Linking stem rehydration kinetics to hydraulic traits using a novel method and mechanistic model.

BACKGROUND: Despite the recognized importance of hydraulic capacitance as a mechanism used by plants to maintain hydraulic functioning during high transpiration, characterizing the dynamics of capacitance remains a challenge. METHODS: We used a novel 'two-balance method' to investigate relationships between stem rehydration kinetics and other hydraulic traits in multiple tree species, and we developed a model to explore stem rehydration kinetics further. KEY RESULTS: We found that: (1) rehydration time constants and the amount of water uptake occurring during rehydration differed significantly across species; (2) time constants did not change with declining water potential (Ψ), while water uptake increased at lower Ψ in some species; (3) longer time constants were associated with lower wood density, higher capacitance and less negative stem pressures causing 50 % loss of hydraulic conductivity (P50); (4) greater water uptake occurred in stems with lower wood density and less negative P50 values; and (5) the model could estimate the total hydraulic resistance of the rehydration path, which cannot be measured directly. CONCLUSIONS: Overall, the two-balance method can be used to examine rehydration dynamics quickly and thoroughly in detached woody stems. This method has the potential to improve our understanding of how capacitance functions across tree species, which is an often-overlooked component of whole-plant hydraulics.

Hydroscapes, hydroscape plasticity and relationships to functional traits and mesophyll photosynthetic sensitivity to leaf water potential in Eucalyptus species.

The isohydric-anisohydric continuum describes the relative stringency of stomatal control of leaf water potential (ψleaf ) during drought. Hydroscape area (HA)-the water potential landscape over which stomata regulate ψleaf -has emerged as a useful metric of the iso/anisohydric continuum because it is strongly linked to several hydraulic, photosynthetic and structural traits. Previous research on HA focused on broad ecological patterns involving several plant clades. Here we investigate the relationships between HA and climatic conditions and functional traits across ecologically diverse but closely related species while accounting for phylogeny. Across a macroclimatic moisture gradient, defined by the ratio of mean annual precipitation to mean annual pan evaporation (P/Ep ), HA decreased with increased P/Ep across 10 Eucalyptus species. Greater anisohydry reflects lower turgor loss points and greater hydraulic safety, mirroring global patterns. Larger HA coincides with mesophyll photosynthetic capacity that is more sensitive to ψleaf . Hydroscapes exhibit little plasticity in response to variation in water supply, and the extent of plasticity does not vary with P/Ep of native habitats. These findings strengthen the case that HA is a useful metric for characterizing drought tolerance and water-status regulation.

Scaling the leaf length-times-width equation to predict total leaf area of shoots.

BACKGROUND AND AIMS: An individual plant consists of different-sized shoots, each of which consists of different-sized leaves. To predict plant-level physiological responses from the responses of individual leaves, modelling this within-shoot leaf size variation is necessary. Within-plant leaf trait variation has been well investigated in canopy photosynthesis models but less so in plant allometry. Therefore, integration of these two different approaches is needed. METHODS: We focused on an established leaf-level relationship that the area of an individual leaf lamina is proportional to the product of its length and width. The geometric interpretation of this equation is that different-sized leaf laminas from a single species share the same basic form. Based on this shared basic form, we synthesized a new length-times-width equation predicting total shoot leaf area from the collective dimensions of leaves that comprise a shoot. Furthermore, we showed that several previously established empirical relationships, including the allometric relationships between total shoot leaf area, maximum individual leaf length within the shoot and total leaf number of the shoot, can be unified under the same geometric argument. We tested the model predictions using five species, all of which have simple leaves, selected from diverse taxa (Magnoliids, monocots and eudicots) and from different growth forms (trees, erect herbs and rosette herbs). KEY RESULTS: For all five species, the length-times-width equation explained within-species variation of total leaf area of a shoot with high accuracy (R2 > 0.994). These strong relationships existed despite leaf dimensions scaling very differently between species. We also found good support for all derived predictions from the model (R2 > 0.85). CONCLUSIONS: Our model can be incorporated to improve previous models of allometry that do not consider within-shoot size variation of individual leaves, providing a cross-scale linkage between individual leaf-size variation and shoot-size variation.

