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Leaves as bottlenecks: The contribution of tree leaves to hydraulic resistance within the soil‐plant‐atmosphere continuum
Abstract
Within vascular plants, the partitioning of hydraulic resistance along the soil‐to‐leaf continuum affects transpiration and its response to environmental conditions. In trees, the fractional contribution of leaf hydraulic resistance (Rleaf) to total soil‐to‐leaf hydraulic resistance (Rtotal), or fRleaf (= Rleaf/Rtotal), is thought to be large, but this has not been tested comprehensively. We compiled a multi‐biome dataset of fRleaf using new and previously published measurements of pressure differences within trees in situ. Across 80 samples, fRleaf averaged 0.51 (95% CI = 0.46, 0.57) and it declined with tree height. We also used the allometric relationship between field‐based measurements of soil‐to‐leaf hydraulic conductance and laboratory‐based measurements of leaf hydraulic conductance to compute the average fRleaf for 19 tree samples, which was 0.40 (95% CI = 0.29, 0.56). The in‐situ technique produces a more accurate descriptor of fRleaf because it accounts for dynamic leaf hydraulic conductance. Both approaches demonstrate the outsized role of leaves in controlling tree hydrodynamics. A larger fRleaf may play a role in protecting stems from loss of hydraulic conductance. Thus, the decline in fRleaf with tree height would contribute to greater drought vulnerability in taller trees and potentially to their observed disproportionate drought mortality. This article is protected by copyright. All rights reserved.
... The thickness of the double-wall (t) divided by the width of the lumen (b) is widely applied to reflect the mechanical resistance against tracheid implosion due to increased negative pressure during drought (Hacke et al., 2001;Jansen et al., 2009), relating to woody density (Lachenbruch and McCulloh, 2014) and hydraulic vulnerability (Blackman et al., 2010;Jordan et al., 2013). Interestingly, in L. sibirica, no significant (all p > 0.05) relations were found between E(t/b) 2 , L (t/b) 2 , Leaf(t/b) 2 and RGR branch (Fig. 7a, 7b and 7c), suggesting that hydraulic vulnerability is not coupled with performance in field, consistent with some studies (Martínez-Vilalta et al., 2009), probably due to the pit-margo structural regulation (Domec and Gartner, 2003;Isasa et al., 2023) in sapwood, and the reversible tracheid's collapse when drought occurred in pine needles (Cochard et al., 2004;Wolfe et al., 2023;Zhang et al., 2023). In P. obovata, no relation between E (t/b) 2 and RGR branch , as well as a strong positive relation between L (t/b) 2 and RGR branch were observed. ...
Despite inter-specific differences in hydraulic traits at broad scale have been comprehensively studied, intra- specific hydraulic variability in situ is less well known. Which hydraulic traits can better predict whole-plant performance in field both within and across species remains largely ambiguous. In the study, we conducted a field investigation on branch radial growth, leaf and branch anatomical traits related to hydraulics, as well as leaf pressure–volume curve parameters of two dominant conifer species (Larix sibirica and Picea obovata) at four sites over an aridity gradient across the Altay Mountain range, which locates at the southern edge of Taiga ecosystem, one of the largest and the most sensitive terrestrial biomes to climate change. L. sibirica is a generalist deciduous conifer species, while P. obovata is a specialist evergreen conifer species. It was found that: 1) P. obovata showed ten times higher slope of branch radial growth (RGRbranch) fitted to aridity than L. sibirica; 2) the hydraulic distance from the bundle sheath to the stomata (DMC) can predict the growth rate both within and across species; 3) earlywood and latewood anatomies showed different relations to RGRbranch within and across species; 4) leaf saturated osmotic potential (Ψsat) but not turgor loss osmotic potential (Ψtlp) was significantly and positively related to RGRbranch within species. Our results support the hypothesis that specialists are more sensitive in growth to climate change than generalists. Further, the results highlight DMC as a pivotal role in water transport and associated carbon assimilation both within and across species in Taiga ecosystem, therefore at the core of the structural adjustments to climate change in this largest and the most sensitive terrestrial biome.
... Leaves and roots represent the primary regions of resistance to the flow of water within a plant: in both cases due to the necessary flow path outside the xylem where very large frictional costs are incurred as water moves between and into the living cells (Tyree & Cheung, 1977;Frensch & Steudle, 1989;Steudle & Peterson, 1998;Wolfe et al., 2023). Leaves play an essential role in photosynthesis and transpiration and have commonly been observed to cavitate earlier than stems during drought (Choat et al., 2005;Brodribb & Cochard, 2009;Nolf et al., 2015;Charrier et al., 2016;Zhu et al., 2016;Scoffoni & Sack, 2017;Skelton et al., 2019;Mantova et al., 2023), although exceptions exist (Klepsch et al., 2018;Levionnois et al., 2020;Guan et al., 2022). ...
The propagation of xylem embolism throughout the root systems of drought‐affected plants remains largely unknown, despite this process being comparatively well characterized in aboveground tissues.
We used optical and X‐ray imaging to capture xylem embolism propagation across the intact root systems of bread wheat ( Triticum aestivum L. ‘Krichauff’) plants subjected to drying. Patterns in vulnerability to xylem cavitation were examined to investigate whether vulnerability may vary based on root size and placement across the entire root system.
Individual plants exhibited similar mean whole root system vulnerabilities to xylem cavitation but showed enormous 6 MPa variation within their component roots ( c . 50 roots per plant). Xylem cavitation typically initiated in the smallest, peripheral parts of the root system and moved inwards and upwards towards the root collar last, although this trend was highly variable.
This pattern of xylem embolism spread likely results in the sacrifice of replaceable small roots while preserving function in larger, more costly central roots. A distinct pattern of embolism‐spread belowground has implications for how we understand the impact of drought in the root system as a critical interface between plant and soil.
... The field of leaf hydraulics has grown in the last 15 years, following the discovery that leaves act as a hydraulic bottleneck in trees, accounting for more than 30 % of the hydraulic resistance in the soilplant-atmosphere continuum (Sack et al., 2003;Sack and Holbrook, 2006;Sack and Tyree, 2005;Scoffoni et al., 2011;Wolfe et al., 2022). More than 40 trillion tonnes of water traverse leaves each year (Chahine, 1992). ...
Background and aims:
Many succulent species are characterised by the presence of crassulacean acid metabolism (CAM) and/or elevated bulk hydraulic capacitance (CFT). Both CAM and elevated CFT substantially reduce the rate at which water moves through transpiring leaves. However, little is known about how these physiological adaptations are coordinated with leaf vascular architecture.
Methods:
The genus Clusia contains species spanning the entire C3-CAM continuum, and also is known to have > five-fold interspecific variation in CFT. We used this highly diverse genus to explore how interspecific variation in leaf vein density is coordinated with CAM and CFT.
Key results:
We found that constitutive CAM phenotypes were associated with lower vein length per leaf area (VLA) and vein termini density (VTD), compared to C3 or facultative CAM species. However, when vein densities were standardised by leaf thickness, this value was higher in CAM than C3 species, which is likely an adaptation to overcome apoplastic hydraulic resistance in deep chlorenchyma tissue. In contrast, CFT did not correlate with any xylem anatomical trait measured, suggesting CAM has a greater impact on leaf transpiration rates than CFT.
Conclusions:
Our findings strongly suggest that CAM photosynthesis is coordinated with leaf vein densities. The link between CAM and vascular anatomy will be important to consider when attempting to bioengineer CAM into C3 crops.
