Contrasting shrub and grass hydraulic responses to experimental drought.

Whole-plant hydraulics provide important information about responses to water limitation and can be used to understand how plant communities may change in a drier climate when measured on multiple species. Here, we measured above- and belowground hydraulic traits in Cornus drummondii, an encroaching shrub within North American tallgrass prairies, and Andropogon gerardii, a dominant C4 grass, to assess the potential hydraulic responses to future drought as this region undergoes woody expansion. Shelters that reduced precipitation by 50% and 0% were built over shrubs and grasses growing in sites that are burned at 1-year and 4-year frequencies. We then measured aboveground (Kshoot), belowground (Kroot), and whole-plant maximum hydraulic conductance (Kplant) in C. drummondii and Kroot in A. gerardii. We also measured vulnerability to embolism (P50) in C. drummondii stems. Overall, we show that: (1) A. gerardii had substantially greater Kroot than C. drummondii; (2) belowground hydraulic functioning was linked with aboveground processes; (3) above- and belowground C. drummondii hydraulics were not negatively impacted by the rainfall reductions imposed here. These results suggest that a multi-year drought will not ameliorate rates of woody expansion and highlight key differences in aboveground and belowground hydraulics for dominant species within the same ecosystem.

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.

Reproductive phases coincide with changes in morphology and photosynthetic physiology in an endangered cycad species.

Cycadales is highly endangered and one of the oldest dioecious gymnosperm lineages, making their reproductive biology highly relevant to conservation efforts and our understanding of the impact of dioecy, yet cycad reproductive ecophysiology is poorly understood. We examined how the costs associated with reproduction may impact basic physiological variation in cycad species. Specifically, we measured traits related to functional morphology and photosynthetic physiology in sterile and fertile staminate plants ('males') of Zamia portoricensis. Light response curves showed that sterile plants had greater light-use efficiency and maximum photosynthetic capacity per area compared with fertile plants. However, fertile and sterile plants exhibited similar respiration rates. We found significantly more nitrogen in leaves of fertile individuals, but similar nitrogen isotope composition and no differences in carbon content between sterile and fertile individuals. Despite having lower leaf-level photosynthetic rates, fertile plants had greater canopy-level photosynthesis than sterile plants, which was achieved by increasing leaf number and total leaf area. Our data suggest that sterile individuals may have greater light demands relative to fertile individuals, and fertile individuals may have greater nitrogen demands, which may be critical for successful reproductive events in staminate plants of the endangered cycad, Z. portoricensis.

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.

Functional traits and trait coordination change over the life of a leaf in a tropical fern species.

PREMISE: Plant ecological strategies are often defined by the integration of underlying traits related to resource acquisition, allocation, and growth. Correlations between key traits across diverse plants suggest that variation in plant ecological strategies is largely driven by a fast-slow continuum of plant economics. However, trait correlations may not be constant through the life of a leaf, and it is still poorly understood how trait function varies over time in long-lived leaves. METHODS: Here, we compared trait correlations related to resource acquisition and allocation across three different mature frond age cohorts in a tropical fern species, Saccoloma inaequale. RESULTS: Fronds exhibited high initial investments of nitrogen and carbon, but with declining return in photosynthetic capacity after the first year. In the youngest fronds, we found water-use efficiency to be significantly lower than in the oldest mature fronds due to increased transpiration rates. Our data suggest that middle-aged fronds are more efficient relative to younger, less water-use efficient fronds and that older fronds exhibit greater nitrogen investments without higher photosynthetic return. In addition, several trait correlations expected under the leaf economics spectrum (LES) do not hold within this species, and some trait correlations only appear in fronds of a specific developmental age. CONCLUSIONS: These findings contextualize the relationship between traits and leaf developmental age with those predicted to underlie plant ecological strategy and the LES and are among the first pieces of evidence for when relative physiological trait efficiency is maximized in a tropical fern species.

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.

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.

Trehalose increases tomato drought tolerance, induces defenses, and increases resistance to bacterial wilt disease.