Mesophyll photosynthetic sensitivity to leaf water potential in Eucalyptus: a new dimension of plant adaptation to native moisture supply.

Photosynthetic sensitivity to drought is a fundamental constraint on land-plant evolution and ecosystem function. However, little is known about how the sensitivity of photosynthesis to nonstomatal limitations varies among species in the context of phylogenetic relationships. Using saplings of 10 Eucalyptus species, we measured maximum CO2 -saturated photosynthesis using A-ci curves at several different leaf water potentials (ψleaf ) to quantify mesophyll photosynthetic sensitivity to ψleaf (MPS), a measure of how rapidly nonstomatal limitations to carbon uptake increase with declining ψleaf . MPS was compared to the macroclimatic moisture availability of the species' native habitats, while accounting for phylogenetic relationships. We found that species native to mesic habitats have greater MPS but higher maximum photosynthetic rates during non-water-stressed conditions, revealing a trade-off between maximum photosynthesis and drought sensitivity. Species with lower turgor loss points have lower MPS, indicating coordination among photosynthetic and water-relations traits. By accounting for phylogenetic relationships among closely related species, we provide the first compelling evidence that MPS in Eucalyptus evolved in an adaptive fashion with climatically determined moisture availability, opening the way for further study of this poorly explored dimension of plant adaptation to drought.

Mistletoes and their eucalypt hosts differ in the response of leaf functional traits to climatic moisture supply.

Trade-offs between photosynthesis and the costs of resource capture inform economic strategies of plants across environmental gradients and result in predictable variation in leaf traits. However, understudied functional groups like hemiparasites that involve dramatically different strategies for resource capture may have traits that deviate from expectations. We measured leaf traits related to gas exchange in mistletoes and their eucalypt hosts along a climatic gradient in relative moisture supply, measured as the ratio of precipitation to pan evaporation (P/Ep), in Victoria, Australia. We compared traits for mistletoes vs. hosts as functions of relative moisture supply and examined trait-trait correlations in both groups. Eucalypt leaf traits responded strongly to decreasing P/Ep, consistent with economic theory. Leaf area and specific leaf area (SLA) decreased along the P/Ep gradient, while C:N ratio, leaf thickness, N per area, and δ13C all increased. Mistletoes responded overall less strongly to P/Ep based on multivariate analyses; individual traits sometimes shifted in parallel with those of hosts, but SLA, leaf thickness, and N per area showed no significant change across the gradient. For mistletoes, leaf thickness was inversely related to leaf dry matter content (LDMC), with no relationship between SLA and mass-based N. In mistletoes, reduced costs of transpiration (reflecting their lack of roots) and abundant succulent leaf tissue help account for observed differences from their eucalypt hosts. Trait-based analysis of atypical functional types such as mistletoes help refine hypotheses based on plant economics and specialized adaptations to resource limitation.

A dynamic yet vulnerable pipeline: Integration and coordination of hydraulic traits across whole plants.

The vast majority of measurements in the field of plant hydraulics have been on small-diameter branches from woody species. These measurements have provided considerable insight into plant functioning, but our understanding of plant physiology and ecology would benefit from a broader view, because branch hydraulic properties are influenced by many factors. Here, we discuss the influence that other components of the hydraulic network have on branch vulnerability to embolism propagation. We also modelled the impact of changes in the ratio of root-to-leaf areas and soil texture on vulnerability to hydraulic failure along the soil-to-leaf continuum and showed that hydraulic function is better maintained through changes in root vulnerability and root-to-leaf area ratio than in branch vulnerability. Differences among species in the stringency with which they regulate leaf water potential and in reliance on stored water to buffer changes in water potential also affect the need to construct embolism resistant branches. Many approaches, such as measurements on fine roots, small individuals, combining sap flow and psychrometry techniques, and modelling efforts, could vastly improve our understanding of whole-plant hydraulic functioning. A better understanding of how traits are coordinated across the whole plant will improve predictions for plant function under future climate conditions.