Significance
Plant vascular systems play a central role in global water and carbon cycles and drought resistance. These vascular systems perform multiple functions that affect the fitness of plants, and trade-offs are present among these functions. Some trade-offs are well established, but studies have not examined the full suite of functions of these complex systems. Here, we used a powerful multivariate method, structural equation modeling, to test hypotheses about the trade-offs that govern this vital and globally important tissue. We show that xylem traits are broadly governed by trade-offs related to transport, mechanical support, and storage, which are rooted in cellular structure, and that the level of dehydration experienced by plants in the field exerts a strong influence over these relationships.
Intensified droughts are affecting tropical forests across the globe. However, the underlying mechanisms of tree drought response and mortality are poorly understood. Hydraulic traits and especially hydraulic safety margins (HSMs), that is, the extent to which plants buffer themselves from thresholds of water stress, provide insights into species‐specific drought vulnerability. We investigated hydraulic traits during an intense drought triggered by the 2015–2016 El Niño on 27 canopy tree species across three tropical forest sites with differing precipitation. We capitalized on the drought event as a time when plant water status might approach or exceed thresholds of water stress. We investigated the degree to which these traits varied across the rainfall gradient, as well as relationships among hydraulic traits and species‐specific optimal moisture and mortality rates. There were no differences among sites for any measured trait. There was strong coordination among traits, with a network analysis revealing two major groups of coordinated traits. In one group, there were water potentials, turgor loss point, sapwood capacitance and density, HSMs, and mortality rate. In the second group, there was leaf mass per area, leaf dry matter content, hydraulic architecture (leaf area to sapwood area ratio), and species‐specific optimal moisture. These results demonstrated that while species with greater safety from turgor loss had lower mortality rates, hydraulic architecture was the only trait that explained species’ moisture dependency. Species with a greater leaf area to sapwood area ratio were associated with drier sites and reduced their transpirational demand during the dry season via deciduousness.
Abstract in Spanish is available with online material.
Climate change-driven increases in drought frequency and severity could compromise forest ecosystems and the terrestrial carbon sink1–3. While the impacts of single droughts on forests have been widely studied4–6, understanding whether forests acclimate to or become more vulnerable to sequential droughts remains largely unknown and is crucial for predicting future forest health. We combine cross-biome datasets of tree growth, tree mortality and ecosystem water content to quantify the effects of multiple droughts at a range of scales from individual trees to the globe from 1900 to 2018. We find that subsequent droughts generally have a more deleterious impact than initial droughts, but this effect differs enormously by clade and ecosystem, with gymnosperms and conifer-dominated ecosystems more often exhibiting increased vulnerability to multiple droughts. The differential impacts of multiple droughts across clades and biomes indicate that drought frequency changes may have fundamentally different ecological and carbon-cycle consequences across ecosystems.
Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere–atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function
Stomata regulate CO2 uptake for photosynthesis and water loss through transpiration. The approaches used to represent stomatal conductance (gs) in models vary. In particular, current understanding of drivers of the variation in a key parameter in those models, the slope parameter (i.e. a measure of intrinsic plant water‐use‐efficiency), is still limited, particularly in the tropics. Here we collected diurnal measurements of leaf gas exchange and leaf water potential (Ψleaf), and a suite of plant traits from the upper canopy of 15 tropical trees in two contrasting Panamanian forests throughout the dry season of the 2016 El Niño. The plant traits included wood density, leaf‐mass‐per‐area (LMA), leaf carboxylation capacity (Vc,max), leaf water content, the degree of isohydry, and predawn Ψleaf. We first investigated how the choice of four commonly used leaf‐level gs models with and without the inclusion of Ψleaf as an additional predictor variable influence the ability to predict gs, and then explored the abiotic (i.e. month, site‐month interaction) and biotic (i.e. tree‐species‐specific characteristics) drivers of slope parameter variation. Our results show that the inclusion of Ψleaf did not improve model performance and that the models that represent the response of gs to vapor pressure deficit performed better than corresponding models that respond to relative humidity. Within each gs model, we found large variation in the slope parameter, and this variation was attributable to the biotic driver, rather than abiotic drivers. We further investigated potential relationships between the slope parameter and the six available plant traits mentioned above, and found that only one trait, LMA, had a significant correlation with the slope parameter (R2=0.66, n=15), highlighting a potential path towards improved model parameterization. This study advances understanding of gs dynamics over seasonal drought, and identifies a practical, trait‐based approach to improve modeling of carbon and water exchange in tropical forests. This article is protected by copyright. All rights reserved.
Forest leaf area has enormous leverage on the carbon cycle because it mediates both forest productivity and resilience to climate extremes. Despite widespread evidence that trees are capable of adjusting to changes in environment across both space and time through modifying carbon allocation to leaves, many vegetation models use fixed carbon allocation schemes independent of environment, which introduces large uncertainties into predictions of future forest responses to atmospheric CO2 fertilization and anthropogenic climate change. Here, we develop an optimization‐based model whereby tree carbon allocation to leaves is an emergent property of environment and plant hydraulic traits. Using a combination of meta‐analysis, observational datasets, and model predictions, we find strong evidence that optimal hydraulic‐carbon coupling explains observed patterns in leaf allocation across large environmental and CO2 concentration gradients. Further, testing the sensitivity of leaf allocation strategy to a diversity in hydraulic and economic spectrum physiological traits, we show that plant hydraulic traits in particular have an enormous impact on the global change response of forest leaf area. Our results provide a rigorous theoretical underpinning for improving carbon cycle predictions through advancing model predictions of leaf area and underscore that tree‐level carbon allocation to leaves should be derived from first principles using mechanistic plant hydraulic processes in the next generation of vegetation models.
This article is protected by copyright. All rights reserved.
Loblolly pine plantations in the western portion of the species’ range are sometimes planted with genotypes from the eastern portion of its range to improve plantation productivity. Advances in loblolly pine breeding have led to the development of clonally propagated genotypes with higher potential growth rates and better form than more commonly planted half-sib genotypes. At a site in the western portion of the loblolly pine range, four genotypes from the eastern portion of the loblolly pine range were established. Two genotypes (HS756 and HS8103) were half-sib, and two genotypes (V9 and V93) were varieties. The V93 genotype was propagated from the HS756 genotype. The objective of this study was to determine the effects of genotype on seasonal trends in gas exchange parameters at the leaf and crown levels, growth, and biomass allocation patterns. During the two-year study, one year had precipitation and temperature trends similar to the long-term average and one year had extreme drought, with record heat. The HS756, V9, and V93 genotypes had the highest height growth throughout the study. The V93 genotype was sensitive to the drought; its leaf- and crown-level Asat and gs , declined during the drought more markedly than those of the other genotypes. Although its Asat and gs were affected by drought, height growth productivity of V93 may have been sustained during the drought by its biomass partitioning pattern of allocating higher proportions of its root biomass to small and fine roots and its aboveground biomass to foliage. These results suggest that a variety such as V93 could be more susceptible to changes in C fixation and water uptake with recurrent drought.
The capacity of plant species to resist xylem cavitation is an important determinant of resistance to drought, mortality thresholds, geographic distribution and productivity. Unravelling the role of xylem cavitation vulnerability in plant evolution and adaptation requires a clear understanding of how this key trait varies between the tissues of individuals and between individuals of species.
Here, we examine questions of variation within individuals by measuring how cavitation
moves between organs of individual plants. Using multiple cameras placed simultaneously on roots, stems and leaves, we were able to record systemic xylem cavitation during drying of individual olive plants.
Unlike previous studies, we found a consistent pattern of root > stem > leaf in terms of
xylem resistance to cavitation. The substantial variation in vulnerability to cavitation, evident among individuals, within individuals and within tissues of olive seedlings, was coordinated such that plants with more resistant roots also had more resistant leaves.
