David R. Woodruff

Carbon dynamics in trees: feast or famine?

Research on the degree to which carbon (C) availability limits growth in trees, as well as recent trends in climate change and concurrent increases in drought-related tree mortality, have led to a renewed focus on the physiological mechanisms associated with tree growth responses to current and future climate. This has led to some dispute over the role of stored non-structural C compounds as indicators of a trees current demands for photosynthate. Much of the uncertainty surrounding this issue could be resolved by developing a better understanding of the potential functions of non-structural C stored within trees. In addition to functioning as a buffer to reconcile temporal asynchrony between C demand and supply, the storage of non-structural C compounds may be under greater regulation than commonly recognized. We propose that in the face of environmental stochasticity, large, long-lived trees may require larger C investments in storage pools as safety margins than previously recognized, and that an important function of these pools may be to maintain hydraulic transport, particularly during episodes of severe stress. If so, survival and long-term growth in trees remain a function of C availability. Given that drought, freeze-thaw events and increasing tree height all impose additional constraints on vascular transport, the common trend of an increase in non-structural carbohydrate concentrations with tree size, drought or cold is consistent with our hypothesis. If the regulated maintenance of relatively large constitutive stored C pools in trees serves to maintain hydraulic integrity, then the minimum thresholds are expected to vary depending on the specific tissues, species, environment, growth form and habit. Much research is needed to elucidate the extent to which allocation of C to storage in trees is a passive vs. an active process, the specific functions of stored C pools, and the factors that drive active C allocation to storage.

Maximum height in a conifer is associated with conflicting requirements for xylem design

Despite renewed interest in the nature of limitations on maximum tree height, the mechanisms governing ultimate and species-specific height limits are not yet understood, but they likely involve water transport dynamics. Tall trees experience increased risk of xylem embolism from air-seeding because tension in their water column increases with height because of path-length resistance and gravity. We used morphological measurements to estimate the hydraulic properties of the bordered pits between tracheids in Douglas-fir trees along a height gradient of 85 m. With increasing height, the xylem structural modifications that satisfied hydraulic requirements for avoidance of runaway embolism imposed increasing constraints on water transport efficiency. In the branches and trunks, the pit aperture diameter of tracheids decreases steadily with height, whereas torus diameter remains relatively constant. The resulting increase in the ratio of torus to pit aperture diameter allows the pits to withstand higher tensions before air-seeding but at the cost of reduced pit aperture conductance. Extrapolations of vertical trends for trunks and branches show that water transport across pits will approach zero at a heights of 109 m and 138 m, respectively, which is consistent with historic height records of 100–127 m for this species. Likewise, the twig water potential corresponding to the threshold for runaway embolism would be attained at a height of ≈107 m. Our results suggest that the maximum height of Douglas-fir trees may be limited in part by the conflicting requirements for water transport and water column safety.

Leaf hydraulic conductance, measured in situ, declines and recovers daily: leaf hydraulics, water potential and stomatal conductance in four temperate and three tropical tree species.