Coordination and trade-offs between leaf and stem hydraulic traits and stomatal regulation along a spectrum of isohydry to anisohydry.

The degree of plant iso/anisohydry, a widely used framework for classifying species-specific hydraulic strategies, integrates multiple components of the whole-plant hydraulic pathway. However, little is known about how it associates with coordination of functional and structural traits within and across different organs. We examined stem and leaf hydraulic capacitance and conductivity/conductance, stem xylem anatomical features, stomatal regulation of daily minimum leaf and stem water potential (Ψ), and the kinetics of stomatal responses to vapour pressure deficit (VPD) in six diverse woody species differing markedly in their degree of iso/anisohydry. At the stem level, more anisohydric species had higher wood density and lower native capacitance and conductivity. Like stems, leaves of more anisohydric species had lower hydraulic conductance; however, unlike stems, their leaves had higher native capacitance at their daily minimum values of leaf Ψ. Moreover, rates of VPD-induced stomatal closure were related to intrinsic rather than native leaf capacitance and were not associated with species' degree of iso/anisohydry. Our results suggest a trade-off between hydraulic storage and efficiency in the leaf, but a coordination between hydraulic storage and efficiency in the stem along a spectrum of plant iso/anisohydry.

A synthesis of the effects of atmospheric carbon dioxide enrichment on plant hydraulics: implications for whole-plant water use efficiency and resistance to drought.

Here, we summarize studies on the effects of elevated [CO2 ] (CO2e ) on the structure and function of plant hydraulic architecture and explore the implications of those changes using a model. Changes in conduit diameter and hydraulic conductance due to CO2e vary among species. Ring-porous species tend towards an increase in conduit size and consequently conductivity. The effect in diffuse-porous species is much more limited. In conifers, the results are mixed, some species show minor changes in xylem structure, while other studies found increases in tracheid density and diameter. Non-woody plants generally exhibited the reverse pattern with narrower conduits and lower hydraulic conductivity under CO2e . Further, changes in drought-resistance traits suggest that non-woody plants were the most affected by CO2e , which may permit them to better resist drought-induced embolism under future conditions. Due to their complexity, acclimation in hydraulic traits in response to CO2e is difficult to interpret when relying solely on measurements. When we examined how the observed tissues-specific trends might alter plant function, our modelling results suggest that these hydraulic changes would lead to reduced conductance and more frequent drought stress in trees that develop under CO2e with a more pronounced effect in isohydric than in anisohydric species.

Stomatal kinetics and photosynthetic gas exchange along a continuum of isohydric to anisohydric regulation of plant water status.

Species' differences in the stringency of stomatal control of plant water potential represent a continuum of isohydric to anisohydric behaviours. However, little is known about how quasi-steady-state stomatal regulation of water potential may relate to dynamic behaviour of stomata and photosynthetic gas exchange in species operating at different positions along this continuum. Here, we evaluated kinetics of light-induced stomatal opening, activation of photosynthesis and features of quasi-steady-state photosynthetic gas exchange in 10 woody species selected to represent different degrees of anisohydry. Based on a previously developed proxy for the degree of anisohydry, species' leaf water potentials at turgor loss, we found consistent trends in photosynthetic gas exchange traits across a spectrum of isohydry to anisohydry. More anisohydric species had faster kinetics of stomatal opening and activation of photosynthesis, and these kinetics were closely coordinated within species. Quasi-steady-state stomatal conductance and measures of photosynthetic capacity and performance were also greater in more anisohydric species. Intrinsic water-use efficiency estimated from leaf gas exchange and stable carbon isotope ratios was lowest in the most anisohydric species. In comparisons between gas exchange traits, species rankings were highly consistent, leading to species-independent scaling relationships over the range of isohydry to anisohydry observed.