Preservation of root integrity means that roots can continue to supply water for the regeneration of drought-damaged aerial tissues after post-drought rain. Furthermore, coordinated variation in vulnerability between leaf, stem and root in olive plants suggests a strong selective pressure to maintain a fixed order of cavitation during drought.
Resolving the drivers of hydraulic decline during drought is crucial for understanding drought tolerance in crops and natural ecosystems. In the past 15 years, studies of the decline of leaf hydraulic conductance (Kleaf) have supported a major role in controlling plant drought responses. We analyzed the variation in Kleaf decline with dehydration in a global database of 310 species, providing novel insights into its underlying mechanisms, its co-ordination with stem hydraulics, its influence on gas exchange and drought tolerance, and its linkage with species ecological distributions. Kleaf vulnerability varied strongly within and across lineages, growth forms, and biomes. A critical literature review indicates that changes in hydraulic conductance outside the xylem with dehydration drive the overall decline of Kleaf. We demonstrate a significant leaf hydraulic safety-efficiency trade-off across angiosperm species and discuss the importance of the large variation around this trend. Leaves tend to be more vulnerable than stems, with their vulnerabilities co-ordinated across species, and importantly linked with adaptation across biomes. We hypothesize a novel framework to explain diversity across species in the co-ordination of Kleaf and gas exchange during dehydration. These findings reflect considerable recent progress, yet new tools for measurement, visualization, and modeling will result in ongoing discoveries important across fields in plant biology.
Many plant species experience large differences in soil moisture availability within a season, potentially leading to a wide range of leaf water potentials (Ψ LEAF ). In order to decrease the risk of leaf dehydration, among species, there is a continuum ranging from strict control (isohydry) to little control (anisohydry) of minimum Ψ LEAF .
In central Texas USA, species are exposed to a range of soil moisture from wet springs to hot, dry summers. There are diverging water management strategies among the four dominant woody species in this system; two of these species are more isohydric ( Prosopis glandulosa , Quercus fusiformis ) while two others are more anisohydric ( Diospyros texana , Juniperus asheii ).
To maintain leaf turgor and photosynthesis during periods of limited soil moisture, anisohydric species may adjust leaf hydraulic parameters more than isohydric species. To test this hypothesis, we quantified iso/anisohydry from 3 years of Ψ LEAF predawn and midday measurements, and we measured the changes in turgor loss points (Ψ TLP ), osmotic potential at full hydration (Ψ π100 ), and resistance to leaf hydraulic dysfunction (leaf P 50 ) throughout the spring and summer of 2016.
Diospyros and Juniperus experienced more negative Ψ LEAF and adjusted Ψ TLP and Ψ π100 in response to both drying soils during the summer also in response to rainfall events during September. In contrast, the more isohydric species ( Quercus and Prosopis ) did not appear to adjust Ψ TLP or Ψ π100 in response to soil moisture. The more anisohydric species also adjusted leaf P 50 during periods of reduced soil moisture.
Our results suggest that species that experience wider ranges of Ψ LEAF have a greater ability to alter leaf hydraulic properties. This provides insight on how species with different strategies for water potential regulation may modify properties to mitigate drought effects in the future.
A plain language summary is available for this article.
Numerous current efforts seek to improve the representation of ecosystem ecology and vegetation demographic processes within Earth System Models (ESMs). These developments are widely viewed as an important step in developing greater realism in predictions of future ecosystem states and fluxes. Increased realism, however, leads to increased model complexity, with new features raising a suite of ecological questions that require empirical constraints. Here, we review the developments that permit the representation of plant demographics in ESMs, and identify issues raised by these developments that highlight important gaps in ecological understanding. These issues inevitably translate into uncertainty in model projections but also allow models to be applied to new processes and questions concerning the dynamics of real-world ecosystems. We argue that stronger and more innovative connections to data, across the range of scales considered, are required to address these gaps in understanding. The development of first-generation land surface models as a unifying framework for ecophysiological understanding stimulated much research into plant physiological traits and gas exchange. Constraining predictions at ecologically relevant spatial and temporal scales will require a similar investment of effort and intensified inter-disciplinary communication. This article is protected by copyright. All rights reserved.
Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere-atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.
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 exponential shape vulnerability curves. We analyze the trade-offs existing between water transport safety and efficiency. We also stress how limited is the information 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.
Forest ecosystem models based on heuristic water stress functions poorly predict tropical forest response to drought partly because they do not capture the diversity of hydraulic traits (including variation in tree size) observed in tropical forests. We developed a continuous porous media approach to modeling plant hydraulics in which all parameters of the constitutive equations are biologically interpretable and measurable plant hydraulic traits (e.g., turgor loss point πtlp, bulk elastic modulus ε, hydraulic capacitance Cft, xylem hydraulic conductivity ks,max, water potential at 50 % loss of conductivity for both xylem (P50,x) and stomata (P50,gs), and the leaf : sapwood area ratio Al : As). We embedded this plant hydraulics model within a trait forest simulator (TFS) that models light environments of individual trees and their upper boundary conditions (transpiration), as well as providing a means for parameterizing variation in hydraulic traits among individuals. We synthesized literature and existing databases to parameterize all hydraulic traits as a function of stem and leaf traits, including wood density (WD), leaf mass per area (LMA), and photosynthetic capacity (Amax), and evaluated the coupled model (called TFS v.1-Hydro) predictions, against observed diurnal and seasonal variability in stem and leaf water potential as well as stand-scaled sap flux.
Our hydraulic trait synthesis revealed coordination among leaf and xylem hydraulic traits and statistically significant relationships of most hydraulic traits with more easily measured plant traits. Using the most informative empirical trait–trait relationships derived from this synthesis, TFS v.1-Hydro successfully captured individual variation in leaf and stem water potential due to increasing tree size and light environment, with model representation of hydraulic architecture and plant traits exerting primary and secondary controls, respectively, on the fidelity of model predictions. The plant hydraulics model made substantial improvements to simulations of total ecosystem transpiration. Remaining uncertainties and limitations of the trait paradigm for plant hydraulics modeling are highlighted.
We report a novel form of xylem dysfunction in angiosperms: reversible collapse of the xylem conduits of the smallest vein orders that demarcate and intrusively irrigate the areoles of Quercus rubra leaves. Cryo-scanning electron microscopy revealed gradual increases in collapse from ~ -2 MPa down to ~ -3 MPa, saturating thereafter (to -4 MPa). Over this range cavitation remained negligible in these veins. Imaging of rehydration experiments showed spatially variable recovery from collapse within 20 seconds, and complete recovery after two minutes. More broadly, the patterns of deformation induced by desiccation in both mesophyll and xylem suggest that cell wall collapse is unlikely to depend solely on individual wall properties, as mechanical constraints imposed by neighbors appear to be important. From the perspective of equilibrium leaf water potentials, petioles, whose vessels extend into the major vein orders, showed a vulnerability to cavitation that overlapped in the water potential domain both minor vein collapse and buckling (turgor loss) of the living cells. However, models of transpiration transients showed that minor vein collapse and mesophyll capacitance could effectively buffer major veins from cavitation over time scales relevant to rectification of stomatal wrong-way responses. We suggest that for angiosperms, whose subsidiary cells give up large volumes to allow large stomatal apertures at the cost of potentially large wrong-way responses, vein collapse could make an important contribution to these plants ability to transpire near the brink of cavitation-inducing water potentials.
