Daniel M. Johnson

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 altitude of alpine treeline: a bellwether of climate change effects.

Because of the characteristically low temperatures and ambient CO2 concentrations associated with greater altitudes, mountain forests may be particularly sensitive to global warming and increased atmospheric CO2. Moreover, the upper treeline is probably the most stressful location within these forests, possibly providing an early bellwether of forest response. Most treeline studies of the past century, as well as recently, have correlated temperatures with the altitudinal limits observed for treelines. In contrast, investigations on pre-establishment seedlings, the most vulnerable life stage of most tree species, are rare. There appears to be specific microclimatic factors dictated by wind and sky exposure that limit seedling survival, and also generate the distorted tree forms commonly observed at treeline. Seedling survival appears critical for creating the biological facilitation of microclimate at the community level which is necessary for the growth of seedlings to normal tree stature, forming new subalpine forest at a higher altitude.AbstractEs posible que—a causa de características que están asociadas con altitudes más altas: las bajas temperaturas y las concentraciones ambientales de dióxido de carbono—los bosques en las montañas están extra sensibles al calentamiento global y el aumento de dióxido de carbono en la atmósfera. El borde superior del bosque es probablemente el lugar con la más estrés y proviene uno de los primeros avisos de cómo reaccionará el bosque entero. En el pasado y hoy en día, la mayoría de los estudios del borde del bosque ha conectado la temperatura con los límites de la altitud. En contraste, investigaciones de árboles infantiles son raras, y la infancia de los árboles es el período de vida más vulnerable. Aparece que hay factores micro-climáticos dictados por la exposición del viento y cielo que limitan la sobrevivencia de los árboles infantiles, y que generan árboles deformados observados al borde del bosque. Es más, la sobrevivencia de árboles infantiles es crítica para crear la facilitación biológica del micro-clima en una comunidad arbolada. Esta facilitación es necesaria para el crecimiento de árboles infantiles a árboles maduros, los que forman un nuevo bosque subalpino en una altitud más alta.

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.

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.

Coordination of leaf structure and gas exchange along a height gradient in a tall conifer

The gravitational component of water potential and frictional resistance during transpiration lead to substantial reductions in leaf water potential (Psi(l)) near the tops of tall trees, which can influence both leaf growth and physiology. We examined the relationships between morphological features and gas exchange in foliage collected near the tops of Douglas-fir (Pseudotsuga menziesii (Mirb.) Franco) trees of different height classes ranging from 5 to 55 m. This sampling allowed us to investigate the effects of tree height on leaf structural characteristics in the absence of potentially confounding factors such as irradiance, temperature, relative humidity and branch length. The use of cut foliage for measurement of intrinsic gas-exchange characteristics allowed identification of height-related trends without the immediate influences of path length and gravity. Stomatal density, needle length, needle width and needle area declined with increasing tree height by 0.70 mm(-2) m(-1), 0.20 mm m(-1), 5.9 x 10(-3) mm m(-1) and 0.012 mm(2) m(-1), respectively. Needle thickness and mesophyll thickness increased with tree height by 4.8 x 10(-2) mm m(-1) and 0.74 microm m(-1), respectively. Mesophyll conductance (g(m)) and CO(2) assimilation in ambient [CO(2)] (A(amb)) decreased by 1.1 mmol m(-2) s(-1) per m and 0.082 micromol m(-2) s(-1) per m increase in height, respectively. Mean reductions in g(m) and A(amb) of foliage from 5 to 55 m were 47% and 42%, respectively. The observed trend in A(amb) was associated with g(m) and several leaf anatomic characteristics that are likely to be determined by the prevailing vertical tension gradient during foliar development. A linear increase in foliar delta(13)C values with height (0.042 per thousand m(-1)) implied that relative stomatal and mesophyll limitations of photosynthesis in intact shoots increased with height. These data suggest that increasing height leads to both fixed structural constraints on leaf gas exchange and dynamic constraints related to prevailing stomatal behavior.

