Melanie Zeppel

Tree mortality from drought, insects, and their interactions in a changing climate

Climate change is expected to drive increased tree mortality through drought, heat stress, and insect attacks, with manifold impacts on forest ecosystems. Yet, climate-induced tree mortality and biotic disturbance agents are largely absent from process-based ecosystem models. Using data sets from the western USA and associated studies, we present a framework for determining the relative contribution of drought stress, insect attack, and their interactions, which is critical for modeling mortality in future climates. We outline a simple approach that identifies the mechanisms associated with two guilds of insects - bark beetles and defoliators - which are responsible for substantial tree mortality. We then discuss cross-biome patterns of insect-driven tree mortality and draw upon available evidence contrasting the prevalence of insect outbreaks in temperate and tropical regions. We conclude with an overview of tools and promising avenues to address major challenges. Ultimately, a multitrophic approach that captures tree physiology, insect populations, and tree-insect interactions will better inform projections of forest ecosystem responses to climate change.

Seasonal responses of xylem sap velocity to VPD and solar radiation during drought in a stand of native trees in temperate Australia

Xylem sap velocity of two dominant tree species, Eucalyptus crebra F. Muell. and Callitris glaucophylla J. Thompson & L.A.S. Johnson, in a native remnant forest of eastern Australia was measured in winter and summer during a prolonged (> 12 months) and extensive drought. The influence of vapour pressure deficit (VPD) and solar radiation levels on the velocity of sap was determined. Pronounced hysteresis in sap velocity was observed in both species as a function of VPD and solar radiation. However, the rotation of the hysteresis curve was clockwise for the response of sap velocity to VPD but anti-clockwise in the response of sap velocity to radiation levels. A possible reason for this difference is discussed.The degree of hysteresis (area bounded by the curve) was larger for the VPD response than the response to solar radiation and also varied with season. A simple linear model was able to predict sap velocity from knowledge of VPD and solar radiation in winter and summer. The consistent presence of hysteresis in the response to sap velocity to VPD and solar radiation suggests that large temporal and spatial models of vegetation water use may require some provision for the different responses of sap velocity, and hence water use, to VPD and solar radiation, between morning and afternoon and between seasons.

Rates of nocturnal transpiration in two evergreen temperate woodland species with differing water-use strategies.

Nocturnal fluxes may be a significant factor in the annual water budget of forested ecosystems. Here, we assessed sap flow in two co-occurring evergreen species (Eucalyptus parramattensis and Angophora bakeri) in a temperate woodland for 2 years in order to quantify the magnitude of seasonal nocturnal sap flow (E(n)) under different environmental conditions. The two species showed different diurnal water relations, demonstrated by different diurnal curves of stomatal conductance, sap flow and leaf water potential. The relative influence of several microclimatic variables, including wind speed (U), vapour pressure deficit (D), the product of U and D (UD) and soil moisture content, were quantified. D exerted the strongest influence on E(n) (r² = 0.59-0.86), soil moisture content influenced E(n) when D was constant, but U and UD did not generally influence E(n). In both species, cuticular conductance (G(c)) was a small proportion of total leaf conductance (G(s)) and was not a major pathway for E(n). We found that E(n) was primarily a function of transpiration from the canopy rather than refilling of stem storage, with canopy transpiration accounting for 50-70% of nocturnal flows. Mean E(n) was 6-8% of the 24-h flux across seasons (spring, summer and winter), but was up to 19% of the 24-h flux on some days in both species. Despite different daytime strategies in water use of the two species, both species demonstrated low night-time water loss, suggesting similar controls on water loss at night. In order to account for the impact of E(n) on pre-dawn leaf water potential arising from the influence of disequilibria between root zone and leaf water potential, we also developed a simple model to more accurately predict soil water potential (ψ(s)).

Nocturnal stomatal conductance responses to rising [CO2], temperature and drought

The response of nocturnal stomatal conductance (g(s,n)) to rising atmospheric CO(2) concentration ([CO(2)]) is currently unknown, and may differ from responses of daytime stomatal conductance (g(s,d)). Because night-time water fluxes can have a significant impact on landscape water budgets, an understanding of the effects of [CO(2)] and temperature on g(s,n) is crucial for predicting water fluxes under future climates. Here, we examined the effects of [CO(2)] (280, 400 and 640 μmol mol(-1)), temperature (ambient and ambient + 4°C) and drought on g(s,n,) and g(s,d) in Eucalyptus sideroxylon saplings. g(s,n) was substantially higher than zero, averaging 34% of g(s,d). Before the onset of drought, g(s,n) increased by 85% when [CO(2)] increased from 280 to 640 μmol mol(-1), averaged across both temperature treatments. g(s,n) declined with drought, but an increase in [CO(2)] slowed this decline. Consequently, the soil water potential at which g(s,n) was zero (Ψ(0)) was significantly more negative in elevated [CO(2)] and temperature treatments. g(s,d) showed inconsistent responses to [CO(2)] and temperature. g (s,n) may be higher in future climates, potentially increasing nocturnal water loss and susceptibility to drought, but cannot be predicted easily from g(s,d). Therefore, predictive models using stomatal conductance must account for both g(s,n) and g(s,d) when estimating ecosystem water fluxes.

A multi-species synthesis of physiological mechanisms in drought-induced tree mortality

Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere–atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.The mechanisms underlying drought-induced tree mortality are not fully resolved. Here, the authors show that, across multiple tree species, loss of xylem conductivity above 60% is associated with mortality, while carbon starvation is not universal.

