Thermal imagery of woodland tree canopies provides new insights into drought-induced tree mortality.

Our understanding of how water dynamics determines the probability of tree mortality during drought is incomplete. Here we help address this shortcoming by coupling approaches from the disciplines of ecophysiology, geophysics and remote sensing in a woodland ecosystem undergoing protracted drying. Water uptake and use strategies varied between the dominant canopy species of the ecosystem. At one extreme were species that tightly regulate their water status, which is broadly consistent with the definition of isohydry. The higher leaf temperatures revealed by thermal imagery of these isohydric species are likely a reflection of reduced latent cooling owing to a stringent control of transpiration rate. Where silty sediments occur in the root zone, this strategy may have the effect of limiting the water sources available to these species during prolonged drought because of an insufficient hydraulic gradient for water uptake. In contrast were species that allowed their water status to fluctuate, operating in a fashion more consistent with anisohydry. For these species, latent cooling owing to relatively high transpiration rates maintained leaf temperatures near, or below, the ambient air temperature. The resulting drawdown in leaf water potential between soil and leaves in these anisohydric species may generate a sufficient hydraulic gradient to enable water uptake from silty soil during seasonal or prolonged droughts. In this way the spatial distribution of fine textured soil could indicate areas where the isohydric hydraulic control strategy is disadvantageous during prolonged droughts or where annual soil water recharge has fallen below a critical threshold.

Two sides to every leaf: water and CO2 transport in hypostomatous and amphistomatous leaves.

Leaves with stomata on both upper and lower surfaces, termed amphistomatous, are relatively rare compared with hypostomatous leaves with stomata only on the lower surface. Amphistomaty occurs predominantly in fast-growing herbaceous annuals and in slow-growing perennial shrubs and trees. In this paper, we present the current understanding and hypotheses on the costs and benefits of amphistomaty related to water and CO2 transport in contrasting leaf morphologies. First, there is no evidence that amphistomatous species achieve higher stomatal densities on a projected leaf area basis than hypostomatous species, but two-sided gas exchange is less limited by boundary layer effects. Second, amphistomaty may provide a specific advantage in thick leaves by shortening the pathway for CO2 transport between the atmosphere and the chloroplasts. In thin leaves of fast-growing herbaceous annuals, in which both the adaxial and abaxial pathways are already short, amphistomaty enhances leaf-atmosphere gas-exchange capacity. Third, amphistomaty may help to optimise the leaf-interior water status for CO2 transport by reducing temperature gradients and so preventing the condensation of water that could limit CO2 diffusion. Fourth, a potential cost of amphistomaty is the need for additional investments in leaf water transport tissue to balance the water loss through the adaxial surface.

Apparent Overinvestment in Leaf Venation Relaxes Leaf Morphological Constraints on Photosynthesis in Arid Habitats.

Leaf veins supply the mesophyll with water that evaporates when stomata are open to allow CO2 uptake for photosynthesis. Theoretical analyses suggest that water is optimally distributed in the mesophyll when the lateral distance between veins (dx) is equal to the distance from these veins to the epidermis (dy), expressed as dx:dy ≈ 1. Although this theory is supported by observations of many derived angiosperms, we hypothesize that plants in arid environments may reduce dx:dy below unity owing to climate-specific functional adaptations of increased leaf thickness and increased vein density. To test our hypothesis, we assembled leaf hydraulic, morphological, and photosynthetic traits of 68 species from the Eucalyptus and Corymbia genera (termed eucalypts) along an aridity gradient in southwestern Australia. We inferred the potential gas-exchange advantage of reducing dx beyond dy using a model that links leaf morphology and hydraulics to photosynthesis. Our observations reveal that eucalypts in arid environments have thick amphistomatous leaves with high vein densities, resulting in dx:dy ratios that range from 1.6 to 0.15 along the aridity gradient. Our model suggests that, as leaves become thicker, the effect of reducing dx beyond dy is to offset the reduction in leaf gas exchange that would result from maintaining dx:dy at unity. This apparent overinvestment in leaf venation may be explained from the selective pressure of aridity, under which traits associated with long leaf life span, high hydraulic and thermal capacitances, and high potential rates of leaf water transport confer a competitive advantage.

