Katherine A. McCulloh

Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure

Wood density (Dt), an excellent predictor of mechanical properties, is typically viewed in relation to support against gravity, wind, snow, and other environmental forces. In contrast, we show the surprising extent to which variation in Dt and wood structure is linked to support against implosion by negative pressure in the xylem pipeline. The more drought-tolerant the plant, the more negative the xylem pressure can become without cavitation, and the greater the internal load on the xylem conduit walls. Accordingly, Dt was correlated with cavitation resistance. This trend was consistent with the maintenance of a safety factor from implosion by negative pressure: conduit wall span (b) and thickness (t) scaled so that (t/b)2 was proportional to cavitation resistance as required to avoid wall collapse. Unexpectedly, trends in Dt may be as much or more related to support of the xylem pipeline as to support of the plant.

Water transport in plants obeys Murray's law

The optimal water transport system in plants should maximize hydraulic conductance (which is proportional to photosynthesis) for a given investment in transport tissue. To investigate how this optimum may be achieved, we have performed computer simulations of the hydraulic conductance of a branched transport system. Here we show that the optimum network is not achieved by the commonly assumed pipe model of plant form, or its antecedent, da Vincis rule. In these representations, the number and area of xylem conduits is constant at every branch rank. Instead, the optimum network has a minimum number of wide conduits at the base that feed an increasing number of narrower conduits distally. This follows from the application of Murrays law, which predicts the optimal taper of blood vessels in the cardiovascular system. Our measurements of plant xylem indicate that these conduits conform to the Murrays law optimum as long as they do not function additionally as supports for the plant body.

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.

Moving water well: comparing hydraulic efficiency in twigs and trunks of coniferous, ring‐porous, and diffuse‐porous saplings from temperate and tropical forests

*Coniferous, diffuse-porous and ring-porous trees vary in their xylem anatomy, but the functional consequences of these differences are not well understood from the scale of the conduit to the individual. *Hydraulic and anatomical measurements were made on branches and trunks from 16 species from temperate and tropical areas, representing all three wood types. Scaling of stem conductivity (K(h)) with stem diameter was used to model the hydraulic conductance of the stem network. *Ring-porous trees showed the steepest increase in K(h) with stem size. Temperate diffuse-porous trees were at the opposite extreme, and conifers and tropical diffuse-porous species were intermediate. Scaling of K(h) was influenced by differences in the allometry of conduit diameter (taper) and packing (number per wood area) with stem size. *The K(h) trends were mirrored by the modeled stem-network conductances. Ring-porous species had the greatest network conductance and this value increased isometrically with trunk basal area, indicating that conductance per unit sapwood was independent of tree size. Conductances were lowest and most size-dependent in conifers. The results indicate that differences in conduit taper and packing between functional types propagate to the network level and have an important influence on metabolic scaling concepts.

Testing the metabolic theory of ecology

The metabolic theory of ecology (MTE) predicts the effects of body size and temperature on metabolism through considerations of vascular distribution networks and biochemical kinetics. MTE has also been extended to characterise processes from cellular to global levels. MTE has generated both enthusiasm and controversy across a broad range of research areas. However, most efforts that claim to validate or invalidate MTE have focused on testing predictions. We argue that critical evaluation of MTE also requires strong tests of both its theoretical foundations and simplifying assumptions. To this end, we synthesise available information and find that MTEs original derivations require additional assumptions to obtain the full scope of attendant predictions. Moreover, although some of MTEs simplifying assumptions are well supported by data, others are inconsistent with empirical tests and even more remain untested. Further, although many predictions are empirically supported on average, work remains to explain the often large variability in data. We suggest that greater effort be focused on evaluating MTEs underlying theory and simplifying assumptions to help delineate the scope of MTE, generate new theory and shed light on fundamental aspects of biological form and function.

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.

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.