Climate change exposes vegetation to unusual drought, causing declines in productivity and increased mortality. Drought responses are hard to anticipate because canopy transpiration and diffusive ...conductance (G) respond to drying soil and vapor pressure deficit (D) in complex ways. A growing database of hydraulic traits, combined with a parsimonious theory of tree water transport and its regulation, may improve predictions of at-risk vegetation. The theory uses the physics of flow through soil and xylem to quantify how canopy water supply declines with drought and ceases by hydraulic failure. This transpiration ‘supply function’ is used to predict a water ‘loss function’ by assuming that stomatal regulation exploits transport capacity while avoiding failure. Supply–loss theory incorporates root distribution, hydraulic redistribution, cavitation vulnerability, and cavitation reversal. The theory efficiently defines stomatal responses to D, drying soil, and hydraulic vulnerability. Driving the theory with climate predicts drought-induced loss of plant hydraulic conductance (k), canopy G, carbon assimilation, and productivity. Data lead to the ‘chronic stress hypothesis’ wherein > 60% loss of k increases mortality by multiple mechanisms. Supply–loss theory predicts the climatic conditions that push vegetation over this risk threshold. The theory's simplicity and predictive power encourage testing and application in large-scale modeling.
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.
Water is transported in xylem conduits from the soil to the leaves under negative pressures. This is a metabolically inexpensive transport system but it is subjected to the risk of cavitation failure. Herein we address methodologies for measuring xylem resistance to cavitation, current debates, and future research opportunities in plant hydraulics.
Recent decades have been characterized by increasing temperatures worldwide, resulting in an exponential climb in vapor pressure deficit (VPD). VPD has been identified as an increasingly important ...driver of plant functioning in terrestrial biomes and has been established as a major contributor in recent drought-induced plant mortality independent of other drivers associated with climate change. Despite this, few studies have isolated the physiological response of plant functioning to high VPD, thus limiting our understanding and ability to predict future impacts on terrestrial ecosystems. An abundance of evidence suggests that stomatal conductance declines under high VPD and transpiration increases in most species up until a given VPD threshold, leading to a cascade of subsequent impacts including reduced photosynthesis and growth, and higher risks of carbon starvation and hydraulic failure. Incorporation of photosynthetic and hydraulic traits in ‘next-generation’ land-surface models has the greatest potential for improved prediction of VPD responses at the plant- and global-scale, and will yield more mechanistic simulations of plant responses to a changing climate. By providing a fully integrated framework and evaluation of the impacts of high VPD on plant function, improvements in forecasting and long-term projections of climate impacts can be made.
During droughts, leaves are predicted to act as ‘hydraulic fuses’ by shedding when plants reach critically low water potential (Ψplant), thereby slowing water loss, stabilizing Ψplant and protecting ...against cavitation-induced loss of stem hydraulic conductivity (K
s).
We tested these predictions among trees in seasonally dry tropical forests, where leaf shedding is common, yet variable, among species. We tracked leaf phenology, Ψplant and K
s in saplings of six tree species distributed across two forests.
Species differed in their timing and extent of leaf shedding, yet converged in shedding leaves as they approached the Ψplant value associated with a 50% loss of K
s and at which their model-estimated maximum sustainable transpiration rate approached zero. However, after shedding all leaves, the Ψplant value of one species, Genipa americana, continued to decline, indicating that water loss continued after leaf shedding. K
s was highly variable among saplings within species and seasons, suggesting a minimal influence of seasonal drought on K
s.
Hydraulic limits appear to drive diverse patterns of leaf shedding among tropical trees, supporting the hydraulic fuse hypothesis. However, leaf shedding is not universally effective at stabilizing Ψplant, suggesting that the main function of drought deciduousness may vary among species.
Stomatal regulation presumably evolved to optimize CO2 for H2O 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.
Current land surface models struggle to represent the complex and species‐specific manner by which stomata respond to environmental cues, especially soil drought. This paper offers a solution to this problem by assuming that the goal of stomatal regulation is to maximize photosynthetic gain minus hydraulic cost. A trait‐ and process‐based ‘profit‐maximizing’ algorithm predicts realistic stomatal behaviour in response to the gamut of environmental stimuli. This new approach to stomatal optimization theory may prove useful in large‐scale modelling of responses to climate change.
