Frederick C. Meinzer

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.

Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees.

We investigated how water transport capacity, wood density and wood anatomy were related to leaf photosynthetic traits in two lowland forests in Panama. Leaf-specific hydraulic conductivity (kL) of upper branches was positively correlated with maximum rates of net CO2 assimilation per unit leaf area (Aarea) and stomatal conductance (gs) across 20 species of canopy trees. Maximum kL showed stronger correlation with Aarea than initial kL suggesting that allocation to photosynthetic potential is proportional to maximum water transport capacity. Terminal branch kL was negatively correlated with Aarea/gs and positively correlated with photosynthesis per unit N, indicating a trade-off of efficient use of water against efficient use of N in photosynthesis as water transport efficiency varied. Specific hydraulic conductivity calculated from xylem anatomical characteristics (ktheoretical) was positively related to Aarea and kL, consistent with relationships among physiological measurements. Branch wood density was negatively correlated with wood water storage at saturation, kL, Aarea, net CO2 assimilation per unit leaf mass (Amass), and minimum leaf water potential measured on covered leaves, suggesting that wood density constrains physiological function to specific operating ranges. Kinetic and static indices of branch water transport capacity thus exhibit considerable co-ordination with allocation to potential carbon gain. Our results indicate that understanding tree hydraulic architecture provides added insights to comparisons of leaf level measurements among species, and links photosynthetic allocation patterns with branch hydraulic processes.

Functional convergence in plant responses to the environment.

Abstract. Much comparative ecophysiological research has focused on contrasting species-specific behavior or ecological strategies with regard to regulation of basic physiological processes such as transpiration, photosynthesis and growth, leading to an emphasis on divergence rather than convergence in plant functioning. This review highlights selected examples in which substantial functional convergence among taxonomically, phylogenetically and architecturally diverse species has been revealed by applying appropriate scaling factors and identifying universal constraints or trade-offs. Recent empirical and theoretical scaling models emphasize the strong role that plant size, architecture, allometry and chemistry play in constraining functional traits related to water and carbon economy and growth. Taken together, the findings summarized here strongly suggest that there are a limited number of physiological solutions to a given problem of plant adaptation to the environment. Comparative ecophysiological studies will therefore benefit from consideration of the constraints that plant anatomical, structural and chemical attributes place on physiological functioning.

Partitioning of soil water among canopy trees in a seasonally dry tropical forest

Abstract Little is known about partitioning of soil water resources in species-rich, seasonally dry tropical forests. We assessed spatial and temporal patterns of soil water utilization in several canopy tree species on Barro Colorado Island, Panama, during the 1997 dry season. Stable hydrogen isotope composition (δD) of xylem and soil water, soil volumetric water content (θv), and sap flow were measured concurrently. Evaporative fractionation near the soil surface caused soil water δD to decrease from about –15‰ at 0.1 m to –50 to –55‰ at 1.2 m depth. Groundwater sampled at the sources of nearby springs during this period yielded an average δD value of –60‰. θv increased sharply and nearly linearly with depth to 0.7 m, then increased more slowly between 0.7 and 1.05 m. Based on xylem δD values, water uptake in some individual plants appeared to be restricted largely to the upper 20 cm of the soil profile where θv dropped below 20% during the dry season. In contrast, other individuals appeared to have access to water at depths greater than 1 m where θv remained above 45% throughout the dry season. The depths of water sources for trees with intermediate xylem δD values were less certain because variation in soil water δD between 20 and 70 cm was relatively small. Xylem water δD was also strongly dependent on tree size (diameter at breast height), with smaller trees appearing to preferentially tap deeper sources of soil water than larger trees. This relationship appeared to be species independent. Trees able to exploit progressively deeper sources of soil water during the dry season, as indicated by increasingly negative xylem δD values, were also able to maintain constant or even increase rates of water use. Seasonal courses of water use and soil water partitioning were associated with leaf phenology. Species with the smallest seasonal variability in leaf fall were also able to tap increasingly deep sources of soil water as the dry season progressed. Comparison of xylem, soil, and groundwater δD values thus pointed to spatial and temporal partitioning of water resources among several tropical forest canopy tree species during the dry season.