Ralstonia solanacearum causes bacterial wilt disease, leading to severe crop losses. Xylem sap from R. solanacearum-infected tomato is enriched in the disaccharide trehalose. Water-stressed plants also accumulate trehalose, which increases drought tolerance via abscisic acid (ABA) signaling. Because R. solanacearum-infected plants suffer reduced water flow, we hypothesized that bacterial wilt physiologically mimics drought stress, which trehalose could mitigate. We found that R. solanacearum-infected plants differentially expressed drought-associated genes, including those involved in ABA and trehalose metabolism, and had more ABA in xylem sap. Consistent with this, treating tomato roots with ABA reduced both stomatal conductance and stem colonization by R. solanacearum. Treating roots with trehalose increased xylem sap ABA and reduced plant water use by lowering stomatal conductance and temporarily improving water use efficiency. Trehalose treatment also upregulated expression of salicylic acid (SA)-dependent tomato defense genes; increased xylem sap levels of SA and other antimicrobial compounds; and increased bacterial wilt resistance of SA-insensitive NahG tomato plants. Additionally, trehalose treatment increased xylem concentrations of jasmonic acid and related oxylipins. Finally, trehalose-treated plants were substantially more resistant to bacterial wilt disease. Together, these data show that exogenous trehalose reduced both water stress and bacterial wilt disease and triggered systemic disease resistance, possibly through a Damage Associated Molecular Pattern (DAMP) response pathway. This suite of responses revealed unexpected linkages between plant responses to biotic and abiotic stress and suggested that R. solanacearum-infected plants increase trehalose to improve water use efficiency and increase wilt disease resistance. The pathogen may degrade trehalose to counter these efforts. Together, these results suggest that treating tomatoes with exogenous trehalose could be a practical strategy for bacterial wilt management.

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.

Tip-to-base xylem conduit widening as an adaptation: causes, consequences, and empirical priorities.

In the stems of terrestrial vascular plants studied to date, the diameter of xylem water-conducting conduits D widens predictably with distance from the stem tip L approximating D âˆ Lb , with b ≈ 0.2. Because conduit diameter is central for conductance, it is essential to understand the cause of this remarkably pervasive pattern. We give reason to suspect that tip-to-base conduit widening is an adaptation, favored by natural selection because widening helps minimize the increase in hydraulic resistance that would otherwise occur as an individual stem grows longer and conductive path length increases. Evidence consistent with adaptation includes optimality models that predict the 0.2 exponent. The fact that this prediction can be made with a simple model of a single capillary, omitting much biological detail, itself makes numerous important predictions, e.g. that pit resistance must scale isometrically with conduit resistance. The idea that tip-to-base conduit widening has a nonadaptive cause, with temperature, drought, or turgor limiting the conduit diameters that plants are able to produce, is less consistent with the data than an adaptive explanation. We identify empirical priorities for testing the cause of tip-to-base conduit widening and underscore the need to study plant hydraulic systems leaf to root as integrated wholes.

Limited physiological acclimation to recurrent heatwaves in two boreal tree species.

The intensity of extreme heat and drought events has drastically risen in recent decades and will likely continue throughout the century. Northern forests have already seen increases in tree mortality and a lack of new recruitment, which is partially attributed to these extreme events. Boreal species, such as paper birch (Betula papyrifera) and white spruce (Picea glauca), appear to be more sensitive to these changes than lower-latitude species. Our objectives were to investigate the effects of repeated heatwaves and drought on young paper birch and white spruce trees by examining (i) responses in leaf gas exchange and plant growth and (ii) thermal acclimation of photosynthetic and respiratory traits to compare ecophysiological responses of two co-occurring, yet functionally dissimilar species. To address these objectives, we subjected greenhouse-grown seedlings to two consecutive summers of three 8-day long, +10 °C heatwaves in elevated atmospheric CO2 conditions with and without water restriction. The data show that heatwave stress reduced net photosynthesis, stomatal conductance and growth-more severely so when combined with drought. Acclimation of both photosynthesis and respiration did not occur in either species. The combination of heat and drought stress had a similar total effect on both species, but each species adjusted traits differently to the combined stress. Birch experienced greater declines in gas exchange across both years and showed moderate respiratory but not photosynthetic acclimation to heatwaves. In spruce, heatwave stress reduced the increase in basal area in both experimental years and had a minor effect on photosynthetic acclimation. The data suggest these species lack the ability to physiologically adjust to extreme heat events, which may limit their future distributions, thereby altering the composition of boreal forests.

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.

A new protocol for psychrometric pressure-volume curves of fern gametophytes.

PREMISE: Pressure-volume curves are a widely used analytical framework to derive several key physiological traits related to plant-water relations, including a species' turgor loss point, osmotic potential at full turgor, and the elasticity of cell walls. We developed a novel protocol, including the preparation and treatment of fern gametophytes, to generate data for pressure-volume curve analyses using thermocouple psychrometry. METHODS AND RESULTS: Gametophytes of the fern species Polystichum lemmonii were grown from spore, harvested, and subjected to a series of drying intervals. We constructed pressure-volume curves using thermocouple psychrometers to calculate gametophyte water potential and a balance to measure relative water loss. CONCLUSIONS: We present the first protocol for fern gametophyte pressure-volume curves that can accurately determine key physiological traits in fern gametophytes such as the turgor loss point and osmotic potential at full turgor.

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.

Linking leaf hydraulic properties, photosynthetic rates, and leaf lifespan in xerophytic species: a test of global hypotheses.