Does homeostasis or disturbance of homeostasis in minimum leaf water potential explain the isohydric versus anisohydric behavior of Vitis vinifera L. cultivars

Due to the diurnal and seasonal fluctuations in leaf-to-air vapor pressure deficit (D), one of the key regulatory roles played by stomata is to limit transpiration-induced leaf water deficit. Different types of plants are known to vary in the sensitivity of stomatal conductance (gs) to D with important consequences for their survival and growth. Plants that minimize any increase in transpiration with increasing D have a tight stomatal regulation of a constant minimum leaf water potential (Ψleaf); these plants are termed as ‘isohydric’ (Stocker 1956). Plants that have less control of Ψleaf have been termed as ‘anisohydric’ (Tardieu and Simonneau 1998). Isohydric plants maintain a constant Ψleaf by reducing gs and transpiration under drought stress. Therefore, as drought pushes soil water potential (Ψsoil) below this Ψleaf set point, the plant can no longer extract water for gas exchange. Anisohydric plants allow Ψleaf to decrease with rising D, reaching a much lower Ψleaf in droughted plants relative to well-watered plants (Tardieu and Simonneau 1998), so this strategy produces a gradient between Ψsoil and Ψleaf that allows gas exchange to continue over a greater decline in Ψsoil. Thus, anisohydric plants sustain longer periods of transpiration and photosynthesis, even under large soil water deficit, and are thought to be more drought tolerant than isohydric species (McDowell 2011). In practice, the distinctions between isohydric and anisohydric strategies are often not clear (Franks et al. 2007), even among different cultivars of the same species. For example, cultivars of poplar (Hinckley et al. 1994) and grapevine (Schultz 2003, Lovisolo et al. 2010) have been shown to exhibit both contrasting hydraulic behaviors. A third mode of behavior was also suggested by Franks et al. (2007), in which the difference between soil and midday water potential (Ψsoil − Ψleaf) is maintained seasonally constant but Ψleaf fluctuates in synchrony with soil water availability (isohydrodynamic behavior). The lack of a clear distinction between these two strategies and the complex and variable responses of stomata to D under high and low soil moisture is depicted in two papers in this issue (Rogiers et al. 2012 and Zhang et al. 2012), showing that even typically anisohydric grape (Vitis vinifera L.) cultivars (Semillon and Merlot, respectively) may constrain gs during periods of extremely low Ψsoil. The same individuals can switch from an isohydric-like behavior when transpiration is low to an anisohydric-like behavior with increasing water demand. Interestingly, both studies indicated that classifying species as either isohydric or anisohydric is a simplistic view of stomatal functioning and does not represent well the complex stomatal behavior under drying soil, and Zhang et al. (2012) also reported an isohydrodynamic behavior. Both studies suggested that when soil water is limited, gs is aimed at protecting the integrity of the hydraulic system, whereas as soil water content increases, stomata regulate transpiration less. The results of Zhang et al. (2012) indicated that under limited soil moisture the decrease in gs with increasing D was proportional to reference gs (gs at D = 1 kPa); which is in agreement with the stomata-sensitivity model developed by Oren et al. (1999) for isohydric species (see xeric line in Figure 1A). However, a significant departure from this theoretical model was observed under high soil moisture (see wet and mesic lines in Figure 1B). Similarly, in this issue Rogiers et al. (2012) showed that under Tree Physiology 32, 245–248 doi:10.1093/treephys/tps013

Evidence for xylem embolism as a primary factor in dehydration-induced declines in leaf hydraulic conductance

Hydraulic conductance of leaves (K(leaf)) typically decreases with increasing water stress and recent studies have proposed different mechanisms responsible for decreasing K(leaf) . We measured K(leaf) concurrently with ultrasonic acoustic emissions (UAEs) in dehydrating leaves of several species to determine whether declining K(leaf) was associated with xylem embolism. In addition, we performed experiments in which the surface tension of water in the leaf xylem was reduced by using a surfactant solution. Finally, we compared the hydraulic vulnerability of entire leaves with the leaf lamina in three species. Leaf hydraulic vulnerability based on rehydration kinetics and UAE was very similar, except in Quercus garryana. However, water potentials corresponding to the initial decline in K(leaf) and the onset of UAE in Q. garryana were similar. In all species tested, reducing the surface tension of water caused K(leaf) to decline at less negative water potentials compared with leaves supplied with water. Microscopy revealed that as the fraction of embolized xylem increased, K(leaf) declined sharply in Q. garryana. Measurements on leaf discs revealed that reductions in lamina hydraulic conductance with dehydration were not as great as those observed in intact leaves, suggesting that embolism was the primary mechanism for reductions in K(leaf) during dehydration.

