Water availability affects seasonal CO₂-induced photosynthetic enhancement in herbaceous species in a periodically dry woodland

Elevated atmospheric CO2 (eCO2) is expected to reduce the impacts of drought and increase photosynthetic rates via two key mechanisms: first, through decreased stomatal conductance (gs) and increased soil water content (VSWC) and second, through increased leaf internal CO2 (Ci) and decreased stomatal limitations (Slim>). It is unclear if such findings from temperate grassland studies similarly pertain to warmer ecosystems with periodic water deficits. We tested these mechanisms in three important C3 herbaceous species in a periodically dry Eucalyptus woodland and investigated how eCO2-induced photosynthetic enhancement varied with seasonal water availability, over a 3 year period. Leaf photosynthesis increased by 10%–50% with a 150 μmol mol-1 increase in atmospheric CO2 across seasons. This eCO2-induced increase in photosynthesis was a function of seasonal water availability, given by recent precipitation and mean daily VSWC. The highest photosynthetic enhancement by eCO2 (>30%) was observed during the most water-limited period, for example, with VSWC 2 there was neither a significant decrease in gs in the three herbaceous species, nor increases in VSWC, indicating no “water-savings effect” of eCO2. Periods of low VSWC showed lower gs (less than ≈ 0.12 mol m-2 s-1), higher relative Slim (>30%) and decreased Ci under the ambient CO2 concentration (aCO2), with leaf photosynthesis strongly carboxylation-limited. The alleviation of Slim by eCO2 was facilitated by increasing Ci, thus yielding a larger photosynthetic enhancement during dry periods. We demonstrated that water availability, but not eCO2, controls gs and hence the magnitude of photosynthetic enhancement in the understory herbaceous plants. Thus, eCO2 has the potential to alter vegetation functioning in a periodically dry woodland understory through changes in stomatal limitation to photosynthesis, not by the “water-savings effect” usually invoked in grasslands

Aridity drives clinal patterns in leaf traits and responsiveness to precipitation in a broadly distributed Australian tree species

Aridity shapes species distributions and plant growth and function worldwide. Yet, plant traits often show complex relationships with aridity, challenging our understanding of aridity as a driver of evolutionary adaptation. We grew nine genotypes of Eucalyptus camaldulensis subsp. camaldulensis sourced from an aridity gradient together in the field for ~650 days under low and high precipitation treatments. Eucalyptus camaldulesis is considered a phreatophyte (deep-rooted species that utilizes groundwater), so we hypothesized that genotypes from more arid environments would show lower aboveground productivity, higher leaf gas-exchange rates, and greater tolerance/avoidance of dry surface soils (indicated by lower responsiveness) than genotypes from less arid environments. Aridity predicted genotype responses to precipitation, with more arid genotypes showing lower responsiveness to reduced precipitation and dry surface conditions than less arid genotypes. Under low precipitation, genotype net photosynthesis and stomatal conductance increased with home-climate aridity. Across treatments, genotype intrinsic water-use efficiency and osmotic potential declined with increasing aridity while photosynthetic capacity (Rubisco carboxylation and RuBP regeneration) increased with aridity. The observed clinal patterns indicate that E. camaldulensis genotypes from extremely arid environments possess a unique strategy defined by lower responsiveness to dry surface soils, low water-use efficiency, and high photosynthetic capacity. This strategy could be underpinned by deep rooting and could be adaptive under arid conditions where heat avoidance is critical and water demand is high