Root systems perform the crucial task of absorbing water from the soil to meet the demands of a transpiring canopy. Roots are thought to operate like electrical fuses, which break when carrying an excessive load under conditions of drought stress. Yet the exact site and sequence of this dysfunction in roots remains elusive. Using in vivo X-ray computed microtomography (microCT), we found that drought-induced mechanical failure (i.e. lacunae formation) in fine root cortical cells is the initial and primary driver of reduced fine root hydraulic conductivity (Lpr) under mild to moderate drought stress. Cortical lacunae started forming under mild drought stress (-0.6 MPa stem), coincided with a dramatic reduction in Lpr, and preceded root shrinkage or significant xylem embolism. Only under increased drought stress was embolism formation observed in the root xylem, and it appeared first in the fine roots (50% loss of hydraulic conductivity, P50, reached at -1.8 MPa) and then in older, coarse roots (P50 = -3.5 MPa). These results show that cortical cells in fine roots function like hydraulic fuses that decouple plants from drying soil, thus preserving the hydraulic integrity of the plant’s vascular system under early stages of drought stress. Cortical lacunae formation led to permanent structural damage of the root cortex and non-recoverable Lpr, pointing to a role in fine root mortality and turnover under drought stress.
This study investigated altitudinal changes in leaf-lamina hydraulic conductance (KL) and leaf morphological traits related to KL using five Rhododendron species growing at different altitudes (2500–4500 m above sea level) in Jaljale Himal region in eastern Nepal. Sun leaves were collected from the highest and the lowest altitude populations of each species, and KL was measured with a high pressure flow meter method. Leaf-lamina hydraulic conductance ranged from 7.7 to 19.3 mmol m−2 s−1 MPa−1 and was significantly positively correlated with altitude. The systematic increase with altitude was also found in KL, leaf nitrogen content and stomatal pore index. These relationships suggest that plants from higher-altitude habitats had a large CO2 supply to the intercellular space in a leaf and high CO2 assimilation capacity, which enables efficient photosynthesis at high altitude. The variation in KL was associated with the variation in several leaf morphological traits. High KL was found in leaves with small leaf area and round shape, both of which result in shorter major veins. These results suggest that the short major veins were important for efficient water transport in unlobed leaves of Rhododendron species. The extent of lignification in bundle sheaths and bundle sheath extension was associated with KL. Lignified compound primary walls inhibit water conduction along apoplastic routes. All species analyzed had heterobaric leaves, in which bundle sheath extensions developed from minor veins, but strongly lignified compound primary walls were found in Rhododendron species with low KL. It is still unclear why cell walls in bundle sheath at minor veins were markedly lignified in Rhododendron species growing at lower altitude. The lignified cell wall provides a high pathogenic resistance to infection and increases the mechanical strength of cell wall. The data imply that lignified bundle sheath may provide a trade-off between leaf hydraulic efficiency and leaf mechanical toughness or longevity.
During droughts, leaves are predicted to act as ‘hydraulic fuses’ by shedding when plants reach critically low water potential (Ψ plant ), thereby slowing water loss, stabilizing Ψ plant 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, Ψ plant 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 Ψ plant 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 Ψ plant 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 Ψ plant , suggesting that the main function of drought deciduousness may vary among species.
Forest ecosystem models based on heuristic water stress functions poorly predict tropical forest response to drought because they do not capture the diversity of hydraulic traits (including variation in tree size) observed in tropical forests. We developed a Richards’ equation-based model of plant hydraulics in which all parameters of its constitutive equations are biologically-interpretable and measureable plant hydraulic traits (e.g., turgor loss point πtlp, bulk elastic modulus ε, hydraulic capacitance Cft, xylem hydraulic conductivity ks,max, water potential at 50 % loss of conductivity for both xylem (P50,x) and stomata (P50,gs), and the leaf:sapwood area ratio Al:As). We embedded this plant hydraulics model within a forest simulator (TFS) that modeled individual tree light environments and their upper boundary condition (transpiration) as well as provided a means for parameterizing individual variation in hydraulic traits. We synthesized literature and existing databases to parameterize all hydraulic traits as a function of stem and leaf traits wood density (WD), leaf mass per area (LMA) and photosynthetic capacity (Amax) and evaluated the coupled model’s (TFS-Hydro) predictions against diurnal and seasonal variability in stem and leaf water potential as well as stand-scaled sap flux.
Our hydraulic trait synthesis revealed coordination among leaf and xylem hydraulic traits and statistically significant relationships of most hydraulic traits with more easily measured plant traits. Using the most informative empirical trait-trait relationships derived from this synthesis, the TFS-Hydro model parameterization is capable of representing patterns of coordination and trade-offs in hydraulic traits. TFS-Hydro successfully captured individual variation in leaf and stem water potential due to increasing tree size and light environment, with model representation of hydraulic architecture and plant traits exerting primary and secondary controls, respectively, on the fidelity of model predictions. The plant hydraulics model made substantial improvements to simulations of total ecosystem transpiration under control conditions, but the absence of a vertically stratified soil hydrology model precluded improvements to the simulation of drought response. Remaining uncertainties and limitations of the trait paradigm for plant hydraulics modeling are highlighted.
Sap flux density was measured throughout a whole growing season at different locations within a 25-year-old maritime pine trunk using a continuous constant-power heating method with the aim of 1) assessing the variability of the sap flux density within a horizontal plane of the stem section and 2) interpreting the time shift in sap flow at different heights over the course of a day. Measurements were made at five height levels, from 1.3 to 15 m above ground level. At two heights (i.e. 1.30 m and beneath the lower living whorl, respectively), sap flux density was also measured at four azimuth angles. Additionally, diurnal time courses of canopy transpiration, needle transpiration, needle and trunk water potential, and trunk volume variations were measured over 4 days with differing soil moisture contents. At the single tree level, the variability of sap flux density with respect to azimuth was higher at the base of the trunk than immediately beneath the live crown. This has important implications for sampling methodologies. The observed pattern suggests that the azimuth variations observed may be attributed to sapwood heterogeneity caused by anisotropic distribution of the sapwoods hydraulic properties rather than to a sectorisation of sap flux. At the stand level, we did not find any evidence of a relationship between the tree social status and its sap flux density, and this we attributed to the high degree of homogeneity within the stand and its low LAI. An unbranched three-compartment RC-analogue model of water transfer through the tree is proposed as a rational basis for interpreting the vertical variations in water flux along the soil-tree-atmosphere continuum. Methods for determining the parameters of the model in the field are described. The model outputs are evaluated through a comparison with tree transpiration and needle water potential collected in the field.
The frequency of severe droughts is increasing in many regions around the world as a result of climate change(1-3). Droughts alter the structure and function of forests(4,5). Site- and region-specific studies suggest that large trees, which play keystone roles in forests(6) and can be disproportionately important to ecosystem carbon storage(7) and hydrology(8), exhibit greater sensitivity to drought than small trees(4,5,9,10). Here, we synthesize data on tree growth and mortality collected during 40 drought events in forests worldwide to see whether this size-dependent sensitivity to drought holds more widely. We find that droughts consistently had a more detrimental impact on the growth and mortality rates of larger trees. Moreover, drought-related mortality increased with tree size in 65% of the droughts examined, especially when community-wide mortality was high or when bark beetles were present. The more pronounced drought sensitivity of larger trees could be underpinned by greater inherent vulnerability to hydraulic stress(11-14), the higher radiation and evaporative demand experienced by exposed crowns4,15, and the tendency for bark beetles to preferentially attack larger trees(16). We suggest that future droughts will have a more detrimental impact on the growth and mortality of larger trees, potentially exacerbating feedbacks to climate change.
Key message
Greater transport capacity of diffuse- vs. ring-porous stem networks translated into greater water use by the diffuse-porous co-dominant, but similar growth indicated higher water use efficiency of the ring-porous species.