Water transport in trees: current perspectives, new insights and some controversies

This review emphasizes recent developments and controversies related to the uptake, transport and loss of water by trees. Comparisons of the stable isotope composition of soil and xylem water have provided new and sometimes unexpected insights concerning spatial and temporal partitioning of soil water by roots. Passive, hydraulic redistribution of water from moister to drier portions of the soil profile via plant root systems may have a substantial impact on vertical profiles of soil water distribution, partitioning of water within and among species, and on ecosystem water balance. The recent development of a technique for direct measurement of pressure in individual xylem elements of intact, transpiring plants elicited a number of challenges to the century-old cohesion-tension theory. The ongoing debate over mechanisms of long-distance water transport has stimulated an intense interest in the phenomenon and mechanisms of embolism repair. Rather than embolism being essentially irreversible, it now appears that there is a dynamic balance between embolism formation and repair throughout the day and that daily release of water from the xylem via cavitation may serve to stabilize leaf water balance by minimizing the temporal imbalance between water supply and demand. Leaf physiology is closely linked to hydraulic architecture and hydraulic perturbations, but the precise nature of the signals to which stomata respond remains to be elucidated. When water transport in trees is studied at multiple scales from single leaves to the whole organism, considerable functional convergence in regulation of water use among phylogenetically diverse species is revealed.

Mechanisms contributing to seasonal homeostasis of minimum leaf water potential and predawn disequilibrium between soil and plant water potential in Neotropical savanna trees

Seasonal regulation of leaf water potential (ΨL) was studied in eight dominant woody savanna species growing in Brazilian savanna (Cerrado) sites that experience a 5-month dry season. Despite marked seasonal variation in precipitation and air saturation deficit (D), seasonal differences in midday minimum ΨL were small in all of the study species. Water use and water status were regulated by a combination of plant physiological and architectural traits. Despite a nearly 3-fold increase in mean D between the wet and dry season, a sharp decline in stomatal conductance with increasing D constrained seasonal variation in minimum ΨL by limiting transpiration per unit leaf area (E). The leaf surface area per unit of sapwood area (LA/SA), a plant architectural index of potential constraints on water supply in relation to transpirational demand, was about 1.5–8 times greater in the wet season compared to the dry season for most of the species. The changes in LA/SA from the wet to the dry season resulted from a reduction in total leaf surface area per plant, which maintained or increased total leaf-specific hydraulic conductance (Gt) during the dry season. The isohydric behavior of Cerrado tree species with respect to minimum ΨL throughout the year thus was the result of strong stomatal control of evaporative losses, a decrease in total leaf surface area per tree during the dry season, an increase in total leaf-specific hydraulic conductance, and a tight coordination between gas and liquid phase conductance. In contrast with the seasonal isohydric behavior of minimum ΨL, predawn ΨL in all species was substantially lower during the dry season compared to the wet season. During the dry season, predawn ΨL was more negative than bulk soil Ψ estimated by extrapolating plots of E versus ΨL to E=0. Predawn disequilibrium between plant and soil Ψ was attributable largely to nocturnal transpiration, which ranged from 15 to 22% of the daily total. High nocturnal water loss may also have prevented internal water storage compartments from being completely refilled at night before the onset of transpiration early in the day.

Antisense Down-Regulation of 4CL Expression Alters Lignification, Tree Growth, and Saccharification Potential of Field-Grown Poplar