Convergence in leaf size versus twig leaf area scaling: do plants optimize leaf area partitioning?

BACKGROUND AND AIMS: Corner's rule states that thicker twigs bear larger leaves. The exact nature of this relationship and why it should occur has been the subject of numerous studies. It is obvious that thicker twigs should support greater total leaf area ([Formula: see text]) for hydraulical and mechanical reasons. But it is not obvious why mean leaf size ([Formula: see text]) should scale positively with [Formula: see text] We asked what this scaling relationship is within species and how variable it is across species. We then developed a model to explain why these relationships exist. METHODS: To minimize potential sources of variability, we compared twig properties from six co-occurring and functionally similar species: Acer grandidentatum, Amelanchier alnifolia, Betula occidentalis, Cornus sericea, Populus fremontii and Symphoricarpos oreophilus We modelled the economics of leaf display, weighing the benefit from light absorption against the cost of leaf tissue, to predict the optimal [Formula: see text] combinations under different canopy openings. KEY RESULTS: We observed a common [Formula: see text] by [Formula: see text] exponent of 0.6, meaning that [Formula: see text]and leaf number on twigs increased in a specific coordination. Common scaling exponents were not supported for relationships between any other measured twig properties. The model consistently predicted positive [Formula: see text] by [Formula: see text] scaling when twigs optimally filled canopy openings. The observed 0·6 exponent was predicted when self-shading decreased with larger canopy opening. CONCLUSIONS: Our results suggest Corner's rule may be better understood when recast as positive [Formula: see text] by [Formula: see text] scaling. Our model provides a tentative explanation of observed [Formula: see text] by [Formula: see text] scaling and suggests different scaling may exist in different environments.

Mapping 'hydroscapes' along the iso- to anisohydric continuum of stomatal regulation of plant water status.

The concept of iso- vs. anisohydry has been used to describe the stringency of stomatal regulation of plant water potential (ψ). However, metrics that accurately and consistently quantify species' operating ranges along a continuum of iso- to anisohydry have been elusive. Additionally, most approaches to quantifying iso/anisohydry require labour-intensive measurements during prolonged drought. We evaluated new and previously developed metrics of stringency of stomatal regulation of ψ during soil drying in eight woody species and determined whether easily-determined leaf pressure-volume traits could serve as proxies for their degree of iso- vs. anisohydry. Two metrics of stringency of stomatal control of ψ, (1) a 'hydroscape' incorporating the landscape of ψ over which stomata control ψ, and (2) the slope of the daily range of ψ as pre-dawn ψ declined, were strongly correlated with each other and with the leaf osmotic potential at full and zero turgor derived from pressure-volume curves.

The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off.

Forest ecosystems store approximately 45% of the carbon found in terrestrial ecosystems, but they are sensitive to climate-induced dieback. Forest die-off constitutes a large uncertainty in projections of climate impacts on terrestrial ecosystems, climate-ecosystem interactions, and carbon-cycle feedbacks. Current understanding of the physiological mechanisms mediating climate-induced forest mortality limits the ability to model or project these threshold events. We report here a direct and in situ study of the mechanisms underlying recent widespread and climate-induced trembling aspen (Populus tremuloides) forest mortality in western North America. We find substantial evidence of hydraulic failure of roots and branches linked to landscape patterns of canopy and root mortality in this species. On the contrary, we find no evidence that drought stress led to depletion of carbohydrate reserves. Our results illuminate proximate mechanisms underpinning recent aspen forest mortality and provide guidance for understanding and projecting forest die-offs under climate change.

Deviation from symmetrically self-similar branching in trees predicts altered hydraulics, mechanics, light interception and metabolic scaling.

