to measurement.

The stomatal response to rising CO2 concentration and drought is predicted by a hydraulic trait-based optimization model.

Modeling stomatal control is critical for predicting forest responses to the changing environment and hence the global water and carbon cycles. A trait-based stomatal control model that optimizes carbon gain while avoiding hydraulic risk has been shown to perform well in response to drought. However, the model's performance against changes in atmospheric CO2, which is rising rapidly due to human emissions, has yet to be evaluated. The present study tested the gain-risk model's ability to predict the stomatal response to CO2 concentration with potted water birch (Betula occidentalis Hook.) saplings in a growth chamber. The model's performance in predicting stomatal response to changes in atmospheric relative humidity and soil moisture was also assessed. The gain-risk model predicted the photosynthetic assimilation, transpiration rate and leaf xylem pressure under different CO2 concentrations, having a mean absolute percentage error (MAPE) of 25%. The model also predicted the responses to relative humidity and soil drought with a MAPE of 21.9% and 41.9%, respectively. Overall, the gain-risk model had an MAPE of 26.8% compared with the 37.5% MAPE obtained by a standard empirical model of stomatal conductance. Importantly, unlike empirical models, the optimization model relies on measurable physiological traits as inputs and performs well in predicting responses to novel environmental conditions without empirical corrections. Incorporating the optimization model in larger scale models has the potential for improving the simulation of water and carbon cycles.

Single vessel air injection estimates of xylem resistance to cavitation are affected by vessel network characteristics and sample length.

Xylem resistance to cavitation is an important trait that is related to the ecology and survival of plant species. Vessel network characteristics, such as vessel length and connectivity, could affect the spread of emboli from gas-filled vessels to functional ones, triggering their cavitation. We hypothesized that the cavitation resistance of xylem vessels is randomly distributed throughout the vessel network. We predicted that single vessel air injection (SVAI) vulnerability curves (VCs) would thus be affected by sample length. Longer stem samples were predicted to appear more resistant than shorter samples due to the sampled path including greater numbers of vessels. We evaluated the vessel network characteristics of grapevine (Vitis vinifera L.), English oak (Quercus robur L.) and black cottonwood (Populus trichocarpa Torr. & A. Gray), and constructed SVAI VCs for 5- and 20-cm-long segments. We also constructed VCs with a standard centrifuge method and used computer modelling to estimate the curve shift expected for pathways composed of different numbers of vessels. For all three species, the SVAI VCs for 5 cm segments rose exponentially and were more vulnerable than the 20 cm segments. The 5 cm curve shapes were exponential and were consistent with centrifuge VCs. Modelling data supported the observed SVAI VC shifts, which were related to path length and vessel network characteristics. These results suggest that exponential VCs represent the most realistic curve shape for individual vessel resistance distributions for these species. At the network level, the presence of some vessels with a higher resistance to cavitation may help avoid emboli spread during tissue dehydration.

Chaparral Shrub Hydraulic Traits, Size, and Life History Types Relate to Species Mortality during California's Historic Drought of 2014.

Chaparral is the most abundant vegetation type in California and current climate change models predict more frequent and severe droughts that could impact plant community structure. Understanding the factors related to species-specific drought mortality is essential to predict such changes. We predicted that life history type, hydraulic traits, and plant size would be related to the ability of species to survive drought. We evaluated the impact of these factors in a mature chaparral stand during the drought of 2014, which has been reported as the most severe in California in the last 1,200 years. We measured tissue water potential, native xylem specific conductivity, leaf specific conductivity, percentage loss in conductivity, and chlorophyll fluorescence for 11 species in February 2014, which was exceptionally dry following protracted drought. Mortality among the 11 dominant species ranged from 0 to 93%. Total stand density was reduced 63.4% and relative dominance of species shifted after the drought. Mortality was negatively correlated with water potential, native xylem specific conductivity, and chlorophyll fluorescence, but not with percent loss in hydraulic conductivity and leaf specific conductivity. The model that best explained mortality included species and plant size as main factors and indicated that larger plants had greater survival for 2 of the species. In general, species with greater resistance to water-stress induced cavitation showed greater mortality levels. Despite adult resprouters typically being more vulnerable to cavitation, results suggest that their more extensive root systems enable them to better access soil moisture and avoid harmful levels of dehydration. These results are consistent with the hypothesis that short-term high intensity droughts have the strongest effect on mature plants of shallow-rooted dehydration tolerant species, whereas deep-rooted dehydration avoiding species fare better in the short-term. Severe droughts can drive changes in chaparral structure as a result of the differential mortality among species.