Thermal limits of leaf metabolism across biomes

High-temperature tolerance in plants is important in a warming world, with extreme heat waves predicted to increase in frequency and duration, potentially leading to lethal heating of leaves. Global patterns of high-temperature tolerance are documented in animals, but generally not in plants, limiting our ability to assess risks associated with climate warming. To assess whether there are global patterns in high-temperature tolerance of leaf metabolism, we quantified Tcrit (high temperature where minimal chlorophyll a fluorescence rises rapidly and thus photosystem II is disrupted) and Tmax (temperature where leaf respiration in darkness is maximal, beyond which respiratory function rapidly declines) in upper canopy leaves of 218 plant species spanning seven biomes. Mean site-based Tcrit values ranged from 41.5 °C in the Alaskan arctic to 50.8 °C in lowland tropical rainforests of Peruvian Amazon. For Tmax, the equivalent values were 51.0 and 60.6 °C in the Arctic and Amazon, respectively. Tcrit and Tmax followed similar biogeographic patterns, increasing linearly (˜8 °C) from polar to equatorial regions. Such increases in high-temperature tolerance are much less than expected based on the 20 °C span in high-temperature extremes across the globe. Moreover, with only modest high-temperature tolerance despite high summer temperature extremes, species in mid-latitude (~20-50°) regions have the narrowest thermal safety margins in upper canopy leaves; these regions are at the greatest risk of damage due to extreme heat-wave events, especially under conditions when leaf temperatures are further elevated by a lack of transpirational cooling. Using predicted heat-wave events for 2050 and accounting for possible thermal acclimation of Tcrit and Tmax, we also found that these safety margins could shrink in a warmer world, as rising temperatures are likely to exceed thermal tolerance limits. Thus, increasing numbers of species in many biomes may be at risk as heat-wave events become more severe with climate change

Thermal limits of leaf metabolism across biomes

High-temperature tolerance in plants is important in a warming world, with extreme heat waves predicted to increase in frequency and duration, potentially leading to lethal heating of leaves. Global patterns of high-temperature tolerance are documented in animals, but generally not in plants, limiting our ability to assess risks associated with climate warming. To assess whether there are global patterns in high-temperature tolerance of leaf metabolism, we quantified Tcrit (high temperature where minimal chlorophyll a fluorescence rises rapidly and thus photosystem II is disrupted) and Tmax (temperature where leaf respiration in darkness is maximal, beyond which respiratory function rapidly declines) in upper canopy leaves of 218 plant species spanning seven biomes. Mean site-based Tcrit values ranged from 41.5 °C in the Alaskan arctic to 50.8 °C in lowland tropical rainforests of Peruvian Amazon. For Tmax, the equivalent values were 51.0 and 60.6 °C in the Arctic and Amazon, respectively. Tcrit and Tmax followed similar biogeographic patterns, increasing linearly (˜8 °C) from polar to equatorial regions. Such increases in high-temperature tolerance are much less than expected based on the 20 °C span in high-temperature extremes across the globe. Moreover, with only modest high-temperature tolerance despite high summer temperature extremes, species in mid-latitude (~20–50°) regions have the narrowest thermal safety margins in upper canopy leaves; these regions are at the greatest risk of damage due to extreme heat-wave events, especially under conditions when leaf temperatures are further elevated by a lack of transpirational cooling. Using predicted heat-wave events for 2050 and accounting for possible thermal acclimation of Tcrit and Tmax, we also found that these safety margins could shrink in a warmer world, as rising temperatures are likely to exceed thermal tolerance limits. Thus, increasing numbers of species in many biomes may be at risk as heat-wave events become more severe with climate change.Access to the two Peruvian sites was also facilitated by a Moore Foundation grant (Oliver Phillips, Yadvinder Mahli, and Jon Lloyd; www.rainfor.org). This work was funded by grants/fellowships from the Australian Research Council (DP0986823, DP130101252, CE140100008, FT0991448) to O.K.A., DP140103415 to M.G.T., FT110100457 to P.M., Natural Environment Research Council (UK) to P.M. (NERC NE/F002149/1), USA National Science Foundation to K.L.G. (DEB-1234162), U.S. Department of Energy to P.B.R. (DE-FG02-7ER64456), and U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research (BER) through the Southeastern Regional Center of the National Institute for Climatic Change Research at Duke University to M.G.T and Texas AgriLife Research to M.G.T

Convergence in the temperature response of leaf respiration across biomes and plant functional types

