Guillermo Goldstein

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.

Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species

Abstract Growth, biomass allocation, and photosynthetic characteristics of seedlings of five invasive non-indigenous and four native species grown under different light regimes were studied to help explain the success of invasive species in Hawaiian rainforests. Plants were grown under three greenhouse light levels representative of those found in the center and edge of gaps and in the understory of Hawaiian rainforests, and under an additional treatment with unaltered shade. Relative growth rates (RGRs) of invasive species grown in sun and partial shade were significantly higher than those for native species, averaging 0.25 and 0.17 g g−1 week−1, respectively, while native species averaged only 0.09 and 0.06 g g−1 week−1, respectively. The RGR of invasive species under the shade treatment was 40% higher than that of native species. Leaf area ratios (LARs) of sun and partial-shade-grown invasive and native species were similar but the LAR of invasive species in the shade was, on average, 20% higher than that of native species. There were no differences between invasive and native species in biomass allocation to shoots and roots, or in leaf mass per area across light environments. Light-saturated photosynthetic rates (Pmax) were higher for invasive species than for native species in all light treatments. Pmax of invasive species grown in the sun treatment, for example, ranged from 5.5 to 11.9 μmol m−2 s−1 as compared with 3.0−4.5 μmol m−2 s−1 for native species grown under similar light conditions. The slope of the linear relationship between Pmax and dark respiration was steeper for invasive than for native species, indicating that invasive species assimilate more CO2 at a lower respiratory cost than native species. These results suggest that the invasive species may have higher growth rates than the native species as a consequence of higher photosynthetic capacities under sun and partial shade, lower dark respiration under all light treatments, and higher LARs when growing under shade conditions. Overall, invasive species appear to be better suited than native species to capturing and utilizing light resources, particularly in high-light environments such as those characterized by relatively high levels of disturbance.

Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawaii.

Abstract The effects of biological invasions are most evident in isolated oceanic islands such as the Hawaiian Archipelago, where invasive plant species are rapidly changing the composition and function of plant communities. In this study, we compared the specific leaf area (SLA), leaf tissue construction cost (CC), leaf nutrient concentration, and net CO2 assimilation (A) of 83 populations of 34 native and 30 invasive species spanning elevation and substrate age gradients on Mauna Loa volcano in the island of Hawaii. In this complex environmental matrix, where annual precipitation is higher than 1500 mm, we predicted that invasive species, as a group, will have leaf traits, such as higher SLA and A and lower leaf CC, which may result in more efficient capture of limiting resources (use more resources at a lower carbon cost) than native species. Overall, invasive species had higher SLA and A, and lower CC than native species, consistent with our prediction. SLA and foliar N and P were 22.5%, 30.5%, and 37.5% higher, respectively, in invasive species compared to native ones. Light-saturated photosynthesis was higher for invasive species (9.59 μmol m−2 s−1) than for native species (7.31 μmol m−2 s−1), and the difference was larger when A was expressed on a mass basis. Leaf construction costs, on the other hand, were lower for the invasive species (1.33 equivalents of glucose g−1) than for native species (1.37). This difference was larger when CC was expressed on an area basis. The trends in the above traits were maintained when groups of ecologically equivalent native and invasive species (i.e., sharing similar life history traits and growing in the same habitat) were compared. Foliar N and P were significantly higher in invasive species across all growth forms. Higher N may partially explain the higher A of invasive species. Despite relatively high N, the photosynthetic nitrogen use efficiency of invasive species was 15% higher than that of native species. These results suggest that invasive species may not only use resources more efficiently than native species, but may potentially demonstrate higher growth rates, consistent with their rapid spread in isolated oceanic islands.

Physiological and morphological variation in Metrosideros polymorpha, a dominant Hawaiian tree species, along an altitudinal gradient: the role of phenotypic plasticity

Metrosideros polymorpha, a dominant tree species in Hawaiian ecosystems, occupies a wide range of habitats. Complementary field and common-garden studies of M. polymorpha populations were conducted across an altitudinal gradient at two different substrate ages to ascertain if the large phenotypic variation of this species is determined by genetic differences or by phenotypic modifications resulting from environmental conditions. Several characteristics, including ecophysiological behavior and anatomical features, were largely induced by the environment. However, other characteristics, particularly leaf morphology, appeared to be mainly determined by genetic background. Common garden plants exhibited higher average rates of net assimilation (5.8 μmol CO2 m−2 s−1) and higher average stomatal conductance (0.18 mol H2O m−2 s−1) than their field counterparts (3.0 μmol CO2 m−2 s−1, and 0.13 mol H2O m−2 s−1 respectively). Foliar δ13C of most common-garden plants was similar among sites of origin with an average value of −26.9‰. In contrast, mean values of foliar δ13C in field plants increased substantially from −29.5‰ at low elevation to −24.8‰ at high elevation. Leaf mass per unit area increased significantly as a function of elevation in both field and common garden plants; however, the range of values was much narrower in common garden plants (211–308 g m−2 for common garden versus 107–407 g m−2 for field plants). Nitrogen content measured on a leaf area basis in common garden plants ranged from 1.4 g m−2 to 2.4 g m−2 and from 0.8 g m−2 to 2.5 g m−2 in field plants. Photosynthetic nitrogen use efficiency (PNUE) decreased 50% with increasing elevation in field plants and only 20% in plants from young substrates in the common garden. This was a result of higher rates of net CO2 assimilation in the common garden plants. Leaf tissue and cell layer thickness, and degree of leaf pubescence increased significantly with elevation in field plants, whereas in common garden plants, variation with elevation of origin was much narrower, or was entirely absent. Morphological characteristics such as leaf size, petiole length, and internode length decreased with increasing elevation in the field and were retained when grown in the common garden, suggesting a potential genetic basis for these traits. The combination of environmentally induced variability in physiological and anatomical characteristics and genetically determined variation in morphological traits allows Hawaiian M. polymorpha to attain and dominate an extremely wide ecological distribution not observed in other tree species.