Low clouds and cloud immersion enhance photosynthesis in understory species of a southern Appalachian spruce–fir forest (USA)

High-altitude forests of the southern Appalachian Mountains (USA) are frequently immersed in clouds, as are many mountain forests. They may be particularly sensitive to predicted increases in cloud base altitude with global warming. However, few studies have addressed the impacts of immersion on incident sunlight and photosynthesis. Understory sunlight (photosynthetically active radiation, PAR) was measured during clear, low cloud, and cloud-immersed conditions at Mount Mitchell and Roan Mountain, NC (USA) along with accompanying photosynthesis in four representative understory species. Understory PAR was substantially less variable on immersed vs. clear days. Photosynthesis became light-saturated between ∼100 and 400 μmol · m(-2) · s(-1) PAR for all species measured, corresponding closely to the sunlight environment measured during immersion. Estimated daily carbon gain was 26% greater on clear days at a more open canopy site but was 22% greater on immersed/cloudy days at a more closed canopy site. F(v)/F(m) (maximum photosystem II efficiency) in Abies fraseri seedlings exposed to 2.5 min full sunlight was significantly reduced (10%), indicating potential reductions in photosynthesis on clear days. In addition, photosynthesis in microsites with canopy cover was nearly 3-fold greater under immersed (2.6 mmol · m(-2) · h(-1)) vs. clear conditions (0.9 mmol · m(-2) · h(-1)). Thus, cloud immersion provided more constant PAR regimes that enhanced photosynthesis, especially in shaded microsites. Future studies are needed to predict the survival of these refugial forests under potential changes in cloud regimes.

Leaf architecture and direction of incident light influence mesophyll fluorescence profiles.

Light propagation and distribution inside leaves have been recognized as important processes influencing photosynthesis. Monochromatic light absorption across the mesophyll was measured using chlorophyll fluorescence generated from illumination of the cut edge (epi-illumination), as well as the adaxial or abaxial surfaces of the leaf. Species were selected that had basic leaf types: laminar leaf with adaxial palisade layer (Rhododendron catawbiense), needle with palisade (Abies fraseri), and needle without palisade (Picea rubens). Fluorescence was more evenly distributed across the mesophyll for adaxially illuminated leaves with a palisade cell layer, as well as for the needles (cylindrical) without palisade, when compared to fluorescence generated by abaxial illumination. Moreover, fluorescence from green light illumination remained high across the mesophyll of adaxially illuminated R. catawbiense, indicating a possible influence of mesophyll structure on internal light distribution beyond that of chlorophyll levels. These data support the idea that light propagation within the mesophyll is associated with asymmetric mesophyll structure, in particular the presence of palisade cell layers. In addition, we propose that the evolution of a more cylindrical leaf form, such as found in conifer species, may be a structural solution to excessive sunlight that replaces the highly differentiated mesophyll found in most laminar-leaved species.

An annual pattern of native embolism in upper branches of four tall conifer species

PREMISE OF THE STUDY The Pacific Northwest of North America experiences relatively mild winters and dry summers. For the tall coniferous trees that grow in this region, we predicted that loss in the hydraulic conductivity of uppermost branches would be avoided because of difficulty reversing accumulated emboli in xylem that is always under negative pressure. METHODS To test this hypothesis, we measured native percent loss in hydraulic conductivity (PLC; the decrease of in situ hydraulic conductivity relative to the maximum) monthly throughout 2009 in branches at the tops (∼50 m) of four species in an old growth forest in southern Washington. KEY RESULTS Contrary to our prediction, freeze-thaw cycles resulted in considerable native PLC. Branches showed hydraulic recovery in the spring and after a moderate increase in native embolism that was observed after an unusually hot period in August. The September recovery occurred despite decreases in the leaf and stem water potentials compared to August values. CONCLUSIONS Recoveries in branches of these trees could not have occurred by raising the water potential enough to dissolve bubbles simply by transporting water from roots and must have occurred either through water absorption through needles and/or refilling under negative pressure. Excluding the August value, native embolism values correlated strongly with air temperature of the preceding 10 d. For three species, we found that branches with lower wood density had higher specific conductivity, but not greater native PLC than branches with higher wood density, which calls into question whether there is any hydraulic benefit to higher wood density in small branches in those species.