Abstract
Coexistence of diffuse- vs. ring-porous trees in north-temperate deciduous forests implies a complementary ecology. The contrasting stem anatomies may result in divergent patterns of water use, and consequences for growth rate are unknown. We investigated tree hydraulics and growth rates in two co-dominants: diffuse-porous Acer grandidentatum (“maple”) and ring-porous Quercus gambelii (“oak”). Our goals were (1) document any differences in seasonal water use and its basis in divergent stem anatomy and (2) compare annual growth rates and hence growth-based water use efficiencies. At maximum transpiration, maple trees used more than double the water than oak trees. Maple also had more leaf area per basal area, resulting in similar water use per leaf area between species. Maple had ca. double the tree hydraulic conductance than oak owing to greater conductance of its diffuse-porous stem network (leaf- and root system conductances were less different between species). Water use in maple increased with vapor pressure deficit (VPD), whereas in oak it decreased very slightly indicating a more sensitive stomatal response. Seasonably stable water use and xylem pressure in oak suggested a deeper water source. Although maple used more water, both species exhibited similar annual biomass growth of the above-ground shoot network, indicating greater growth-based water use efficiency of oak shoots. In sum, water use in maple exceeded that in oak and was more influenced by soil and atmospheric water status. The low and stable water use of oak was associated with a greater efficiency in exchanging water for shoot growth.
Drought and heat-induced tree mortality is accelerating in many forest biomes as a consequence of a warming climate, resulting in a threat to global forests unlike any in recorded history. Forests store the majority of terrestrial carbon, thus their loss may have significant and sustained impacts on the global carbon cycle. We use a hydraulic corollary to Darcy's law, a core principle of vascular plant physiology, to predict characteristics of plants that will survive and die during drought under warmer future climates. Plants that are tall with isohydric stomatal regulation, low hydraulic conductance, and high leaf area are most likely to die from future drought stress. Thus, tall trees of old-growth forests are at the greatest risk of loss, which has ominous implications for terrestrial carbon storage. This application of Darcy's law indicates today's forests generally should be replaced by shorter and more xeric plants, owing to future warmer droughts and associated wildfires and pest attacks. The Darcy's corollary also provides a simple, robust framework for informing forest management interventions needed to promote the survival of current forests. Given the robustness of Darcy's law for predictions of vascular plant function, we conclude with high certainty that today's forests are going to be subject to continued increases in mortality rates that will result in substantial reorganization of their structure and carbon storage.
Leaf hydraulic conductance (k leaf) is a central element in the regulation of leaf water balance but the properties of k leaf remain uncertain. Here, the evidence for the following two models for k leaf in well-hydrated plants is evaluated: (i) k leaf is constant or (ii) k leaf increases as transpiration rate (E) increases. The difference between stem and leaf water potential (ΔΨstem-leaf), stomatal conductance (g s), k leaf, and E over a diurnal cycle for three angiosperm and gymnosperm tree species growing in a common garden, and for Helianthus annuus plants grown under sub-ambient, ambient, and elevated atmospheric CO2 concentration were evaluated. Results show that for well-watered plants k leaf is positively dependent on E. Here, this property is termed the dynamic conductance, k leaf(E), which incorporates the inherent k leaf at zero E, which is distinguished as the static conductance, k leaf(0). Growth under different CO2 concentrations maintained the same relationship between k leaf and E, resulting in similar k leaf(0), while operating along different regions of the curve owing to the influence of CO2 on g s. The positive relationship between k leaf and E minimized variation in ΔΨstem-leaf. This enables leaves to minimize variation in Ψleaf and maximize g s and CO2 assimilation rate over the diurnal course of evaporative demand.
© The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology.
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 M editerranean‐type ecosystem by measuring leaf hydraulic conductance ( K leaf ) and stem hydraulic conductivity ( K S ). We also investigated whether leaves function as safety valves by relating K leaf and the hydraulic safety margin (stem water potential minus the water potential at which 50% of conductivity is lost (Ψ stem − Ψ 50 )). 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, K leaf was negatively correlated with K S , supporting the HSH . Additionally, K leaf 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 K S , or a low safety margin. This critical role of leaves appears to contribute importantly to plant ecological specialization in a drought‐prone environment.
Stem water storage capacity and diurnal patterns of water use were studied in five canopy trees of a seasonal tropical forest in Panama. Sap flow was measured simultaneously at the top and at the base of each tree using constant energy input thermal probes inserted in the sapwood. The daily stem storage capacity was calculated by comparing the diurnal patterns of basal and crown sap flow. The amount of water withdrawn from storage and subsequently replaced daily ranged from 4 kg d–1 in a 0·20-m-diameter individual of Cecropia longipes to 54 kg d–1 in a 1·02-m-diameter individual of Anacardium excelsum, representing 9–15% of the total daily water loss, respectively. Ficus insipida, Luehea seemannii and Spondias mombin had intermediate diurnal water storage capacities. Trees with greater storage capacity maintained maximum rates of transpiration for a substantially longer fraction of the day than trees with smaller water storage capacity. All five trees conformed to a common linear relationship between diurnal storage capacity and basal sapwood area, suggesting that this relationship was species-independent and size-specific for trees at the study site. According to this relationship there was an increment of 10 kg of diurnal water storage capacity for every 0·1 m2 increase in basal sapwood area. The diurnal withdrawal of water from, and refill of, internal stores was a dynamic process, tightly coupled to fluctuations in environmental conditions. The variations in basal and crown sap flow were more synchronized after 1100 h when internal reserves were mostly depleted. Stem water storage may partially compensate for increases in axial hydraulic resistance with tree size and thus play an important role in regulating the water status of leaves exposed to the large diurnal variations in evaporative demand that occur in the upper canopy of seasonal lowland tropical forests.
The West, Brown, Enquist (WBE) model derives symmetrically self‐similar branching to predict metabolic scaling from hydraulic conductance, K , (a metabolism proxy) and tree mass (or volume, V ). The original prediction was K ∝ V 0.75 . We ask whether trees differ from WBE symmetry and if it matters for plant function and scaling. We measure tree branching and model how architecture influences K , V , mechanical stability, light interception and metabolic scaling.
We quantified branching architecture by measuring the path fraction, P f : mean/maximum trunk‐to‐twig pathlength. WBE symmetry produces the maximum, P f = 1.0. We explored tree morphospace using a probability‐based numerical model constrained only by biomechanical principles.
Real tree P f ranged from 0.930 (nearly symmetric) to 0.357 (very asymmetric). At each modeled tree size, a reduction in P f led to: increased K ; decreased V ; increased mechanical stability; and decreased light absorption. When P f was ontogenetically constant, strong asymmetry only slightly steepened metabolic scaling. The P f ontogeny of real trees, however, was ‘U’ shaped, resulting in size‐dependent metabolic scaling that exceeded 0.75 in small trees before falling below 0.65.
Architectural diversity appears to matter considerably for whole‐tree hydraulics, mechanics, photosynthesis and potentially metabolic scaling. Optimal architectures likely exist that maximize carbon gain per structural investment.
