Acclimation of interacting leaf surface traits affects foliar water uptake.

Absorption of water across the surfaces of leaves is an ecologically important aspect of tree physiology. Variation in foliar water uptake capacity depends on environmental conditions when traits associated with the uptake pathway respond to climatic signals. Using a series of experiments, we verify that water enters Sequoia sempervirens (D. Don) Endl. leaves by crossing the cuticle, and show that surface-trait acclimation alters the kinetic parameters of foliar water uptake. Under our experimental conditions, the cuticle was the primary pathway for water entry into the leaf. Exposure to climatic variation may induce surface acclimations, such as increased waxiness, that reduce water-film formation over stomata at the expense of dry-season foliar uptake rates. We found that water uptake is negatively associated with the interaction of leaf-surface wax coverage and stomatal density, and provide an accessible protocol to measure these key traits in Sequoia. Linking absorptive pathways and trait acclimation to physiological performance can provide a foundation for range-wide or genomic investigations of forest interactions with water and a mechanism-centered means to monitor canopy hydraulic parameters over time.

Conifer water-use patterns across temporal and topographic gradients in the southern Sierra Nevada.

Climate change is increasing the severity and duration of drought events experienced by forest ecosystems. Because water is essential for tree physiological processes, the ability of trees to survive prolonged droughts will largely depend on whether they have access to reliable water sources. While many woody plant species exhibit the ability to shift water sources between different depths of soil and rock water in response to changes in climate and water availability, it is unclear if Sierra Nevada conifers exhibit this plasticity. Here we analysed the δ18O and δ13C values of annual tree rings to determine the water-use patterns of large Sierra Nevada conifers during the 2012-16 California drought and 4 years before this drought event (2004-07). We analysed four species (Pinus jeffreyi Grev. & Balf. (Jeffrey pine), Pinus lambertiana Dougl. (sugar pine), Abies concolor (Gord. & Glend.) Lindl. Ex Hilderbr (white fir) and Calocedrus decurrens (Torr.) Florin (incense-cedar)) across a range of topographic positions to investigate differences in water-use patterns by species and position on the landscape. We found no significant differences in δ18O and δ13C values for the pre-drought and drought periods. This stability in δ18O values suggests that trees did not shift their water-use patterns in response to the 2012-16 drought. We did find species-specific differences in water-use patterns, with incense-cedar exhibiting more depleted δ18O values than all other species. We also found trends that suggest the water source used by a tree may depend on topographic and growing environment attributes such as topographic wetness and the surrounding basal area. Overall, our results suggest that the water source used by trees varies by the species and topographic position, but that Sierra Nevada conifers do not switch their water-use patterns in response to the drought. This lack of plasticity could make Sierra Nevada conifers particularly vulnerable to drought mortality as their historically reliable water sources begin to dry out with climate change.

Tracheid buckling buys time, foliar water uptake pays it back: Coordination of leaf structure and function in tall redwood trees.

Tracheid buckling may protect leaves in the dynamic environments of forest canopies, where rapid intensifications of evaporative demand, such as those brought on by changes in light availability, can result in sudden increases in transpiration rate. While treetop leaves function in reliably direct light, leaves below the upper crown must tolerate rapid, thermally driven increases in evaporative demand. Using synchrotron-based X-ray microtomography, we visualized impacts of experimentally induced water stress and subsequent fogging on living cells in redwood leaves, adding ecological and functional context through crown-wide explorations of variation in leaf physiology and microclimate. Under drought, leaf transfusion tracheids buckle, releasing water that supplies sufficient temporal reserves for leaves to reduce stomatal conductance safely while stopping the further rise of tension. Tracheid buckling fraction decreases with height and is closely coordinated with transfusion tissue capacity and stomatal conductance to provide temporal reserves optimized for local variation in microclimate. Foliar water uptake fully restores collapsed and air-filled transfusion tracheids in leaves on excised shoots, suggesting that trees may use aerial water sources for recovery. In the intensely variable deep-crown environment, foliar water uptake can allow for repetitive cycles of tracheid buckling and unbuckling, protecting the tree from damaging levels of hydraulic tension and supporting leaf survival.

Shoot dimorphism enables Sequoia sempervirens to separate requirements for foliar water uptake and photosynthesis.

