Hydraulic segmentation explains differences in loss of branch conductance caused by fire.

The hydraulic death hypothesis suggests that fires kill trees by damaging the plant's hydraulic continuum in addition to stem cambium. A corollary to this hypothesis is that plants that survive fires possess 'pyrohydraulic' traits that prevent heat-induced embolism formation in the xylem and aid post-fire survival. We examine whether hydraulic segmentation within stem xylem may act as such a trait. To do so, we measured the percentage loss of conductance (PLC) and vulnerability to embolism axially along segments of branches exposed to heat plumes in two differing species, fire-tolerant Eucalyptus cladocalyx F. Muell and fire-sensitive Kiggelaria africana L., testing model predictions that fire-tolerant species would exhibit higher degrees of hydraulic segmentation (greater PLC in the distal parts of the branch than the basal) than fire-intolerant species (similar PLC between segments). Following exposure to a heat plume, K. africana suffered between 73 and 84% loss of conductance in all branch segments, whereas E. cladocalyx had 73% loss of conductance in whole branches, including the distal tips, falling to 29% in the most basal part of the branch. There was no evidence for differences in resistance segmentation between the species, and there was limited evidence for differences in distal vulnerability to embolism across the branches. Hydraulic segmentation in E. cladocalyx may enable it to resprout effectively post-fire with a functional hydraulic system. The lack of hydraulic segmentation in K. africana reveals the need to understand possible trade-offs associated with hydraulic segmentation in long-lived woody species with respect to drought and fire.

Exploring within-plant hydraulic trait variation: A test of the vulnerability segmentation hypothesis.

Observations show vulnerability segmentation between stems and leaves is highly variable within and between environments. While a number of species exhibit conventional vulnerability segmentation (stem P 50 < ${P}_{50}\lt $ leaf P 50 ${P}_{50}$ ), others exhibit no vulnerability segmentation and others reverse vulnerability segmentation (stem P 50 > ${P}_{50}\gt $ leaf P 50 ${P}_{50}$ ). We developed a hydraulic model to test hypotheses about vulnerability segmentation and how it interacts with other traits to impact plant conductance. We do this using a series of experiments across a broad parameter space and with a case study of two species with contrasting vulnerability segmentation patterns: Quercus douglasii and Populus trichocarpa. We found that while conventional vulnerability segmentation helps to preserve conductance in stem tissues, reverse vulnerability segmentation can better maintain conductance across the combined stem-leaf hydraulic pathway, particularly when plants have more vulnerable P 50 ${P}_{50}$ s and have hydraulic segmentation with greater resistance in the leaves. These findings show that the impacts of vulnerability segmentation are dependent upon other plant traits, notably hydraulic segmentation, a finding that could assist in the interpretation of variable observations of vulnerability segmentation. Further study is needed to examine how vulnerability segmentation impacts transpiration rates and recovery from water stress.

Consistent responses to moisture stress despite diverse growth forms within mountain fynbos communities.

Understanding climate change impacts on the Cape Floristic Region requires improved knowledge of plant physiological responses to the environment. Studies examining physiological responses of mountain fynbos have consisted of campaign-based measurements, capturing snapshots of plant water relations and photosynthesis. We examine conclusions drawn from prior studies by tracking in situ physiological responses of three species, representing dominant growth forms (proteoid, ericoid, restioid), over 2 years using miniature continuous sap flow technology, long-term observations of leaf/culm water potential and gas exchange, and xylem vulnerability to embolism. We observed considerable inter-specific variation in the timing and extent of seasonal declines in productivity. Shallow-rooted Erica monsoniana exhibited steep within-season declines in sap flow and water potentials, and pronounced inter-annual variability in total daily sap flux (Js). Protea repens showed steady reductions in Js across both years, despite deeper roots and less negative water potentials. Cannomois congesta-a shallow-rooted restioid-was least negatively impacted. Following rehydrating rain at the end of summer, gas exchange recovery was lower in the drier year compared with the normal year, but did not differ between species. Loss of function in the drier year was partially accounted for by loss of xylem transport capacity in Erica and Cannomois, but not Protea. Hitherto unseen water use patterns, including inter-annual variability of gas exchange associated with contrasting water uptake properties, reveal that species use different mechanisms to cope with summer dry periods. Revealing physiological responses of key growth forms enhances predictions of plant function within mountain fynbos under future conditions.