Isometric partitioning of hydraulic conductance between leaves and stems: balancing safety and efficiency in different growth forms and habitats.

Recent advances in modelling the architecture and function of the plant hydraulic network have led to improvements in predicting and interpreting the consequences of functional trait variation on CO2 uptake and water loss. We build upon one such model to make novel predictions for scaling of the total specific hydraulic conductance of leaves and shoots (kL and kSH , respectively) and variation in the partitioning of hydraulic conductance. Consistent with theory, we observed isometric (slope = 1) scaling between kL and kSH across several independently collected datasets and a lower ratio of kL and kSH , termed the leaf-to-shoot conductance ratio (CLSCR ), in arid environments and in woody species. Isometric scaling of kL and kSH supports the concept that hydraulic design is coordinated across the plant. We propose that CLSCR is an important adaptive trait that represents the trade-off between efficiency and safety at the scale of the whole plant.

Smaller, faster stomata: scaling of stomatal size, rate of response, and stomatal conductance.

Maximum and minimum stomatal conductance, as well as stomatal size and rate of response, are known to vary widely across plant species, but the functional relationship between these static and dynamic stomatal properties is unknown. The objective of this study was to test three hypotheses: (i) operating stomatal conductance under standard conditions (g (op)) correlates with minimum stomatal conductance prior to morning light [g (min(dawn))]; (ii) stomatal size (S) is negatively correlated with g (op) and the maximum rate of stomatal opening in response to light, (dg/dt)(max); and (iii) g (op) correlates negatively with instantaneous water-use efficiency (WUE) despite positive correlations with maximum rate of carboxylation (Vc (max)) and light-saturated rate of electron transport (J (max)). Using five closely related species of the genus Banksia, the above variables were measured, and it was found that all three hypotheses were supported by the results. Overall, this indicates that leaves built for higher rates of gas exchange have smaller stomata and faster dynamic characteristics. With the aid of a stomatal control model, it is demonstrated that higher g (op) can potentially expose plants to larger tissue water potential gradients, and that faster stomatal response times can help offset this risk.

Linking hydraulic conductivity and photosynthesis to water-source partitioning in trees versus seedlings.

The relationships between hydraulic and photosynthetic properties in plants have been widely studied, but much less is known about how these properties are linked to water-source partitioning, the spatial and temporal separation of water sources in ecosystems. Plant water-source partitioning is often influenced by the proximity of groundwater from the natural surface. We studied the water acquisition strategy and hydraulic and photosynthetic properties of Tuart (Eucalyptus gomphocephala D.C.), a large coastal tree species that occupies seasonally dry habitats underlain by superficial aquifers. Our goal was to quantify water-source partitioning as the proportion of xylem water derived from the vadose and saturated zones with respect to stage of development and proximity of groundwater. We then sought to associate the proportional contribution of a given water source with xylem hydraulic and photosynthetic properties, thus conferring a linkage. Seedlings were more inclined to use surface soil water when rainfall recharge of the upper profile occurred, suggesting that they maintained or rapidly developed a proportionally high amount of functional roots in the upper, seasonally dry, soil profile. This strategy was associated with a lower xylem-area-specific hydraulic conductivity (K(S)), leaf-area-specific hydraulic conductivity (K(L)) and maximum photon yield of photosystem II (F(V)/F(M)). In contrast, trees acquired water from a variety of sources in different seasons and had a higher K(S), K(L) and F(V)/F(M). Despite the higher K(S) and K(L) in trees, the midday hydrodynamic water potential gradient from soil to leaves, ΔΨ, was similar. We conclude that there was a linkage between hydraulic and photosynthetic properties with the partitioning of water sources and that this adaptation to long-term hydrological regimes accommodated the different hydraulic characteristics and hydrological environments of trees versus seedlings.

Plasticity in maximum stomatal conductance constrained by negative correlation between stomatal size and density: an analysis using Eucalyptus globulus.