Adequate leaf hydraulic conductance (Kleaf) is critical for preventing transpiration-induced desiccation and subsequent stomatal closure that would restrict carbon gain. A few studies have reported midday depression of Kleaf (or petiole conductivity) and its subsequent recovery in situ, but the extent to which this phenomenon is universal is not known. The objectives of this study were to measure Kleaf, using a rehydration kinetics method, (1) in the laboratory (under controlled conditions) across a range of water potentials to construct vulnerability curves (VC) and (2) over the course of the day in the field along with leaf water potential and stomatal conductance (gs). Two broadleaf (one evergreen, Arbutus menziesii Pursh., and one deciduous, Quercus garryana Dougl.) and two coniferous species (Pinus ponderosa Dougl. and Pseudotsuga menziesii [Mirbel]) were chosen as representative of different plant types. In addition, Kleaf in the laboratory and leaf water potential in the field were measured for three tropical evergreen species (Protium panamense (Rose), Tachigalia versicolor Standley and L.O. Williams and Vochysia ferruginea Mart) to predict their daily changes in field Kleaf in situ. It was hypothesized that in the field, leaves would close their stomata at water potential thresholds at which Kleaf begins to decline sharply in laboratory-generated VC, thus preventing substantial losses of Kleaf. The temperate species showed a 15-66% decline in Kleaf by midday, before stomatal closure. Although there were substantial midday declines in Kleaf, recovery was nearly complete by late afternoon. Stomatal conductance began to decrease in Pseudotsuga, Pinus and Quercus once Kleaf began to decline; however, there was no detectable reduction in gs in Arbutus. Predicted Kleaf in the tropical species, based on laboratory-generated VC, decreased by 74% of maximum Kleaf in Tachigalia, but only 22-32% in Vochysia and Protium. The results presented here, from the previous work of the authors and from other published studies, were consistent with two different strategies regarding daily maintenance of Kleaf: (1) substantial loss and subsequent recovery or (2) a more conservative strategy of loss avoidance.

The blind men and the elephant: The impact of context and scale in evaluating conflicts between plant hydraulic safety and efficiency

Given the fundamental importance of xylem safety and efficiency for plant survival and fitness, it is not surprising that these are among the most commonly studied features of hydraulic architecture. However, much remains to be learned about the nature and universality of conflicts between hydraulic safety and efficiency. Although selection for suites of hydraulic traits that confer adequate plant fitness under given conditions is likely to occur at the organismal level, most studies of hydraulic architecture have been confined to scales smaller than the whole plant, such as small-diameter branches and roots. Here we discuss the impact of the spatial and temporal contexts in which hydraulic traits are studied on the interpretation of their role in maintaining plant hydraulic function. We argue that further advances in understanding the ecological implications of different suites of plant hydraulic traits will be enhanced by adopting an integrated approach that considers variation in hydraulic traits throughout the entire plant, dynamic behavior of water transport, xylem tension and water transport efficiency in intact plants, alternate mechanisms that modulate hydraulic safety and efficiency, and alternate measures of hydraulic safety and safety margins.

Hydraulic patterns and safety margins, from stem to stomata, in three eastern US tree species

Adequate water transport is necessary to prevent stomatal closure and allow for photosynthesis. Dysfunction in the water transport pathway can result in stomatal closure, and can be deleterious to overall plant health and survival. Although much is known about small branch hydraulics, little is known about the coordination of leaf and stem hydraulic function. Additionally, the daily variations in leaf hydraulic conductance (K(leaf)), stomatal conductance and water potential (Ψ(L)) have only been measured for a few species. The objective of the current study was to characterize stem and leaf vulnerability to hydraulic dysfunction for three eastern U.S. tree species (Acer rubrum, Liriodendron tulipifera and Pinus virginiana) and to measure in situ daily patterns of K(leaf), leaf and stem Ψ, and stomatal conductance in the field. Sap flow measurements were made on two of the three species to compare patterns of whole-plant water use with changes in K(leaf) and stomatal conductance. Overall, stems were more resistant to hydraulic dysfunction than leaves. Stem P50 (Ψ resulting in 50% loss in conductivity) ranged from -3.0 to -4.2 MPa, whereas leaf P50 ranged from -0.8 to -1.7 MPa. Field Ψ(L) declined over the course of the day, but only P. virginiana experienced reductions in K(leaf) (nearly 100% loss). Stomatal conductance was greatest overall in P. virginiana, but peaked midmorning and then declined in all three species. Midday stem Ψ in all three species remained well above the threshold for embolism formation. The daily course of sap flux in P. virginiana was bell-shaped, whereas in A. rubrum sap flux peaked early in the morning and then declined over the remainder of the day. An analysis of our data and data for 39 other species suggest that there may be at least three distinct trajectories of relationships between maximum K(leaf) and the % K(leaf) at Ψ(min). In one group of species, a trade-off between maximum K(leaf) and % K(leaf) at Ψ(min) appeared to exist, but no trade-off was evident in the other two trajectories.