The leaf area to sapwood area ratio (A l :A s) of trees has been hypothesized to decrease as trees become older and taller. Theory suggests that A l :A s must decrease to maintain leaf-specific hydraulic sufficiency as path length, gravity, and tortuosity constrain whole-plant hydraulic conductance. We tested the hypothesis that A l :A s declines with tree height. Whole-tree A l :A s was measured on 15 individuals of Douglas-fir (Pseudotsuga menziesii var. menziesii) ranging in height from 13 to 62 m (aged 20–450 years). A l :A s declined substantially as height increased (P=0.02). Our test of the hypothesis that A l :A s declines with tree height was extended using a combination of original and published data on nine species across a range of maximum heights and climates. Meta-analysis of 13 whole-tree studies revealed a consistent and significant reduction in A l :A s with increasing height (P<0.05). However, two species (Picea abies and Abies balsamea) exhibited an increase in A l :A s with height, although the reason for this is not clear. The slope of the relationship between A l :A s and tree height (∆A l :A s /∆h) was unrelated to mean annual precipitation. Maximum potential height was positively correlated with ∆A l :A s /∆h. The decrease in A l :A s with increasing tree size that we observed in the majority of species may be a homeostatic mechanism that partially compensates for decreased hydraulic con-ductance as trees grow in height.
Quasi-steady-state measurements of root hydraulic conductance (KR) of Olea oleaster Hoffmgg. et Link potted seedlings were performed using a pressure chamber with the aim of: (a) measuring the impact of different water-stress levels on a KR; (b) measuring the kinetics of KR recovery several days after soil rewetting; (c) relating changes in KR to changes in root anatomy and morphology. Increasing water-stress was applied in terms of ratio of leaf water potential (ΨL) measured at midday to that at zero turgor (ΨTLP), i.e. ΨL/ΨTLP=0·5, 1·0, 1·2, 1·6; KR was measured initially and at 24, 48, 72, 96 h after irrigation.
Values of KR in seedlings stressed to ΨL/ΨTLP=1·2 increased for 48 h after irrigation from 0·23 to 0·97×10−5 kg s−1 m−2 MPa−1 i.e. from 16% to 66% of that measured in unstressed seedlings. A marked shift of the x-axis intercept of the straight line relating flow to pressure (zero flow at non-zero pressure) was recorded initially after irrigation and persisted up to 48 h. Recovery of KR occurred within 24 h after irrigation in seedlings at ΨL/ΨTLP=0·5 and 48 h later in those at ΨL/ΨTLP=1·0.
Severe drought stress (ΨL/ΨTLP=1·6) caused anatomical changes to roots which formed a two-layered exodermis with thicker suberized walls and a three- to four-layered endodermis with completely suberized tangential walls. Recovery of KR in these roots required resumed growth of root tips and emergence of new lateral roots.
Ecologists often standardize data through the use of ratios and indices. Such measures are employed generally to remove a size effect induced by some relatively uniteresting variable. The implications of using the resultant data in correlation and regression analyses are poorly recognized. We show that ratios and indices often provide surprising and spurious results due to their unusual properties. As a solution, we advocate the use of randomization tests to evaluate hypotheses confounded by spurious correlations. In addition, we emphasize that identifying the appropriate null correlation is of utmost importance when statistically evaluating ratios, although this issue is frequently ignored.
Components of the tree water transport pathway; roots, trunks, branches and leaves; can also serve as water storage compartments
and therefore act transiently as intermediate sources of water for transpiring leaves. However, most previous work has focused
on gradual depletion and recharge of tree internal water reserves as soil water availability varies over seasonal cycles.
This chapter focuses on the underappreciated role that internal water storage plays in stabilizing the physiological function
of trees under the dynamic conditions that prevail over the course of a day. Capacitive discharge of water into the transpiration
stream can buffer daily fluctuations in xylem tension, thereby diminishing the risk of xylem embolism and hydraulic failure
under dynamic conditions. Intrinsic sapwood capacitance and reliance on stored water increase with tree size. An inverse
relationship between sapwood capacitance and resistance to embolism across diverse woody species suggests that above a minimum
threshold value of capacitance, the tree survives by using capacitance to provide hydraulic safety by buffering fluctuations
in tension, rather by relying on xylem structural features that directly reduce vulnerability to embolism. Progress in understanding
the physiological role of capacitance in trees is impeded by non-uniformity in the way capacitance is measured and expressed,
preventing much of the available information from being synthesized. To remedy this, standard protocols are described for
defining and expressing capacitance and water storage capacity.
Seasonal regulation of leaf water potential (ΨL) was studied in eight dominant woody savanna species growing in Brazilian savanna (Cerrado) sites that experience a 5-month dry season. Despite marked seasonal variation in precipitation and air saturation deficit (D), seasonal differences in midday minimum ΨL were small in all of the study species. Water use and water status were regulated by a combination of plant physiological and architectural traits. Despite a nearly 3-fold increase in mean D between the wet and dry season, a sharp decline in stomatal conductance with increasing D constrained seasonal variation in minimum ΨL by limiting transpiration per unit leaf area (E). The leaf surface area per unit of sapwood area (LA/SA), a plant architectural index of potential constraints on water supply in relation to transpirational demand, was about 1.5–8 times greater in the wet season compared to the dry season for most of the species. The changes in LA/SA from the wet to the dry season resulted from a reduction in total leaf surface area per plant, which maintained or increased total leaf-specific hydraulic conductance (G
t) during the dry season. The isohydric behavior of Cerrado tree species with respect to minimum ΨL throughout the year thus was the result of strong stomatal control of evaporative losses, a decrease in total leaf surface area per tree during the dry season, an increase in total leaf-specific hydraulic conductance, and a tight coordination between gas and liquid phase conductance. In contrast with the seasonal isohydric behavior of minimum ΨL, predawn ΨL in all species was substantially lower during the dry season compared to the wet season. During the dry season, predawn ΨL was more negative than bulk soil Ψ estimated by extrapolating plots of E versus ΨL to E=0. Predawn disequilibrium between plant and soil Ψ was attributable largely to nocturnal transpiration, which ranged from 15 to 22% of the daily total. High nocturnal water loss may also have prevented internal water storage compartments from being completely refilled at night before the onset of transpiration early in the day.
Using the heat pulse and other techniques, the hydraulic architecture of apricot trees was mapped out. The flows (overall flow, flow across the four main branches) and forces (water potential differences between xylem and leaves) measured allowed us to quantify hydraulic conductance of branches and of the root/soil resistance. The experiment was carried out in a commercial orchard of 11-year-old apricot trees (Prunus armeniaca L., cv. Blida, on Real Fino apricot rootstock) during 1 week (October 27–November 3, 1998). Three representative trees with a cylindrical trunk divided into four main branches of different sizes, orientation and local microclimate were chosen for the experiment. Sap flow was measured throughout the experimental period. Twelve sets of heat-pulse probes were used, one for each main branch. The diurnal course of the environmental conditions, the fraction of the area irradiated and leaf water relations were also considered in each main branch. The relationships between leaf water potential, xylem water potential and transpiration were established for different branches and also for the total plant. Using the slopes of these regressions, total plant conductance, the hydraulic conductance of the stem and root pathway, the hydraulic conductance of the canopy and the hydraulic conductance of each branch were estimated. Our findings show that the root conductance and the canopy hydraulic conductance are similar in magnitude. Leaf hydraulic conductance per leaf area unit was similar for each of the four branch orientations, indicating that, while the light microclimate has a dominant influence on transpiration, in this case it had little effect on the hydraulic properties of the canopy.
Root systems play a major role in supplying the canopy with water, enabling photosynthesis and growth. Yet, much of the dynamic response of root hydraulics and its influence on gas exchange during soil drying and recovery remains uncertain. We examined the decline and recovery of the whole root hydraulic conductance (Kr) and canopy conductance (gc ) during exposure to moderate water stress in two species with contrasting root systems: Tanacetum cinerariifolium (herbaceous Asteraceae) and Callitris rhomboidea (woody conifer). Optical dendrometers were used to record stem water potential at high temporal resolution and enabled non-invasive measurements of Kr calculated from the rapid relaxation kinetics of water potential in hydrating roots. We observed parallel declines in Kr and gc to < 20% of unstressed levels during the early stages of water stress in both species. The recovery of Kr after rewatering differed between species. T. cinerariifolium recovered quickly, with 60% of Kr recovered within 2 h, while C. rhomboidea was much slower to return to its original Kr. Recovery of gc followed a similar trend to Kr in both species, with C. rhomboidea slower to recover. Our findings suggest that the pronounced sensitivity of Kr to drought is a common feature among different plant species, but recovery may vary depending on root type and water stress severity. Kr dynamics are proposed to modulate gc response during and following drought.