Evolutionary relationships between drought-related traits and climate shape large hydraulic safety margins in western North American oaks.

Quantitative knowledge of xylem physical tolerance limits to dehydration is essential to understanding plant drought tolerance but is lacking in many long-vessel angiosperms. We examine the hypothesis that a fundamental association between sustained xylem water transport and downstream tissue function should select for xylem that avoids embolism in long-vessel trees by quantifying xylem capacity to withstand air entry of western North American oaks (Quercus spp.). Optical visualization showed that 50% of embolism occurs at water potentials below -2.7 MPa in all 19 species, and -6.6 MPa in the most resistant species. By mapping the evolution of xylem vulnerability to embolism onto a fossil-dated phylogeny of the western North American oaks, we found large differences between clades (sections) while closely related species within each clade vary little in their capacity to withstand air entry. Phylogenetic conservatism in xylem physical tolerance, together with a significant correlation between species distributions along rainfall gradients and their dehydration tolerance, suggests that closely related species occupy similar climatic niches and that species' geographic ranges may have shifted along aridity gradients in accordance with their physical tolerance. Such trends, coupled with evolutionary associations between capacity to withstand xylem embolism and other hydraulic-related traits, yield wide margins of safety against embolism in oaks from diverse habitats. Evolved responses of the vascular system to aridity support the embolism avoidance hypothesis and reveal the importance of quantifying plant capacity to withstand xylem embolism for understanding function and biogeography of some of the Northern Hemisphere's most ecologically and economically important plants.

No local adaptation in leaf or stem xylem vulnerability to embolism, but consistent vulnerability segmentation in a North American oak.

Vulnerability to embolism varies between con-generic species distributed along aridity gradients, yet little is known about intraspecific variation and its drivers. Even less is known about intraspecific variation in tissues other than stems, despite results suggesting that roots, stems and leaves can differ in vulnerability. We hypothesized that intraspecific variation in vulnerability in leaves and stems is adaptive and driven by aridity. We quantified leaf and stem vulnerability of Quercus douglasii using the optical technique. To assess contributions of genetic variation and phenotypic plasticity to within-species variation, we quantified the vulnerability of individuals growing in a common garden, but originating from populations along an aridity gradient, as well as individuals from the same wild populations. Intraspecific variation in water potential at which 50% of total embolism in a tissue is observed (P50 ) was explained mostly by differences between individuals (>66% of total variance) and tissues (16%). There was little between-population variation in leaf/stem P50 in the garden, which was not related to site of origin aridity. Unexpectedly, we observed a positive relationship between wild individual stem P50 and aridity. Although there is no local adaptation and only minor phenotypic plasticity in leaf/stem vulnerability in Q. douglasii, high levels of potentially heritable variation within populations or strong environmental selection could contribute to adaptive responses under future climate change.

Beyond isohydricity: The role of environmental variability in determining plant drought responses.

Despite the appeal of the iso/anisohydric framework for classifying plant drought responses, recent studies have shown that such classifications can be strongly affected by a plant's environment. Here, we present measured in situ drought responses to demonstrate that apparent isohydricity can be conflated with environmental conditions that vary over space and time. In particular, we (a) use data from an oak species (Quercus douglasii) during the 2012-2015 extreme drought in California to demonstrate how temporal and spatial variability in the environment can influence plant water potential dynamics, masking the role of traits; (b) explain how these environmental variations might arise from climatic, topographic, and edaphic variability; (c) illustrate, through a "common garden" thought experiment, how existing trait-based or response-based isohydricity metrics can be confounded by these environmental variations, leading to Type-1 (false positive) and Type-2 (false negative) errors; and (d) advocate for the use of model-based approaches for formulating alternate classification schemes. Building on recent insights from greenhouse and vineyard studies, we offer additional evidence across multiple field sites to demonstrate the importance of spatial and temporal drivers of plants' apparent isohydricity. This evidence challenges the use of isohydricity indices, per se, to characterize plant water relations at the global scale.

Gas exchange recovery following natural drought is rapid unless limited by loss of leaf hydraulic conductance: evidence from an evergreen woodland.