PREMISE OF THE STUDY: Leaf venation and its hierarchal traits are crucial to the hydraulic and mechanical properties of leaves, reflecting plant life-history strategies. However, there is an extremely limited understanding of how variation in leaf hydraulics affects the leaf economic spectrum (LES) or whether venation correlates more strongly with hydraulic conductance or biomechanical support among hierarchal orders. METHODS: We examined correlations of leaf hydraulics, indicated by vein density, conduit diameter, and stomatal density with light-saturated photosynthetic rates, leaf lifespan (LLS), and leaf morpho-anatomical traits of 39 xerophytic species grown in a common garden. KEY RESULTS: We found positive relationships between light-saturated, area-based photosynthetic rates, and vein densities, regardless of vein orders. Densities of leaf veins had positive correlations with stomatal density. We also found positive relationships between LLS and vein densities. Leaf area was negatively correlated with the density of major veins but not with minor veins. Most anatomical traits were not related to vein densities. CONCLUSIONS: We developed a network diagram of the correlations among leaf hydraulics and leaf economics, which suggests functional trade-offs between hydraulic costs and lifetime carbon gain. Leaf hydraulics efficiency and carbon assimilation were coupled across species. Vein construction costs directly coordinated with the LLS. Our findings indicate that hierarchal orders of leaf veins did not differ in the strength of their correlations between hydraulic conductance and biomechanical support. These findings clarify how leaf hydraulics contributes to the LES and provide new insight into life-history strategies of these xerophytic species.

Vessel scaling in evergreen angiosperm leaves conforms with Murray's law and area-filling assumptions: implications for plant size, leaf size and cold tolerance.

Water transport in leaf vasculature is a fundamental process affecting plant growth, ecological interactions and ecosystem productivity, yet the architecture of leaf vascular networks is poorly understood. Although Murray's law and the West-Brown-Enquist (WBE) theories predict convergent scaling of conduit width and number, it is not known how conduit scaling is affected by habitat aridity or temperature. We measured the scaling of leaf size, conduit width and conduit number within the leaves of 36 evergreen Angiosperms spanning a large range in aridity and temperature in eastern Australia. Scaling of conduit width and number in midribs and 2° veins did not differ across species and habitats (P > 0.786), and did not differ from that predicted by Murray's law (P = 0.151). Leaf size was strongly correlated with the hydraulic radius of petiole conduits (r2  = 0.83, P < 0.001) and did not differ among habitats (P > 0.064), nor did the scaling exponent differ significantly from that predicted by hydraulic theory (P = 0.086). The maximum radius of conduits in petioles was positively correlated with the temperature of the coldest quarter (r2  = 0.67; P < 0.001), suggesting that habitat temperature restricts the occurrence of wide-conduit species in cold habitats.

Water relations of Calycanthus flowers: Hydraulic conductance, capacitance, and embolism resistance.

For most angiosperms, producing and maintaining flowers is critical to sexual reproduction, yet little is known about the physiological processes involved in maintaining flowers throughout anthesis. Among extant species, flowers of the genus Calycanthus have the highest hydraulic conductance and vein densities of species measured to date, yet they can wilt by late morning under hot conditions. Here, we combine diurnal measurements of gas exchange and water potential, pressure-volume relations, functional responses of gas exchange, and characterization of embolism formation using high resolution X-ray computed microtomography to determine drought responses of Calycanthus flowers. Transpiration from flowers frequently exceeded transpiration from leaves, and flowers were unable to limit transpiration under conditions of high vapour pressure deficit. As a result, they rely heavily on hydraulic capacitance to prevent water potential declines. Despite having high water potentials at turgor loss, flowers were very resistant to embolism formation, with no embolism apparent until tepal water potentials had declined to -2 MPa. Although Calycanthus flowers remain connected to the stem xylem and have high hydraulic capacitance, their inability to curtail transpiration leads to turgor loss. These results suggest that extreme climate events may cause flower failure, potentially preventing successful reproduction.

Co-occurring woody species have diverse hydraulic strategies and mortality rates during an extreme drought.

From 2011 to 2013, Texas experienced its worst drought in recorded history. This event provided a unique natural experiment to assess species-specific responses to extreme drought and mortality of four co-occurring woody species: Quercus fusiformis, Diospyros texana, Prosopis glandulosa, and Juniperus ashei. We examined hypothesized mechanisms that could promote these species' diverse mortality patterns using postdrought measurements on surviving trees coupled to retrospective process modelling. The species exhibited a wide range of gas exchange responses, hydraulic strategies, and mortality rates. Multiple proposed indices of mortality mechanisms were inconsistent with the observed mortality patterns across species, including measures of the degree of iso/anisohydry, photosynthesis, carbohydrate depletion, and hydraulic safety margins. Large losses of spring and summer whole-tree conductance (driven by belowground losses of conductance) and shallower rooting depths were associated with species that exhibited greater mortality. Based on this retrospective analysis, we suggest that species more vulnerable to drought were more likely to have succumbed to hydraulic failure belowground.