Plant respiration constitutes a massive carbon flux to the atmosphere, and a major control on the evolution of the global carbon cycle. It therefore has the potential to modulate levels of climate change due to the human burning of fossil fuels. Neither current physiological nor terrestrial biosphere models adequately describe its short-term temperature response, and even minor differences in the shape of the response curve can significantly impact estimates of ecosystem carbon release and/or storage. Given this, it is critical to establish whether there are predictable patterns in the shape of the respiration–temperature response curve, and thus in the intrinsic temperature sensitivity of respiration across the globe. Analyzing measurements in a comprehensive database for 231 species spanning 7 biomes, we demonstrate that temperature-dependent increases in leaf respiration do not follow a commonly used exponential function. Instead, we find a decelerating function as leaves warm, reflecting a declining sensitivity to higher temperatures that is remarkably uniform across all biomes and plant functional types. Such convergence in the temperature sensitivity of leaf respiration suggests that there are universally applicable controls on the temperature response of plant energy metabolism, such that a single new function can predict the temperature dependence of leaf respiration for global vegetation. This simple function enables straightforward description of plant respiration in the land-surface components of coupled earth system models. Our cross-biome analyses shows significant implications for such fluxes in cold climates, generally projecting lower values compared with previous estimates

Global variability in leaf respiration in relation to climate, plant functional types and leaf traits

• Leaf dark respiration (Rdark) is an important yet poorly quantified component of the global carbon cycle. Given this, we analyzed a new global database of Rdark and associated leaf traits. • Data for 899 species were compiled from 100 sites (from the Arctic to the tropics). Several woody and nonwoody plant functional types (PFTs) were represented. Mixed-effects models were used to disentangle sources of variation in Rdark. • Area-based Rdark at the prevailing average daily growth temperature (T) of each site increased only twofold from the Arctic to the tropics, despite a 20°C increase in growing T (8–28°C). By contrast, Rdark at a standard T (25°C, Rdark25) was threefold higher in the Arctic than in the tropics, and twofold higher at arid than at mesic sites. Species and PFTs at cold sites exhibited higher Rdark25 at a given photosynthetic capacity (Vcmax25) or leaf nitrogen concentration ([N]) than species at warmer sites. Rdark25 values at any given Vcmax25 or [N] were higher in herbs than in woody plants. • The results highlight variation in Rdark among species and across global gradients in T and aridity. In addition to their ecological significance, the results provide a framework for improving representation of Rdark in terrestrial biosphere models (TBMs) and associated land-surface components of Earth system models (ESMs)

Understanding the coordination of hydraulic strategies with other traits in determining plant survival under drought

Drought negatively impacts plant growth and survival. The ability to maintain hydraulic functionality during water stress strongly influences whether plants will survive and recover from drought. Although our understanding of the mechanisms underlying drought-induced mortality have improved in recent decades, our understanding of the coordination between stomatal and hydraulic traits and their role in shaping drought resistance and enabling recovery remains poorly understood. In this thesis, I examined plant hydraulic traits across a range of contrasting species in order to better understand how hydraulics determines plant function under drought, governs gas exchange, and drives differences in drought resistance. By subjecting three contrasting Australian tree species to water limitation, we were able to determine the hydraulic vulnerability to embolism of leaves, stems and roots as well as the relationship between stomatal conductance and photosynthesis with decreasing water potential. We found that leaves and/or roots were more vulnerable than stems in Eucalyptus coolabah and Acacia aneura, however E. populnea did not show vulnerability segmentation. Additionally, in these species stomatal closure always occurred prior to significant hydraulic dysfunction. We confirmed this finding in three additional tree species, Arbutus unedo, Ligustrum japonicum and Prunus persica via direct imaging of leaf embolism formation by the Optical Visualisation (OV) method with simultaneous measurements of stomatal conductance on intact plants. Prior drought exposure resulted in higher rates of photosynthesis in E. coolabah and E. melliodora under subsequent water stress in comparison with plants that had not previously experienced drought, due to differences in stomatal regulation that enabled stomata to remain open for longer at lower potentials. Plants that had previously experienced drought also reduced leaf size and had lower overall biomass indicating that these species can acclimate to recurrent drought. In combination, our results strongly suggest that the ability to resist hydraulic dysfunction, rather than recover from xylem embolism underpins plant resilience to drought, with early stomatal regulation to prevent water loss and delay catastrophic xylem dysfunction crucial to plant survival and recovery