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 Kα 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, Pf : mean/maximum trunk-to-twig pathlength. WBE symmetry produces the maximum, Pf = 1.0. We explored tree morphospace using a probability-based numerical model constrained only by biomechanical principles. Real tree Pf ranged from 0.930 (nearly symmetric) to 0.357 (very asymmetric). At each modeled tree size, a reduction in Pf led to: increased K; decreased V; increased mechanical stability; and decreased light absorption. When Pf was ontogenetically constant, strong asymmetry only slightly steepened metabolic scaling. The Pf 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.

Coordination between water transport capacity, biomass growth, metabolic scaling and species stature in co-occurring shrub and tree species.

The significance of xylem function and metabolic scaling theory begins from the idea that water transport is strongly coupled to growth rate. At the same time, coordination of water transport and growth seemingly should differ between plant functional types. We evaluated the relationships between water transport, growth and species stature in six species of co-occurring trees and shrubs. Within species, a strong proportionality between plant hydraulic conductance (K), sap flow (Q) and shoot biomass growth (G) was generally supported. Across species, however, trees grew more for a given K or Q than shrubs, indicating greater growth-based water-use efficiency (WUE) in trees. Trees also showed slower decline in relative growth rate (RGR) than shrubs, equivalent to a steeper G by mass (M) scaling exponent in trees (0.77-0.98). The K and Q by M scaling exponents were common across all species (0.80, 0.82), suggesting that the steeper G scaling in trees reflects a size-dependent increase in their growth-based WUE. The common K and Q by M exponents were statistically consistent with the 0.75 of ideal scaling theory. A model based upon xylem anatomy and branching architecture consistently predicted the observed K by M scaling exponents but only when deviations from ideal symmetric branching were incorporated.

Greater ecophysiological stress tolerance in the core environment than in extreme environments of wild chickpea (Cicer reticulatum).

Global climate change and land use change underlie a need to develop new crop breeding strategies, and crop wild relatives (CWR) have become an important potential source of new genetic material to improve breeding efforts. Many recent approaches assume adaptive trait variation increases towards the relative environmental extremes of a species range, potentially missing valuable trait variation in more moderate or typical climates. Here, we leveraged distinct genotypes of wild chickpea (Cicer reticulatum) that differ in their relative climates from moderate to more extreme and perform targeted assessments of drought and heat tolerance. We found significance variation in ecophysiological function and stress tolerance between genotypes but contrary to expectations and current paradigms, it was individuals from more moderate climates that exhibited greater capacity for stress tolerance than individuals from warmer and drier climates. These results indicate that wild germplasm collection efforts to identify adaptive variation should include the full range of environmental conditions and habitats instead of only environmental extremes, and that doing so may significantly enhance the success of breeding programs broadly.

An empirical assessment of tree branching networks and implications for plant allometric scaling models.

Several theories predict whole-tree function on the basis of allometric scaling relationships assumed to emerge from traits of branching networks. To test this key assumption, and more generally, to explore patterns of external architecture within and across trees, we measure branch traits (radii/lengths) and calculate scaling exponents from five functionally divergent species. Consistent with leading theories, including metabolic scaling theory, branching is area preserving and statistically self-similar within trees. However, differences among scaling exponents calculated at node- and whole-tree levels challenge the assumption of an optimised, symmetrically branching tree. Furthermore, scaling exponents estimated for branch length change across branching orders, and exponents for scaling metabolic rate with plant size (or number of terminal tips) significantly differ from theoretical predictions. These findings, along with variability in the scaling of branch radii being less than for branch lengths, suggest extending current scaling theories to include asymmetrical branching and differential selective pressures in plant architectures.

At least it is a dry cold: the global distribution of freeze-thaw and drought stress and the traits that may impart poly-tolerance in conifers.

