Drought increases heat tolerance of leaf respiration in Eucalyptus globulus saplings grown under both ambient and elevated atmospheric [CO₂] and temperature

Climate change is resulting in increasing atmospheric [CO₂], rising growth temperature (T), and greater frequency/severity of drought, with each factor having the potential to alter the respiratory metabolism of leaves. Here, the effects of elevated atmospheric [CO₂], sustained warming, and drought on leaf dark respiration (R(dark)), and the short-term T response of R(dark) were examined in Eucalyptus globulus. Comparisons were made using seedlings grown under different [CO₂], T, and drought treatments. Using high resolution T-response curves of R(dark) measured over the 15-65 °C range, it was found that elevated [CO₂], elevated growth T, and drought had little effect on rates of R(dark) measured at T <35 °C and that there was no interactive effect of [CO₂], growth T, and drought on T response of R(dark). However, drought increased R(dark) at high leaf T typical of heatwave events (35-45 °C), and increased the measuring T at which maximal rates of R(dark) occurred (Tmax) by 8 °C (from 52 °C in well-watered plants to 60 °C in drought-treated plants). Leaf starch and soluble sugars decreased under drought and elevated growth T, respectively, but no effect was found under elevated [CO₂]. Elevated [CO₂] increased the Q₁₀ of R(dark) (i.e. proportional rise in R(dark) per 10 °C) over the 15-35 °C range, while drought increased Q₁₀ values between 35 °C and 45 °C. Collectively, the study highlights the dynamic nature of the T dependence of R dark in plants experiencing future climate change scenarios, particularly with respect to drought and elevated [CO₂].This work was funded by the Australian Research Council (ARC FT0991448, DP1093759, and CE140100008, to OKA; and DP0879531, to DTT). This project is supported by funding from the Australian Government Department of Agriculture, Fisheries and Forestry under its Forest Industries Climate Change Research Fund programme. Support for the renovation of the Hawkesbury Forest Experiment tree chambers to improve T and humidity control of the WTC was provided as part of an initiative of the Australian Government through the Education Investment Fund supporting research infrastructure

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

A test of the 'one-point method' for estimating maximum carboxylation capacity from field-measured, light-saturated photosynthesis

Simulations of photosynthesis by terrestrial biosphere models typically need a specification of the maximum carboxylation rate (Vcmax). Estimating this parameter using A–Ci curves (net photosynthesis, A, vs intercellular CO2 concentration, Ci) is laborious, which limits availability of Vcmax data. However, many multispecies field datasets include net photosynthetic rate at saturating irradiance and at ambient atmospheric CO2 concentration (Asat) measurements, from which Vcmax can be extracted using a 'one-point method'.\ud \ud We used a global dataset of A–Ci curves (564 species from 46 field sites, covering a range of plant functional types) to test the validity of an alternative approach to estimate Vcmax from Asat via this 'one-point method'.\ud \ud If leaf respiration during the day (Rday) is known exactly, Vcmax can be estimated with an r2 value of 0.98 and a root-mean-squared error (RMSE) of 8.19 μmol m−2 s−1. However, Rday typically must be estimated. Estimating Rday as 1.5% of Vcmax, we found that Vcmax could be estimated with an r2 of 0.95 and an RMSE of 17.1 μmol m−2 s−1.\ud \ud The one-point method provides a robust means to expand current databases of field-measured Vcmax, giving new potential to improve vegetation models and quantify the environmental drivers of Vcmax variation

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

Non-structural carbohydrates in woody plants compared among laboratories

Non-structural carbohydrates (NSC) in plant tissue are frequently quantified to make inferences about plant responses to environmental conditions. Laboratories publishing estimates of NSC of woody plants use many different methods to evaluate NSC. We asked whether NSC estimates in the recent literature could be quantitatively compared among studies. We also asked whether any differences among laboratories were related to the extraction and quantification methods used to determine starch and sugar concentrations. These questions were addressed by sending sub-samples collected from five woody plant tissues, which varied in NSC content and chemical composition, to 29 laboratories. Each laboratory analyzed the samples with their laboratory-specific protocols, based on recent publications, to determine concentrations of soluble sugars, starch and their sum, total NSC. Laboratory estimates differed substantially for all samples. For example, estimates for Eucalyptus globulus leaves (EGL) varied from 23 to 116 (mean = 56) mg g⁻¹ for soluble sugars, 6–533 (mean = 94) mg g⁻¹ for starch and 53–649 (mean = 153) mg g⁻¹ for total NSC. Mixed model analysis of variance showed that much of the variability among laboratories was unrelated to the categories we used for extraction and quantification methods (method category R² = 0.05–0.12 for soluble sugars, 0.10–0.33 for starch and 0.01–0.09 for total NSC). For EGL, the difference between the highest and lowest least squares means for categories in the mixed model analysis was 33 mg g⁻¹ for total NSC, compared with the range of laboratory estimates of 596 mg g⁻¹. Laboratories were reasonably consistent in their ranks of estimates among tissues for starch (r = 0.41–0.91), but less so for total NSC (r = 0.45–0.84) and soluble sugars (r = 0.11–0.83). Our results show that NSC estimates for woody plant tissues cannot be compared among laboratories. The relative changes in NSC between treatments measured within a laboratory may be comparable within and between laboratories, especially for starch. To obtain comparable NSC estimates, we suggest that users can either adopt the reference method given in this publication, or report estimates for a portion of samples using the reference method, and report estimates for a standard reference material. Researchers interested in NSC estimates should work to identify and adopt standard methods.This is the publisher’s final pdf. The published article is copyrighted by the author(s) and published by Oxford University Press. The published article can be found at: http://treephys.oxfordjournals.org/Keywords: soluble sugars, starch, particle size, reference method, standardization, non-structural carbohydrate chemical analysis, extraction and quantification consistenc