Leaf xylem embolism, detected acoustically and by cryo‐SEM, corresponds to decreases in leaf hydraulic conductance in four evergreen species

Hydraulic conductance of leaves (K(leaf)) typically decreases with increasing water stress. However, the extent to which the decrease in K(leaf) is due to xylem cavitation, conduit deformation or changes in the extra-xylary pathway is unclear. We measured K(leaf) concurrently with ultrasonic acoustic emission (UAE) in dehydrating leaves of two vessel-bearing and two tracheid-bearing species to determine whether declining K(leaf) was associated with an accumulation of cavitation events. In addition, images of leaf internal structure were captured using cryo-scanning electron microscopy, which allowed detection of empty versus full and also deformed conduits. Overall, K(leaf) decreased as leaf water potentials (Psi(L)) became more negative. Values of K(leaf) corresponding to bulk leaf turgor loss points ranged from 13 to 45% of their maximum. Additionally, Psi(L) corresponding to a 50% loss in conductivity and 50% accumulated UAE ranged from -1.5 to -2.4 MPa and from -1.1 to -2.8 MPa, respectively, across species. Decreases in K(leaf) were closely associated with accumulated UAE and the percentage of empty conduits. The mean amplitude of UAEs was tightly correlated with mean conduit diameter (R(2) = 0.94, P = 0.018). These results suggest that water stress-induced decreases in K(leaf) in these species are directly related to xylem embolism.

Water stress, shoot growth and storage of non-structural carbohydrates along a tree height gradient in a tall conifer.

We analysed concentrations of starch, sucrose, glucose and fructose in upper branch wood, foliage and trunk sapwood of Douglas-fir trees in height classes ranging from ~2 to ~57 m. Mean concentrations of non-structural carbohydrates (NSC) for all tissues were highest in the tallest height class and lowest in the lowest height class, and height-related trends in NSC were most pronounced in branches. Throughout a 17-month sampling period, mean values of branch NSC from the 57 m trees ranged between 30 and 377% greater than the 2 m trees. Branch NSC was inversely correlated with midday shoot water potential (Ψ(l)), shoot osmotic potential at full turgor (Ψ) and shoot extension. Temporal fluctuation in branch NSC was inversely correlated with height, and positively correlated with midday Ψ(l) , Ψ and shoot extension. The positive correlation between height and storage of NSC, and the negative correlation between NSC storage and shoot extension provide evidence that size-related growth decline in trees is not strongly associated with constraints on photosynthesis. The negative correlation between height and fluctuation in NSC suggests that mobilization of photosynthate in taller trees is constrained by some factor such as reductions in turgor-driven cell expansion or constraints on phloem transport.