Conifers inhabit some of the most challenging landscapes where multiple abiotic stressors (e.g., aridity, freezing temperatures) often co-occur. Physiological tolerance to multiple stressors ('poly-tolerance') is thought to be rare because exposure to one stress generally limits responses to another through functional trade-offs. However, the capacity to exhibit poly-tolerance may be greater when combined abiotic stressors have similar physiological impacts, such as the disruption of hydraulic function imposed by drought or freezing. Here, we reviewed empirical data in light of theoretical expectations for conifer adaptations to drought and freeze-thaw cycles with particular attention to hydraulic traits of the stem and leaf. Additionally, we examined the commonality and spatial distribution of poly-stress along indices of these combined stressors. We found that locations with the highest values of our poly-stress index (PSi) are characterized by moderate drought and moderate freeze-thaw, and most of the global conifer distribution occupies areas of moderate poly-stress. Among traits examined, we found diverse responses to the stressors. Turgor loss point did not correlate with freeze-thaw or drought stress individually, but did with the PSi, albeit inverse to what was hypothesized. Leaf mass per area was more strongly linked with drought stress than the poly-stress and not at all with freeze-thaw stress. In stems, the water potential causing 50% loss of hydraulic conductivity became more negative with increasing drought stress and poly-stress but did not correlate with freeze-thaw stress. For these traits, we identified a striking lack of coverage for substantial portions of species ranges, particularly at the upper boundaries of their respective PSis, demonstrating a critical gap in our understanding of trait prevalence and plasticity along these stress gradients. Future research should investigate traits that confer tolerance to both freeze-thaw and drought stress in a wide range of species across broad geographic scales.

Ecophysiological adaptations shape distributions of closely related trees along a climatic moisture gradient.

Tradeoffs between the energetic benefits and costs of traits can shape species and trait distributions along environmental gradients. Here we test predictions based on such tradeoffs using survival, growth, and 50 photosynthetic, hydraulic, and allocational traits of ten Eucalyptus species grown in four common gardens along an 8-fold gradient in precipitation/pan evaporation (P/Ep) in Victoria, Australia. Phylogenetically structured tests show that most trait-environment relationships accord qualitatively with theory. Most traits appear adaptive across species within gardens (indicating fixed genetic differences) and within species across gardens (indicating plasticity). However, species from moister climates have lower stomatal conductance than others grown under the same conditions. Responses in stomatal conductance and five related traits appear to reflect greater mesophyll photosynthetic sensitivity of mesic species to lower leaf water potential. Our data support adaptive cross-over, with realized height growth of most species exceeding that of others in climates they dominate. Our findings show that pervasive physiological, hydraulic, and allocational adaptations shape the distributions of dominant Eucalyptus species along a subcontinental climatic moisture gradient, driven by rapid divergence in species P/Ep and associated adaptations.

Rare pits, large vessels and extreme vulnerability to cavitation in a ring-porous tree species.

• The rare pit hypothesis predicts that the extensive inter-vessel pitting in large early-wood vessels of ring-porous trees should render many of these vessels extremely vulnerable to cavitation by air-seeding. This prediction was tested in Quercus gambelii. • Cavitation was assessed from native hydraulic conductivity at field sap tension and in dehydrated branches. Single-vessel air injections gave air-seeding pressures through vessel files; these data were used to estimate air-seeding pressures for inter-vessel walls and pits. • Extensive cavitation occurred at xylem sap tensions below 1 MPa. Refilling occurred below 0.5 MPa and was inhibited by phloem girdling. Remaining vessels cavitated over a wide range to above 4 MPa. Similarly, 40% of injected vessel files air-seeded below 1.0 MPa, whereas the remainder seeded over a wide range exceeding 5 MPa. Inter-vessel walls averaged 1.02 MPa air-seeding pressure, similar and opposite to the mean cavitation tension of 1.22 MPa. Consistent with the rare pit hypothesis, only 7% of inter-vessel pits were estimated to air-seed by 1.22 MPa. • The results confirm the rare pit prediction that a significant fraction of large vessels in Q. gambelii experience high probability of failure by air-seeding.