PREMISE: Trees in wet forests often have features that prevent water films from covering stomata and inhibiting gas exchange, while many trees in drier environments use foliar water uptake to reduce water stress. In forests with both wet and dry seasons, evergreen trees would benefit from producing leaves capable of balancing rainy-season photosynthesis with summertime water absorption. METHODS: Using samples collected from across the vertical gradient in tall redwood (Sequoia sempervirens) crowns, we estimated tree-level foliar water uptake and employed physics-based causative modeling to identify key functional traits that determine uptake potential by setting hydraulic resistance. RESULTS: We showed that Sequoia has two functionally distinct shoot morphotypes. While most shoots specialize in photosynthesis, the axial shoot type is capable of much greater foliar water uptake, and its within-crown distribution varies with latitude. A suite of leaf surface traits cause hydraulic resistance, leading to variation in uptake capacity among samples. CONCLUSIONS: Shoot dimorphism gives tall Sequoia trees the capacity to absorb up to 48 kg H2 O h-1 during the first hour of leaf wetting, ameliorating water stress while presumably maintaining high photosynthetic capacity year round. Geographic variation in shoot dimorphism suggests that plasticity in shoot-type distribution and leaf surface traits helps Sequoia maintain a dominate presence in both wet and dry forests.

Vertical gradients in foliar physiology of tall Picea sitchensis trees.

In tall conifers, leaf structure can vary dramatically with height due to decreasing water potential (Ψ) and increasing light availability. This variation in leaf structure can have physiological consequences such as increased respiratory costs, reduced internal carbon dioxide conductance rates and ultimately reduced maximum photosynthetic rates (Amax). In Picea sitchensis (Bong.) Carrière, the leaf structure varies along the vertical gradient in ways that suggest compensatory changes to enhance photosynthesis, and this variation seems to be driven largely by light availability rather than by Ψ. These trends in leaf structure coupled with remarkably fast growth rates and dependence on moist environments inspire two important questions about P. sitchensis: (i) does foliar water uptake minimize the adverse effects of decreasing Ψ with height on leaf structure, and (ii) do trends in leaf structure increase photosynthetic rates despite increasing height? To answer these questions, we measured foliar water uptake capacity, predawn (Ψpd) and midday water potential and gas-exchange rates as they varied between 25- and 89-m heights in 300-year-old P. sitchensis trees in northwestern California. Our major findings for P. sitchensis include the following: (i) foliar water uptake capacity was quite high relative to published values for other woody species; (ii) foliar water uptake capacity increased between the crown base and treetop; (iii) wet season Ψpd was higher than predicted by the gravitational potential gradient, indicating foliar water uptake; and (iv) the maximum photosynthetic rate increased with height, presumably due to shifts in leaf structure between the crown base and treetop, mitigating height-related decreases in Amax. These findings suggest that together, the use of fog, dew and rain deposits on leaves and shifts in the leaf structure to conserve and possibly enhance photosynthetic capacity likely contribute to the rapid growth rates measured in this species.

Sensitivity of ring growth and carbon allocation to climatic variation vary within ponderosa pine trees.

Most dendrochronological studies focus on cores sampled from standard positions (main stem, breast height), yet vertical gradients in hydraulic constraints and priorities for carbon allocation may contribute to different growth sensitivities with position. Using cores taken from five positions (coarse roots, breast height, base of live crown, mid-crown branch and treetop), we investigated how radial growth sensitivity to climate over the period of 1895-2008 varies by position within 36 large ponderosa pines (Pinus ponderosa Dougl.) in northern Arizona. The climate parameters investigated were Palmer Drought Severity Index, water year and monsoon precipitation, maximum annual temperature, minimum annual temperature and average annual temperature. For each study tree, we generated Pearson correlation coefficients between ring width indices from each position and six climate parameters. We also investigated whether the number of missing rings differed among positions and bole heights. We found that tree density did not significantly influence climatic sensitivity to any of the climate parameters investigated at any of the sample positions. Results from three types of analyses suggest that climatic sensitivity of tree growth varied with position height: (i) correlations of radial growth and climate variables consistently increased with height; (ii) model strength based on Akaike's information criterion increased with height, where treetop growth consistently had the highest sensitivity and coarse roots the lowest sensitivity to each climatic parameter; and (iii) the correlation between bole ring width indices decreased with distance between positions. We speculate that increased sensitivity to climate at higher positions is related to hydraulic limitation because higher positions experience greater xylem tensions due to gravitational effects that render these positions more sensitive to climatic stresses. The low sensitivity of root growth to all climatic variables measured suggests that tree carbon allocation to coarse roots is independent of annual climate variability. The greater number of missing rings in branches highlights the fact that canopy development is a low priority for carbon allocation during poor growing conditions.