Non-structural carbohydrates in woody plants compared among laboratories

Non-structural carbohydrates (NSC) in plant tissue are frequently quantified to make inferences about plant responses to environmental conditions. Laboratories publishing estimates of NSC of woody plants use many different methods to evaluate NSC. We asked whether NSC estimates in the recent literature could be quantitatively compared among studies. We also asked whether any differences among laboratories were related to the extraction and quantification methods used to determine starch and sugar concentrations. These questions were addressed by sending sub-samples collected from five woody plant tissues, which varied in NSC content and chemical composition, to 29 laboratories. Each laboratory analyzed the samples with their laboratory-specific protocols, based on recent publications, to determine concentrations of soluble sugars, starch and their sum, total NSC. Laboratory estimates differed substantially for all samples. For example, estimates for Eucalyptus globulus leaves (EGL) varied from 23 to 116 (mean = 56) mg g(-1) for soluble sugars, 6-533 (mean = 94) mg g(-1) for starch and 53-649 (mean = 153) mg g(-1) for total NSC. Mixed model analysis of variance showed that much of the variability among laboratories was unrelated to the categories we used for extraction and quantification methods (method category R(2) = 0.05-0.12 for soluble sugars, 0.10-0.33 for starch and 0.01-0.09 for total NSC). For EGL, the difference between the highest and lowest least squares means for categories in the mixed model analysis was 33 mg g(-1) for total NSC, compared with the range of laboratory estimates of 596 mg g(-1). Laboratories were reasonably consistent in their ranks of estimates among tissues for starch (r = 0.41-0.91), but less so for total NSC (r = 0.45-0.84) and soluble sugars (r = 0.11-0.83). Our results show that NSC estimates for woody plant tissues cannot be compared among laboratories. The relative changes in NSC between treatments measured within a laboratory may be comparable within and between laboratories, especially for starch. To obtain comparable NSC estimates, we suggest that users can either adopt the reference method given in this publication, or report estimates for a portion of samples using the reference method, and report estimates for a standard reference material. Researchers interested in NSC estimates should work to identify and adopt standard methods.

Above- and belowground controls on water use by trees of different wood types in an eastern US deciduous forest

Stomata control tree transpiration by sensing and integrating environmental signals originating in the atmosphere and soil, and co-occurring species may differ in inherent stomatal sensitivity to these above- and belowground signals and in the types of signals to which they respond. Stomatal responsiveness to environmental signals is likely to differ across species having different types of wood (e.g., ring-porous, diffuse-porous and coniferous) because each wood type differs in the structure, size and spatial distribution of its xylem conduits as well as in the scaling of hydraulic properties with stem diameter. The objective of this study was to evaluate the impact of variation in soil water availability and atmospheric evaporative demand on stomatal regulation of transpiration in seven co-occurring temperate deciduous forest species representing three wood types. We measured whole-tree sap flux and soil and atmospheric variables in a mixed deciduous forest in central Pennsylvania over the course of a growing season characterized by severe drought and large fluctuations in atmospheric vapor pressure deficit (D). The relative sensitivity of sap flux to soil drying was ∼2.2-2.3 times greater in the diffuse-porous and coniferous species than in the ring-porous species. Stomata of the ring-porous oaks were only about half as responsive to increased D as those of trees of the other two wood types. These differences in responsiveness to changes in the below- and aboveground environment implied that regulation of leaf water potential in the ring-porous oaks was less stringent than that in the diffuse-porous angiosperms or the conifers. The results suggest that increases in the frequency or intensity of summer droughts in the study region could have multiple consequences for forest function, including altered successional time courses or climax species composition and cumulative effects on whole-tree architecture, resulting in a structural and physiological legacy that would restrict the ability of trees to respond rapidly to more favorable growth conditions.

The dynamic pipeline: hydraulic capacitance and xylem hydraulic safety in four tall conifer species

Recent work has suggested that plants differ in their relative reliance on structural avoidance of embolism versus maintenance of the xylem water column through dynamic traits such as capacitance, but we still know little about how and why species differ along this continuum. It is even less clear how or if different parts of a plant vary along this spectrum. Here we examined how traits such as hydraulic conductivity or conductance, xylem vulnerability curves, and capacitance differ in trunks, large- and small-diameter branches, and foliated shoots of four species of co-occurring conifers. We found striking similarities among species in most traits, but large differences among plant parts. Vulnerability to embolism was high in shoots, low in small- and large-diameter branches, and high again in the trunks. Safety margins, defined as the pressure causing 50% loss of hydraulic conductivity or conductance minus the midday water potential, were large in small-diameter branches, small in trunks and negative in shoots. Sapwood capacitance increased with stem diameter, and was correlated with stem vulnerability, wood density and latewood proportion. Capacitive release of water is a dynamic aspect of plant hydraulics that is integral to maintenance of long-distance water transport.