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)

Canopy position affects the relationships between leaf respiration and associated traits in a tropical rainforest in Far North Queensland

We explored the impact of canopy position on leaf respiration (R) and associated traits in tree and shrub species growing in a lowland tropical rainforest in Far North Queensland, Australia. The range of traits quantified included: leaf R in darkness (RD) and in the light (RL; estimated using the Kok method); the temperature (T)-sensitivity of RD; light-saturated photosynthesis (Asat); leaf dry mass per unit area (LMA); and concentrations of leaf nitrogen (N), phosphorus (P), soluble sugars and starch. We found that LMA, and area-based N, P, sugars and starch concentrations were all higher in sun-exposed/upper canopy leaves, compared with their shaded/lower canopy and deep-shade/understory counterparts; similarly, area-based rates of RD, RL and Asat (at 28 °C) were all higher in the upper canopy leaves, indicating higher metabolic capacity in the upper canopy. The extent to which light inhibited R did not differ significantly between upper and lower canopy leaves, with the overall average inhibition being 32% across both canopy levels. Log–log RD–Asat relationships differed between upper and lower canopy leaves, with upper canopy leaves exhibiting higher rates of RD for a given Asat (both on an area and mass basis), as well as higher mass-based rates of RD for a given [N] and [P]. Over the 25–45 °C range, the T-sensitivity of RD was similar in upper and lower canopy leaves, with both canopy positions exhibiting Q10 values near 2.0 (i.e., doubling for every 10 °C rise in T) and Tmax values near 60 °C (i.e., T where RD reached maximal values). Thus, while rates of RD at 28 °C decreased with increasing depth in the canopy, the T-dependence of RD remained constant; these findings have important implications for vegetation-climate models that seek to predict carbon fluxes between tropical lowland rainforests and the atmosphere

Supporting Information (Guilherme Pereira et al. 2019), Journal of Ecology

This file contains the individual replicate data reported in Guilherme Pereira et al. (2019). Details on site location, sampling procedures and species are provided in the paper. The data is provided to others to freely use in their own analyses - we ask that users to cite Guilherme Pereira et al. (2019) in any output that may emerge

High-resolution temperature responses of leaf respiration in snow gum (Eucalyptus pauciflora) reveal high-temperature limits to respiratory function

We tested whether snow gum (Eucalyptus pauciflora) trees growing in thermally contrasting environments exhibit generalizable temperature (T) response functions of leaf respiration (R) and fluorescence (Fo). Measurements were made on pot-grown saplings and field-grown trees (growing between 1380 and 2110m a.s.l.). Using a continuous, high-resolution protocol, we quantified T response curves of R and Fo - these data were used to identify an algorithm for modelling R-T curves at subcritical T's and establish variations in heat tolerance. For the latter, we quantified Tmax [T where R is maximal] and Tcrit [T where Fo rises rapidly]. Tmax ranged from 51 to 57°C, varying with season (e.g. winter > summer). Tcrit ranged from 41 to 49°C in summer and from 58 to 63°C in winter. Thus, surprisingly, leaf energy metabolism was more heat-tolerant in trees experiencing ice-encasement in winter than warmer conditions in summer. A polynomial model fitted to log-transformed R data provided the best description of the T-sensitivity of R (between 10 and 45°C); using these model fits, we found that the negative slope of the Q10-T relationship was greater in winter than in summer. Collectively, our results (1) highlight high-T limits of energy metabolism in E.pauciflora and (2) provide a framework for improving representation of T-responses of leaf R in predictive models

Data from: Trait convergence in photosynthetic nutrient-use efficiency along a 2-million year dune chronosequence in a global biodiversity hotspot

1. The Jurien Bay dune chronosequence in south-western Australia’s biodiversity hotspot comprises sites differing in nutrient availability, with phosphorus (P) availability declining strongly with increasing soil age. We have explored the exceptionally high photosynthetic P-use efficiency (PPUE) of Proteaceae in this region, triggering the question what the PPUE of co-occurring species in other families might be along the Jurien Bay chronosequence. 2. We explored how traits associated with PPUE, photosynthetic nitrogen (N)-use efficiency (PNUE) and leaf respiration might converge along the chronosequence, and whether Proteaceae and non-Proteaceae species differ in leaf traits associated with nutrient use. 3. Seven to 10 species were sampled at three sites differing in nutrient availability (ranging from N- to P-limited). Measurements of leaf light-saturated photosynthesis and dark respiration were integrated with measurements of total N and P concentration in both mature and senesced leaves, and leaf mass per unit area (LMA). 4. Contrary to what is known for other chronosequences, rates of photosynthesis and respiration did not decrease with increasing soil age and LMA along the Jurien Bay chronosequence. However, they increased when expressed per unit leaf P. Both N and P were used much more efficiently for photosynthesis on nutrient-poor sites, in both Proteaceae and non-Proteaceae species. Proteaceae had the fastest rate of photosynthesis per unit leaf P, followed by species that preferentially allocate P to mesophyll cells, rather than epidermal cells. 5. Synthesis. Our results show that with declining soil P availability, PPUE of all investigated species from different families increased. Plants growing on the oldest, most nutrient-impoverished soils exhibited similar rates of CO2-exchange as plants growing on more nutrient-rich younger soils, and extraordinarily high PPUE. This indicates convergence in leaf traits related to photosynthetic nutrient use on severely P-impoverished sites