Transgenic down-regulation of the Pt4CL1 gene family encoding 4-coumarate:coenzyme A ligase (4CL) has been reported as a means for reducing lignin content in cell walls and increasing overall growth rates, thereby improving feedstock quality for paper and bioethanol production. Using hybrid poplar (Populus tremula × Populus alba), we applied this strategy and examined field-grown transformants for both effects on wood biochemistry and tree productivity. The reductions in lignin contents obtained correlated well with 4CL RNA expression, with a sharp decrease in lignin amount being observed for RNA expression below approximately 50% of the nontransgenic control. Relatively small lignin reductions of approximately 10% were associated with reduced productivity, decreased wood syringyl/guaiacyl lignin monomer ratios, and a small increase in the level of incorporation of H-monomers (p-hydroxyphenyl) into cell walls. Transgenic events with less than approximately 50% 4CL RNA expression were characterized by patches of reddish-brown discolored wood that had approximately twice the extractive content of controls (largely complex polyphenolics). There was no evidence that substantially reduced lignin contents increased growth rates or saccharification potential. Our results suggest that the capacity for lignin reduction is limited; below a threshold, large changes in wood chemistry and plant metabolism were observed that adversely affected productivity and potential ethanol yield. They also underline the importance of field studies to obtain physiologically meaningful results and to support technology development with transgenic trees.

Regulation of water flux through trunks, branches, and leaves in trees of a lowland tropical forest

Abstract We studied regulation of whole-tree water use in individuals of five diverse canopy tree species growing in a Panamanian seasonal forest. A construction crane equipped with a gondola was used to access the upper crowns and points along the branches and trunks of the study trees for making concurrent measurements of sap flow at the whole-tree and branch levels, and vapor phase conductances and water status at the leaf level. These measurements were integrated to assess physiological regulation of water use from the whole-tree to the single-leaf scale. Whole-tree water use ranged from 379 kg day−1 in a 35 m-tall Anacardium excelsum tree to 46 kg day−1 in an 18 m-tall Cecropia longipes tree. The dependence of whole-tree and branch sap velocity and sap flow on sapwood area was essentially identical in the five trees studied. However, large differences in transpiration per unit leaf area (E) among individuals and among branches on the same individual were observed. These differences were substantially reduced when E was normalized by the corresponding branch leaf area:sapwood area ratio (LA/SA). Variation in stomatal conductance (gs) and crown conductance (gc), a total vapor phase conductance that includes stomatal and boundary layer components, was closely associated with variation in the leaf area-specific total hydraulic conductance of the soil/leaf pathway (Gt). Vapor phase conductance in all five trees responded similarly to variation in Gt. Large diurnal variations in Gt were associated with diurnal variation in exchange of water between the transpiration stream and internal stem storage compartments. Differences in stomatal regulation of transpiration on a leaf area basis appeared to be governed largely by tree size and hydraulic architectural features rather than physiological differences in the responsiveness of stomata. We suggest that reliance on measurements gathered at a single scale or inadequate range of scale may result in misleading conclusions concerning physiological differences in regulation of transpiration.

Stem and leaf hydraulics of congeneric tree species from adjacent tropical savanna and forest ecosystems.

Leaf and stem functional traits related to plant water relations were studied for six congeneric species pairs, each composed of one tree species typical of savanna habitats and another typical of adjacent forest habitats, to determine whether there were intrinsic differences in plant hydraulics between these two functional types. Only individuals growing in savanna habitats were studied. Most stem traits, including wood density, the xylem water potential at 50% loss of hydraulic conductivity, sapwood area specific conductivity, and leaf area specific conductivity did not differ significantly between savanna and forest species. However, maximum leaf hydraulic conductance (Kleaf) and leaf capacitance tended to be higher in savanna species. Predawn leaf water potential and leaf mass per area were also higher in savanna species in all congeneric pairs. Hydraulic vulnerability curves of stems and leaves indicated that leaves were more vulnerable to drought-induced cavitation than terminal branches regardless of genus. The midday Kleaf values estimated from leaf vulnerability curves were very low implying that daily embolism repair may occur in leaves. An electric circuit analog model predicted that, compared to forest species, savanna species took longer for their leaf water potentials to drop from predawn values to values corresponding to 50% loss of Kleaf or to the turgor loss points, suggesting that savanna species were more buffered from changes in leaf water potential. The results of this study suggest that the relative success of savanna over forest species in savanna is related in part to their ability to cope with drought, which is determined more by leaf than by stem hydraulic traits. Variation among genera accounted for a large proportion of the total variance in most traits, which indicates that, despite different selective pressures in savanna and forest habitats, phylogeny has a stronger effect than habitat in determining most hydraulic traits.

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.