Xylem embolism in leaves does not occur with open stomata: evidence from direct observations using the optical visualization technique

Drought represents a major abiotic constraint to plant growth and survival. On the one hand, plants keep stomata open for efficient carbon assimilation while, on the other hand, they close them to prevent permanent hydraulic impairment from xylem embolism. The order of occurrence of these two processes (stomatal closure and the onset of leaf embolism) during plant dehydration has remained controversial, largely due to methodological limitations. However, the newly developed optical visualization method now allows concurrent monitoring of stomatal behaviour and leaf embolism formation in intact plants. We used this new approach directly by dehydrating intact saplings of three contrasting tree species and indirectly by conducting a literature survey across a greater range of plant taxa. Our results indicate that increasing water stress generates the onset of leaf embolism consistently after stomatal closure, and that the lag time between these processes (i.e. the safety margin) rises with increasing embolism resistance. This suggests that during water stress, embolism-mediated declines in leaf hydraulic conductivity are unlikely to act as a signal for stomatal down-regulation. Instead, these species converge towards a strategy of closing stomata early to prevent water loss and delay catastrophic xylem dysfunction

Xylem embolism in leaves does not occur with open stomata: evidence from direct observations using the optical visualisation technique

Drought represents a major abiotic constraint to plant growth and survival. On one hand, plants keep stomata open for efficient carbon assimilation, while on the other hand, they close them to prevent permanent hydraulic impairment from xylem embolism. The order of occurrence of these two processes (stomatal closure and the onset of leaf embolism) throughout plant dehydration has remained controversial, largely due to methodological limitations. However, the newly developed Optical Visualisation (OV) method now allows simultaneous monitoring of stomatal behaviour and leaf embolism formation in intact plants. We used this new approach directly by dehydrating intact saplings of three contrasting tree species and indirectly by conducting a literature survey across a greater range of plant taxa. Our results indicate that increasing water stress generates the onset of leaf embolism consistently after stomatal closure, and that the lag time between these processes (i.e. the safety margin) increases with increasing embolism resistance. This suggests that during water stress, embolism-mediated declines in leaf hydraulic conductivity are unlikely to act as a signal for stomatal down-regulation. Instead, plants converge towards a strategy of closing stomata early to prevent water loss and delay catastrophic xylem dysfunction

Xylem embolism in leaves does not occur with open stomata: evidence from direct observations using the optical visualisation technique

Drought represents a major abiotic constraint to plant growth and survival. On one hand, plants keep stomata open for efficient carbon assimilation, while on the other hand, they close them to prevent permanent hydraulic impairment from xylem embolism. The order of occurrence of these two processes (stomatal closure and the onset of leaf embolism) throughout plant dehydration has remained controversial, largely due to methodological limitations. However, the newly developed Optical Visualisation (OV) method now allows simultaneous monitoring of stomatal behaviour and leaf embolism formation in intact plants. We used this new approach directly by dehydrating intact saplings of three contrasting tree species and indirectly by conducting a literature survey across a greater range of plant taxa. Our results indicate that increasing water stress generates the onset of leaf embolism consistently after stomatal closure, and that the lag time between these processes (i.e. the safety margin) increases with increasing embolism resistance. This suggests that during water stress, embolism-mediated declines in leaf hydraulic conductivity are unlikely to act as a signal for stomatal down-regulation. Instead, plants converge towards a strategy of closing stomata early to prevent water loss and delay catastrophic xylem dysfunction