The influence of aquaporin (AQP) activity on plant water movement remains unclear, especially in plants subject to unfavorable conditions. We applied a multitiered approach at a range of plant scales to (i) characterize the resistances controlling water transport under drought, flooding and flooding plus salinity conditions; (ii) quantify the respective effects of AQP activity and xylem structure on root (Kroot), stem (Kstem) and leaf (Kleaf) conductances, and (iii) evaluate the impact of AQP-regulated transport capacity on gas exchange. We found that drought, flooding and flooding-salinity reduced Kroot and root AQP activity in Pinus taeda, whereas Kroot of the flood-tolerant Taxodium distichum did not decline under flooding. The extent of the AQP-control of transport efficiency varied among organs and species, ranging from 35%-55% in Kroot to 10%-30% in Kstem and Kleaf. In response to treatments, AQP-mediated inhibition of Kroot rather than changes in xylem acclimation controlled the fluctuations in Kroot. The reduction in stomatal conductance and its sensitivity to vapor pressure deficit were direct responses to decreased whole-plant conductance triggered by lower Kroot and larger resistance belowground. Our results provide new mechanistic and functional insights on plant hydraulics that are essential to quantifying the influences of future stress on ecosystem function.
Understanding how water use and drought stress in woody plants change in relation to compositional, structural and environmental variability of mixed forests is key to understand their functioning and dynamics. Observational and experimental studies have so far shown a complex array of water use and drought stress responses to species mixing, but progress is hampered by the costs of replicating measurements. A complementary approach consists in using in silico experiments with trait-based forest ecosystem models, which have the advantage of allowing the interpretation of the net mixing effect as the result of specific combinations of trait differences. We explore the potential of such an approach using a novel trait-based forest ecosystem model with a strong focus on plant hydraulics and data from 186 mixed forest inventory plots including holm oak (Quercus ilex L.) and eight co-occurring species. Sensitivity analyses focusing on the effect of differences in individual plant traits indicate that water use and summer drought stress of holm oak trees respond primarily to the variation in competitor's height, root distribution and xylem hydraulic efficiency and safety. Simulations of pure and mixed stands across different combinations of climate aridity and stand leaf area index indicate that differences in traits may compensate for one another, so that the influence of a given trait (e.g. tree height) on water use or drought stress can be decreased or offset by the influence of another one (e.g. hydraulic efficiency). Importantly, we show that species mixing does not always have positive effects at the stand level. Overall, our simulation study shows that the complexity of species-and stand-level mixing effects on water use and drought stress arises primarily as the result of differences in key functional traits of the competitor, although stand structure and climate aridity may modulate mixing effects.
Drought, a recurring phenomenon with major impacts on both human and natural systems, is the most widespread climatic extreme that negatively affects the land carbon sink. Although twentieth-century trends in drought regimes are ambiguous, across many regions more frequent and severe droughts are expected in the twenty-first century. Recovery time - how long an ecosystem requires to revert to its pre-drought functional state - is a critical metric of drought impact. Yet the factors influencing drought recovery and its spatiotemporal patterns at the global scale are largely unknown. Here we analyse three independent datasets of gross primary productivity and show that, across diverse ecosystems, drought recovery times are strongly associated with climate and carbon cycle dynamics, with biodiversity and CO 2 fertilization as secondary factors. Our analysis also provides two key insights into the spatiotemporal patterns of drought recovery time: first, that recovery is longest in the tropics and high northern latitudes (both vulnerable areas of Earth's climate system) and second, that drought impacts (assessed using the area of ecosystems actively recovering and time to recovery) have increased over the twentieth century. If droughts become more frequent, as expected, the time between droughts may become shorter than drought recovery time, leading to permanently damaged ecosystems and widespread degradation of the land carbon sink. © 2017 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.
Ecosystem models have difficulty predicting plant drought responses, partially from uncertainty in the stomatal response to water deficits in soil and atmosphere. We evaluate a ‘supply–demand’ theory for water‐limited stomatal behavior that avoids the typical scaffold of empirical response functions. The premise is that canopy water demand is regulated in proportion to threat to supply posed by xylem cavitation and soil drying.
The theory was implemented in a trait‐based soil–plant–atmosphere model. The model predicted canopy transpiration ( E ), canopy diffusive conductance ( G ), and canopy xylem pressure ( P canopy ) from soil water potential ( P soil ) and vapor pressure deficit ( D ).
Modeled responses to D and P soil were consistent with empirical response functions, but controlling parameters were hydraulic traits rather than coefficients. Maximum hydraulic and diffusive conductances and vulnerability to loss in hydraulic conductance dictated stomatal sensitivity and hence the iso‐ to anisohydric spectrum of regulation. The model matched wide fluctuations in G and P canopy across nine data sets from seasonally dry tropical forest and piñon–juniper woodland with < 26% mean error.
Promising initial performance suggests the theory could be useful in improving ecosystem models. Better understanding of the variation in hydraulic properties along the root–stem–leaf continuum will simplify parameterization.
Recent advances in modelling the architecture and function of the plant hydraulic network have led to improvements in predicting and interpreting the consequences of functional trait variation on CO2 uptake and water loss. We build upon one such model to make novel predictions for scaling of the total specific hydraulic conductance of leaves and shoots (kL and kSH respectively) and variation in the partitioning of hydraulic conductance. Consistent with theory, we observed isometric (slope=1) scaling between kL and kSH across several independently collected datasets, and a lower ratio of kL and kSH , termed the leaf to shoot conductance ratio (CLSCR ), in arid environments and in woody species. Isometric scaling of kL and kSH supports the concept that hydraulic design is coordinated across the plant. We propose that CLSCR is an important adaptive trait that represents the trade-off between efficiency and safety at the scale of the whole plant.
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Conifers decrease the amount of biomass apportioned to leaves relative to sapwood in response to increasing atmospheric evaporative demand. We determined how these climate-driven shifts in allocation affect the aboveground water relations of ponderosa pine growing in contrasting arid (desert) and humid (montane) climates. To support higher transpiration rates, a low leaf:sapwood area ratio (A L/A S) in desert versus montane trees could increase leaf-specific hydraulic conductance (K L). Alternatively, a high sapwood volume:leaf area ratio in the desert environment may increase the contribution of stored water to transpiration. Transpiration and hydraulic conductance were determined by measuring sap flow (J S) and shoot water potential during the summer (June-July) and fall (August-September). The daily contribution of stored water to transpiration was determined using the lag between the beginning of transpiration from the crown at sunrise and J S. In the summer, mean maximum J S was 31.80±5.74 and 24.34±3.05 g m(-2) s(-1) for desert and montane trees (a 30.6% difference), respectively. In the fall, J S was 25.33±8.52 and 16.36±4.64 g m(-2) s(-1) in desert and montane trees (a 54.8% difference), respectively. J S was significantly higher in desert relative to montane trees during summer and fall (P<0.05). Predawn and midday shoot water potential and sapwood relative water content did not differ between environments. Desert trees had a 129% higher K L than montane trees in the summer (2.41×10(-5) versus 1.05×10(-5) kg m(-2) s(-1) MPa(-1), P<0.001) and a 162% higher K L in the fall (1.97×10(-5) versus 0.75×10(-5) kg m(-2) s(-1) MPa(-1), P<0.001). Canopy conductance decreased with D in all trees at all measurement periods (P<0.05). Maximum g C was 3.91 times higher in desert relative to montane trees averaged over the summer and fall. Water storage capacity accounted for 11 kg (11%) and 10.6 kg (17%) of daily transpiration in the summer and fall, respectively, and did not differ between desert and montane trees. By preventing xylem tensions from reaching levels that cause xylem cavitation, high K L in desert ponderosa pine may facilitate its avoidance. Thus, the primary benefit of low leaf:sapwood allocation in progressively arid environments is to increase K L and not to increase the contribution of stored water to transpiration.