Research frontiers in drought-induced tree mortality: Crossing scales and disciplines

Sudden and widespread forest die-back and die-off (e.g., Huang & Anderegg, 2012) and increased mortality rates (e.g., Peng et al., 2011) in many forest ecosystems across the globe have been linked to drought and elevated temperatures (Allen et al., 2010, Fig. 1). Furthermore, these observations have caused a focus on the physiological mechanisms of drought-induced tree mortality (e.g. McDowell et al., 2008) and many studies, both observational and manipulative, have been carried out to explain tree death during drought from a physiological perspective.

Responses of two semiarid conifer tree species to reduced precipitation and warming reveal new perspectives for stomatal regulation

Relatively anisohydric species are predicted to be more predisposed to hydraulic failure than relatively isohydric species, as they operate with narrower hydraulic safety margins. We subjected co-occurring anisohydric Juniperus monosperma and isohydric Pinus edulis trees to warming, reduced precipitation, or both, and measured their gas exchange and hydraulic responses. We found that reductions in stomatal conductance and assimilation by heat and drought were more frequent during relatively moist periods, but these effects were not exacerbated in the combined heat and drought treatment. Counter to expectations, both species exhibited similar gs temporal dynamics in response to drought. Further, whereas P. edulis exhibited chronic embolism, J. monosperma showed very little embolism due to its conservative stomatal regulation and maintenance of xylem water potential above the embolism entry point. This tight stomatal control and low levels of embolism experienced by juniper refuted the notion that very low water potentials during drought are associated with loose stomatal control and with the hypothesis that anisohydric species are more prone to hydraulic failure than isohydric species. Because direct association of stomatal behaviour with embolism resistance can be misleading, we advocate consideration of stomatal behaviour relative to embolism resistance for classifying species drought response strategies.

An automated procedure for estimating the leaf area index (LAI) of woodland ecosystems using digital imagery, MATLAB programming and its application to an examination of the relationship between remotely sensed and field measurements of LAI

Leaf area index (LAI) is one of the most important variables required for modelling growth and water use of forests. Functional-structural plant models use these models to represent physiological processes in 3-D tree representations. Accuracy of these models depends on accurate estimation of LAI at tree and stand scales for validation purposes. A recent method to estimate LAI from digital images (LAID) uses digital image capture and gap fraction analysis (Macfarlane et al. 2007b) of upward-looking digital photographs to capture canopy LAID (cover photography). After implementing this technique in Australian evergreen Eucalyptus woodland, we have improved the method of image analysis and replaced the time consuming manual technique with an automated procedure using a script written in MATLAB 7.4 (LAIM). Furthermore, we used this method to compare MODIS LAI values with LAID values for a range of woodlands in Australia to obtain LAI at the forest scale. Results showed that the MATLAB script developed was able to successfully automate gap analysis to obtain LAIM. Good relationships were achieved when comparing averaged LAID and LAIM (LAIM = 1.009 - 0.0066 LAID; R2 = 0.90) and at the forest scale, MODIS LAI compared well with LAID (MODIS LAI = 0.9591 LAID - 0.2371; R2 = 0.89). This comparison improved when correcting LAID with the clumping index to obtain effective LAI (MODIS LAI = 1.0296 LAIe + 0.3468; R2 = 0.91). Furthermore, the script developed incorporates a function to connect directly a digital camera, or high resolution webcam, from a laptop to obtain cover photographs and LAI analysis in real time. The later is a novel feature which is not available on commercial LAI analysis softwares for cover photography. This script is available for interested researchers.

An analysis of the sensitivity of sap flux to soil and plant variables assessed for an Australian woodland using a soil–plant–atmosphere model

Daily and seasonal patterns of tree water use were measured for the two dominant tree species, Angophora bakeri E.C.Hall (narrow-leaved apple) and Eucalyptus sclerophylla (Blakely) L.A.S. Johnson & Blaxell (scribbly gum), in a temperate, open, evergreen woodland using sap flow sensors, along with information about soil, leaf, tree and micro-climatological variables. The aims of this work were to: (a) validate a soil-plant-atmosphere (SPA) model for the specific site; (b) determine the total depth from which water uptake must occur to achieve the observed rates of tree sap flow; (c) examine whether the water content of the upper soil profile was a significant determinant of daily rates of sap flow; and (d) examine the sensitivity of sap flow to several biotic factors. It was found that: (a) the SPA model was able to accurately replicate the hourly, daily and seasonal patterns of sap flow; (b) water uptake must have occurred from depths of up to 3 m; (c) sap flow was independent of the water content of the top 80 cm of the soil profile; and (d) sap flow was very sensitive to the leaf area of the stand, whole tree hydraulic conductance and the critical water potential of the leaves, but insensitive to stem capacitance and increases in root biomass. These results are important to future studies of the regulation of vegetation water use, landscape-scale behaviour of vegetation, and to water resource managers, because they allow testing of large-scale management options without the need for large-scale manipulations of vegetation cover.

Drought and resprouting plants

Many species have the ability to resprout vegetatively after a substantial loss of biomass induced by environmental stress, including drought. Many of the regions characterised by ecosystems where resprouting is common are projected to experience more frequent and intense drought during the 21st Century. However, in assessments of ecosystem response to drought disturbance there has been scant consideration of the resilience and post-drought recovery of resprouting species. Systematic differences in hydraulic and allocation traits suggest that resprouting species are more resilient to drought-stress than nonresprouting species. Evidence suggests that ecosystems dominated by resprouters recover from disturbance more quickly than ecosystems dominated by nonresprouters. The ability of resprouters to avoid mortality and withstand drought, coupled with their ability to recover rapidly, suggests that the impact of increased drought stress in ecosystems dominated by these species may be small. The strategy of resprouting needs to be modelled explicitly to improve estimates of future climate-change impacts on the carbon cycle, but this will require several important knowledge gaps to be filled before resprouting can be properly implemented.