Drought can cause major damage to plant communities, but species damage thresholds and postdrought recovery of forest productivity are not yet predictable. We used an El Niño drought event as a natural experiment to test whether postdrought recovery of gas exchange could be predicted by properties of the water transport system, or if metabolism, primarily high abscisic acid concentration, might delay recovery. We monitored detailed physiological responses, including shoot sapflow, leaf gas exchange, leaf water potential and foliar abscisic acid (ABA), during drought and through the subsequent rehydration period for a sample of eight canopy and understory species. Severe drought caused major declines in leaf water potential, elevated foliar ABA concentrations and reduced stomatal conductance and assimilation rates in our eight sample species. Leaf water potential surpassed levels associated with incipient loss of leaf hydraulic conductance in four species. Following heavy rainfall gas exchange in all species, except those trees predicted to have suffered hydraulic impairment, recovered to prestressed rates within 1 d. Recovery of plant gas exchange was rapid and could be predicted by the hydraulic safety margin, providing strong support for leaf vulnerability to water deficit as an index of damage under natural drought conditions.

Casting light on xylem vulnerability in an herbaceous species reveals a lack of segmentation.

Finding thresholds at which loss of plant functionality occurs during drought is critical for predicting future crop productivity and survival. Xylem resistance to embolism has been suggested as a key trait associated with water-stress tolerance. Although a substantial literature exists describing the vulnerability of woody stems to embolism, leaves and roots of herbaceous species remain under-represented. Also, little is known about vulnerability to embolism at a whole-plant scale or propagation of embolism within plants. New techniques to view the process of embolism formation provide opportunities to resolve long-standing questions. Here, we used multiple visual techniques, including X-ray micro-computed tomography and the optical vulnerability method, to investigate the spread of embolism within intact stems, leaves and roots of Solanum lycopersicum (common tomato). We found that roots, stems and leaves of tomato plants all exhibited similar vulnerability to embolism, suggesting that embolism rapidly propagates among tissues. Although we found scarce evidence for differentiation of xylem vulnerability among tissues at the scale of the whole plant, within a leaf the midrib embolized at higher water potentials than lower order veins. Substantial overlap between the onset of cavitation and incipient leaf damage suggests that cavitation represents a substantial damage to plants, but the point of lethal cavitation in this herbaceous species remains uncertain.

Visual quantification of embolism reveals leaf vulnerability to hydraulic failure.

Vascular plant mortality during drought has been strongly linked to a failure of the internal water transport system caused by the rapid invasion of air and subsequent blockage of xylem conduits. Quantification of this critical process is greatly complicated by the existence of high water tension in xylem cells making them prone to embolism during experimental manipulation. Here we describe a simple new optical method that can be used to record spatial and temporal patterns of embolism formation in the veins of water-stressed leaves for the first time. Applying this technique in four diverse angiosperm species we found very strong agreement between the dynamics of embolism formation during desiccation and decline of leaf hydraulic conductance. These data connect the failure of the leaf water transport network under drought stress to embolism formation in the leaf xylem, and suggest embolism occurs after stomatal closure under extreme water stress.

External heat-pulse method allows comparative sapflow measurements in diverse functional types in a Mediterranean-type shrubland in South Africa.

There has been limited application of sapflow technology to small-stemmed species and across co-existing functional types, restricting its use in diverse floras such as the Mediterranean-type shrubland in South Africa. Our main objective was to test whether sapflow may provide an alternative to traditional gas-exchange measurements, which would permit comparative evaluation of transpiration at a previously unattained temporal resolution. We tested miniature external heat ratio method (HRM) sapflow gauges on three co-occurring functional types with contrasting stem or culm anatomies and examined the relationship between sapflow and shoot- and leaf-level water loss in both a controlled and field environment. Our sapflow gauges captured dynamic patterns of transpiration in both settings for all three functional types. In a controlled environment the relationship between sapflow and transpiration was linear in all three species with r2 values ranging from 0.78 for Cannomois congesta Mast. (Restionaceae) to 0.96 for Protea repens (L.) L. (Proteaceae) and Erica monsoniana L.f. (Ericaceae). In the field, r2 values were lower, ranging from 0.59 for C. congesta to 0.74 for P. repens. We discuss the efficacy and potential of this methodology to cast light on patterns of community ecology in functionally diverse shrublands by capturing continuous variation in transpiration.