Preface. Acknowledgments. General References. Chapter 1. Structure and Development of the Plant Body-An Overview. Chapter 2. The Protoplast: Plasma Membrane, Nucleus, and Cytoplasmic Organelles. Chapter 3. The Protoplast: Endomembrane System, Secretory Pathways, Cytoskeleton, and Stored Compounds. Chapter 4. Cell Wall . Chapter 5. Meristems and Differentiation. Chapter 6. Apical Meristems. Chapter 7. Parenchyma and Collenchyma. Chapter 8. Sclerenchyma. Chapter 9. Epidermis. Chapter 10. Xylem: Cell Types and Developmental Aspects. Chapter 11. Xylem: Secondary Xylem and Variations in Wood Structure. Chapter 12. Vascular Cambium. Chapter 13. Phloem: Cell Types and Developmental Aspects. Chapter 14. Phloem: Secondary Phloem and Variations in Its Structure. Chapter 15. Periderm. Chapter 16. External Secretory Structures. Chapter 17. Internal Secretory Structures. Addendum: Other Pertinent References Not Cited in the Text. Glossary. Author Index. Subject Index.
1 Conducting Units: Tracheids and Vessels.- 2 The Vessel Network in the Stem.- 3 The Cohesion-Tension Theory of Sap Ascent.- 4 Xylem Dysfunction: When Cohesion Breaks Down.- 5 Hydraulic Architecture of Woody Shoots.- 6 Hydraulic Architecture of Whole Plants and Plant Performance.- 7 Other Functional Adaptations.- 8 Failure and "Senescence" of Xylem Function.- 9 Pathology of the Xylem.- References.
Sap flow (F) and leaf water potential (LWP) were followed diurnally in mature Valencia and Shamouti orange trees in an orchard. The hydraulic conductance of these trees
was computed from the diurnal relationship between the LWP and F. The driving force for water movement was estimated from a weighted average of sunlit and shaded LWP, assuming that leaves in the shade transpire to some extent. LWP of covered, non-transpiring leaves was also measured hourly. It was assumed to represent the xylem water potential within
the axial conduit of the trunk. Relating covered LWP to F on an hourly basis enables the computation of the hydraulic conductance of the root system, including axial conductances.
The hydraulic conductance of the transpiring crown was computed. Its magnitude was comparable to the root system hydraulic
conductance.
Measurements of leaf transpiration and calculations of leaf conductance to water vapor are important in almost all investigations of plant water relations. Transpiration is a primary determinant of leaf energy balance (Chapter 7) and plant water status (Chapter 9). Together with the exchange of CO2 it determines the water use efficiency. The close linkage between CO2 uptake and H2O via the stomatal pore has allowed for separation of stomatal and biochemical limitations to photosynthesis through calculation of intercellular CO2 concentrations. In this chapter we will cover the principles and instruments necessary for measurement of leaf transpiration and the calculation of leaf conductances to water vapor exchange. We will also consider the methodology and problems involved in determining whole-plant and canopy transpiration rates.
1. The Standardised Major Axis Tests and Routines (SMATR) software provides tools for estimation and inference about allometric lines, currently widely used in ecology and evolution.
2. This paper describes some significant improvements to the functionality of the package, now available on R in smatr version 3.
3. New inclusions in the package include sma and ma functions that accept formula input and perform the key inference tasks; multiple comparisons; graphical methods for visualising data and checking (S)MA assumptions; robust (S)MA estimation and inference tools.
The hydraulic limitation theory proposes that the decline of forest productivity with age is a consequence of the loss of whole‐plant and leaf‐specific hydraulic conductance with tree height caused by increased friction. Recent theoretical analyses have suggested that tapering (the broadening of xylem vessel diameter from terminal branches to the base of the stem) could compensate completely for the effect of tree height on hydraulic conductance, and thus on tree growth.
The data available for testing this hypothesis are limited, but they do not support the implication that whole‐tree and leaf‐specific hydraulic conductance are generally independent of tree height. Tapering cannot exclude hydraulic limitation as the principle mechanism for the observed decline in growth.
Reduction of the leaf‐to‐sapwood area ratio, decreased leaf water potential, loss of leaf‐cell turgor, or osmotic adjustments in taller trees could reduce the effect of increased plant hydraulic resistance on stomatal conductance with height. However, these mechanisms operate with diminishing returns, as they infer increased costs to the tree that will ultimately limit tree growth. To understand the decline in forest growth, the effects of these acclimation mechanisms on carbon uptake and allocation should be considered.
In the present study the linkage between hydraulic, photo-synthetic and phenological properties of tropical dry forest trees were investigated. Seasonal patterns of stem-specific conductivity (K SP) described from 12 species, including deciduous, brevi-deciduous and evergreen species, indi-cated that only evergreen species were consistent in their response to a dry-to-wet season transition. In contrast, K SP in deciduous and brevi-deciduous species encompassed a range of responses, from an insignificant increase in K SP following rains in some species, to a nine-fold increase in others. Amongst deciduous species, the minimum K SP dur-ing the dry season ranged from 6 to 56% of wet season K SP, indicating in the latter case that a significant portion of the xylem remained functional during the dry season. In all species and all seasons, leaf-specific stem conductivity (K L) was strongly related to the photosynthetic capacity of the supported foliage, although leaf photosynthesis became saturated in species with high K L . The strength of this cor-relation was surprising given that much of the whole-plant resistance appears to be in the leaves. Hydraulic capacity, defined as the product of K L and the soil–leaf water poten-tial difference, was strongly correlated with the photosyn-thetic rate of foliage in the dry season, but only weakly correlated in the wet season.
The hydraulic conductance of the leaf lamina (Klamina) substantially constrains whole-plant water transport, but little is known of its association with leaf structure and function. Klamina was measured for sun and shade leaves of six woody temperate species growing in moist soil, and tested for correlation with the prevailing leaf irradiance, and with 22 other leaf traits. Klamina varied from 7.40 × 10−5 kg m−2 s−1 MPa−1 for Acer saccharum shade leaves to 2.89 × 10−4 kg m−2 s−1 MPa−1 for Vitis labrusca sun leaves. Tree sun leaves had 15–67% higher Klamina than shade leaves. Klamina was co-ordinated with traits associated with high water flux, including leaf irradiance, petiole hydraulic conductance, guard cell length, and stomatal pore area per lamina area. Klamina was also co-ordinated with lamina thickness, water storage capacitance, 1/mesophyll water transfer resistance, and, in five of the six species, with lamina perimeter/area. However, for the six species, Klamina was independent of inter-related leaf traits including leaf dry mass per area, density, modulus of elasticity, osmotic potential, and cuticular conductance. Klamina was thus co-ordinated with structural and functional traits relating to liquid-phase water transport and to maximum rates of gas exchange, but independent of other traits relating to drought tolerance and to aspects of carbon economy.