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.

Environmental and physiological regulation of transpiration in tropical forest gap species: the influence of boundary layer and hydraulic properties

Environmental and physiological regulation of transpiration were examined in several gap-colonizing shrub and tree species during two consecutive dry seasons in a moist, lowland tropical forest on Barro Colorado Island, Panama. Whole plant transpiration, stomatal and total vapor phase (stomatal + boundary layer) conductance, plant water potential and environmental variables were measured concurrently. This allowed control of transpiration (E) to be partitioned quantitatively between stomatal (gs) and boundary layer (gb) conductance and permitted the impact of invividual environmental and physiological variables on stomatal behavior and E to be assessed. Wind speed in treefall gap sites was often below the 0.25 m s−1 stalling speed of the anemometer used and was rarely above 0.5 m s−1, resulting in uniformly low gb (c. 200–300 mmol m−2 s−1) among all species studied regardless of leaf size. Stomatal conductance was typically equal to or somewhat greater than gb. This strongly decoupled E from control by stomata, so that in Miconia argentea a 10% change in gs when gs was near its mean value was predicted to yield only a 2.5% change in E. Porometric estimates of E, obtained as the product of gs and the leaf-bulk air vapor pressure difference (VPD) without taking gb into account, were up to 300% higher than actual E determined from sap flow measurements. Porometry was thus inadequate as a means of assessing the physiological consequences of stomatal behavior in different gap colonizing species. Stomatal responses to humidity strongly limited the increase in E with increasing evaporative demand. Stomata of all species studied appeared to respond to increasing evaporative demand in the same manner when the leaf surface was selected as the reference point for determination of external vapor pressure and when simultaneous variation of light and leaf-air VPD was taken into account. This result suggests that contrasting stomatal responses to similar leaf-bulk air VPD may be governed as much by the external boundary layer as by intrinsic physiological differences among species. Both E and gs initially increased sharply with increasing leaf area-specific total hydraulic conductance of the soil/root/leaf pathway (Gt), becoming asymptotic at higher values of Gt. For both E and gs a unique relationship appeared to describe the response of all species to variations in Gt. The relatively weak correlation observed between gs and midday leaf water potential suggested that stomatal adjustment to variations in water availability coordinated E with water transport efficiency rather than bulk leaf water status.

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.

Leaf functional traits of Neotropical savanna trees in relation to seasonal water deficit

The seasonal savannas (cerrados) of Central Brazil are characterized by a large diversity of evergreen and deciduous trees, which do not show a clear differentiation in terms of active rooting depth. Irrespective of the depth of the root system, expansion of new foliage in deciduous species occurs at the end of the dry season. In this study, we examined a suite of leaf traits related to C assimilation, water and nutrients (N, P) in five deciduous and six evergreen trees that were among the dominant families of cerrado vegetation. Maximum CO2 assimilation on a mass basis (Amass) was significantly correlated with leaf N and P, and specific leaf area (SLA; leaf area per unit of leaf mass). The highest leaf concentrations of both nutrients were measured in the newly mature leaves of deciduous species at the end of the dry period. The differences in terms of leaf N and P between evergreen and deciduous species decreased during the wet season. Deciduous species also invested less in the production of non-photosynthetic leaf tissues and produced leaves with higher SLA and maintained higher water use efficiency. Thus, deciduous species compensated for their shorter leaf payback period by maintaining higher potential payback capacity (higher values of Amass) and lower leaf construction costs (higher SLA). Their short leafless period and the capacity to flush by the end of the dry season may also contribute to offset the longer payback period of evergreen species, although it may involve the higher cost of maintaining a deep-root system or a tight control of plant water balance in the shallow-rooted ones.

Partitioning of water resources among plants of a lowland tropical forest

Source water used by plants of several species in a semi-evergreen lowland tropical forest on Barro Colorado Island, Panama, was assessed by comparing the relative abundance of deuterium, D, versus hydrogen, H (stable hydrogen isotope composition, δD) in xylem sap and in soil water at different depths, during the dry season of 1992. Ecological correlates of source water were examined by comparing xylem water δD values with leaf phenology, leaf water status determined with a pressure chamber, and rates of water use determined as mass flow of sap using the stem heat balance method. Soil water δD values decreased sharply to 30 cm, then remained relatively constant with increasing depth. Average δD values were-13‰, for 0–30 cm depth and-36.7‰ for 30–100 cm depth. Soil water δD values were negatively associated with soil water content and soil water potential. Concurrent analyses of xylem water revealed a high degree of partitioning of water resources among species of this tropical forest. Xylem water δD of deciduous trees (average=-25.3±1.4‰) was higher than that of evergreen trees (average=-36.3±3.5‰), indicating that evergreen species had access to the more abundant soil water at greater depth than deciduous species. In evergreen shade-tolerant and high-light requiring shrubs and small trees, δD of xylem water was negatively correlated with transpiration rate and leaf water potential indicating that species using deeper, more abundant water resources had both higher rates of water use and more favorable leaf water status.