Plants influence the atmosphere through fluxes of carbon, water and energy
, and can intensify drought through land-atmosphere feedback effects
. The diversity of plant functional traits in forests, ...especially physiological traits related to water (hydraulic) transport, may have a critical role in land-atmosphere feedback, particularly during drought. Here we combine 352 site-years of eddy covariance measurements from 40 forest sites, remote-sensing observations of plant water content and plant functional-trait data to test whether the diversity in plant traits affects the response of the ecosystem to drought. We find evidence that higher hydraulic diversity buffers variation in ecosystem flux during dry periods across temperate and boreal forests. Hydraulic traits were the predominant significant predictors of cross-site patterns in drought response. By contrast, standard leaf and wood traits, such as specific leaf area and wood density, had little explanatory power. Our results demonstrate that diversity in the hydraulic traits of trees mediates ecosystem resilience to drought and is likely to have an important role in future ecosystem-atmosphere feedback effects in a changing climate.
Climate change is expected to lead to increases in drought frequency and severity, with deleterious effects on many ecosystems. Stomatal responses to changing environmental conditions form the ...backbone of all ecosystem models, but are based on empirical relationships and are not well-tested during drought conditions. Here, we use a dataset of 34 woody plant species spanning global forest biomes to examine the effect of leaf water potential on stomatal conductance and test the predictive accuracy of three major stomatal models and a recently proposed model. We find that current leaf-level empirical models have consistent biases of over-prediction of stomatal conductance during dry conditions, particularly at low soil water potentials. Furthermore, the recently proposed stomatal conductance model yields increases in predictive capability compared to current models, and with particular improvement during drought conditions. Our results reveal that including stomatal sensitivity to declining water potential and consequent impairment of plant water transport will improve predictions during drought conditions and show that many biomes contain a diversity of plant stomatal strategies that range from risky to conservative stomatal regulation during water stress. Such improvements in stomatal simulation are greatly needed to help unravel and predict the response of ecosystems to future climate extremes.
Land plants need water to replace the evaporation that occurs while atmospheric CO2 is diffusing into photosynthetic tissue. The water-for-carbon exchange rate is poor, and evolutionary history ...indicates a progression of innovations for cheap water transport-beginning in order with capillary suction at cell walls, stomatal regulation, hydroids, tracheids, secondary xylem, endodermis, and vessels. The radiation of plants in the Silurian and Devonian occurred when the need for water was at an all-time low because of high CO2 concentration. Transport improvements appeared as water demand increased and CO2 dropped to current values in the Carboniferous and Permian. Stomatal regulation and high-conductivity conduits permitted larger plants and a transition from poikilohydric to homoiohydric water relations. The evolution of conduits from hydroids through tracheids to vessels reflects the need to balance resistance to implosion and cavitation versus maximum hydraulic conductance and minimum conduit investment. Localization of rigidifying lignin away from the lumen surface and porous wall regions during tracheid evolution, and the origin of pits, acted to maintain wall strength and permeability while minimizing cavitation. Vessels mark the pinnacle of efficiency, making vines and dense, stiff woods possible without sacrificing conductivity or cavitation resistance. However, vessels make cavitation-resistant wood more expensive and may compromise refilling efficiency versus tracheids. Vascular networks maximize hydraulic conductivity and protection from cavitation at minimum investment by following Murray's law and localizing resistances to the periphery. A future challenge is to quantify the significance of xylem structure in terms of the carbon cost of transpiration and the net carbon profit via gas exchange.
Fine-scale interconduit pit modifications regulating drought-induced embolism. Display omitted
► The hydraulic pathway of plants is vulnerable to develop air bubbles. ► Air bubble formation in plants ...is caused by drought or freeze–thaw events. ► Various mechanical xylem properties are correlated with drought-induced embolisms. ► Angiosperms have a greater ability to repair stem embolisms than gymnosperms. ► Secondarily woody shrubs are more embolism resistant than herbaceous relatives.
One adaptation of plants to cope with drought or frost stress is to develop wood that is able to withstand the formation and distribution of air bubbles (emboli) in its water conducting xylem cells under negative pressure. The ultrastructure of interconduit pits strongly affects drought-induced embolism resistance, but also mechanical properties of the xylem are involved. The first experimental evidence for a lower embolism resistance in stems of herbaceous plants compared to stems of their secondarily woody descendants further supports this mechanical-functional trade-off. An integrative approach combining (ultra)structural observations of the xylem, safety-efficiency aspects of the hydraulic pipeline, and xylem–phloem interactions will shed more light on the multiple adaptive strategies of embolism resistance in plants.
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 soilcanopy 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.
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