Maximum stomatal conductance to water vapour and CO2 (gwmax, gcmax, respectively), which are set at the time of leaf maturity, are determined predominantly by stomatal size (S) and density (D). In theory, many combinations of S and D yield the same gwmax and gcmax, so there is no inherent correlation between S and D, or between S, D and maximum stomatal conductance. However, using basic equations for gas diffusion through stomata of different sizes, we show that a negative correlation between S and D offers several advantages, including plasticity in gwmax and gcmax with minimal change in epidermal area allocation to stomata. Examination of the relationship between S and D in Eucalyptus globulus seedlings and coppice shoots growing in the field under high and low rainfall revealed a strong negative relationship between S and D, whereby S decreased with increasing D according to a negative power function. The results provide evidence that plasticity in maximum stomatal conductance may be constrained by a negative S versus D relationship, with higher maximum stomatal conductance characterized by smaller S and higher D, and a tendency to minimize change in epidermal space allocation to stomata as S and D vary.

A comparison of growth, photosynthetic capacity and water stress in Eucalyptus globulus coppice regrowth and seedlings during early development.

Eucalyptus globulus Labill., a globally significant plantation species, is grown commercially in a multiple rotation framework. Second and subsequent crops of E. globulus may be established either by allowing the cut stumps to resprout (commonly referred to as coppice) or by replanting a new crop of seedlings. Currently, long-term growth data comparing coppice and seedling productivity in second or later rotations in southern Australia is limited. The capacity to predict productivity using these tools is dependent on an understanding of the physiology of seedlings and coppice in response to light, water and nutrient supply. In this study, we compared the intrinsic (independent of the immediate environment) and native (dependent on the immediate environment) physiology of E. globulus coppice and second-generation seedlings during their early development in the field. Coppice not only grew more rapidly, but also used more water and drew on stored soil water to a depth of at least 4.5 m during the first 2 years of growth, whereas the seedlings only accessed the top 0.9 m of the soil profile. During the same period, there was no significant difference between coppice and seedlings in either their stomatal response to leaf-to-air vapour pressure difference (D) or intrinsic water-use efficiency; CO(2)- and light-saturated rates of photosynthesis were greater in seedlings than that in coppice as were the quantum yield of photosynthesis and total leaf chlorophyll content. Thus, at a leaf scale, seedlings are potentially more productive per unit leaf area than coppice during early development, but this is not realised under ambient conditions. The underlying cause of this inherent difference is discussed in the context of the allocation of resources to above- and below-ground organs during early development.

Anisohydric but isohydrodynamic: seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance.

Isohydric and anisohydric regulations of plant water status have been observed over several decades of field, glasshouse and laboratory studies, yet the functional significance and mechanism of both remain obscure. We studied the seasonal trends in plant water status and hydraulic properties in a natural stand of Eucalyptus gomphocephala through cycles of varying environmental moisture (rainfall, groundwater depth, evaporative demand) in order to test for isohydry and to provide physiological information for the mechanistic interpretation of seasonal trends in plant water status. Over a 16 month period of monitoring, spanning two summers, midday leaf water potential (psi(leaf)) correlated with predawn psi(leaf), which was correlated with water table depth below ground level, which in turn was correlated with total monthly rainfall. Eucalyptus gomphocephala was therefore not seasonally isohydric. Despite strong stomatal down-regulation of transpiration rate in response to increasing evaporative demand, this was insufficient to prevent midday psi(leaf) from falling to levels below -2 MPa in the driest month, well into the region likely to induce xylem air embolisms, based on xylem vulnerability curves obtained in the study. However, even though midday psi(leaf) varied by over 1.2 MPa across seasons, the hydrodynamic (transpiration-induced) water potential gradient from roots to shoots (delta psi(plant)), measured as the difference between predawn and midday psi(leaf), was relatively constant across seasons, averaging 0.67 MPa. This unusual pattern of hydraulic regulation, referred to here as isohydrodynamic, is explained by a hydromechanical stomatal control model where plant hydraulic conductance is dependent on transpiration rate.