Similar patterns of leaf temperatures and thermal acclimation to warming in temperate and tropical tree canopies

As the global climate warms, a key question is how increased leaf temperatures will affect tree physiology and the coupling between leaf and air temperatures in forests. To explore the impact of increasing temperatures on plant performance in open air, we warmed leaves in the canopy of two mature evergreen forests, a temperate Eucalyptus woodland and a tropical rainforest. The leaf heaters consistently maintained leaves at a target of 4 °C above ambient leaf temperatures. Ambient leaf temperatures (Tleaf) were mostly coupled to air temperatures (Tair), but at times, leaves could be 8–10 °C warmer than ambient air temperatures, especially in full sun. At both sites, Tleaf was warmer at higher air temperatures (Tair > 25 °C), but was cooler at lower Tair, contrary to the ‘leaf homeothermy hypothesis’. Warmed leaves showed significantly lower stomatal conductance (−0.05 mol m−2 s−1 or −43% across species) and net photosynthesis (−3.91 μmol m−2 s−1 or −39%), with similar rates in leaf respiration rates at a common temperature (no acclimation). Increased canopy leaf temperatures due to future warming could reduce carbon assimilation via reduced photosynthesis in these forests, potentially weakening the land carbon sink in tropical and temperate forests

Incorporating non-stomatal limitation improves the performance of leaf and canopy models at high vapour pressure deficit

Vapour pressure deficit (D) is projected to increase in the future as temperature rises. In response to increased D, stomatal conductance (gs) and photosynthesis (A) are reduced, which may result in significant reductions in terrestrial carbon, water and energy fluxes. It is thus important for gas exchange models to capture the observed responses of gs and A with increasing D. We tested a series of coupled A-gs models against leaf gas exchange measurements from the Cumberland Plain Woodland (Australia), where D regularly exceeds 2 kPa and can reach 8 kPa in summer. Two commonly used A-gs models were not able to capture the observed decrease in A and gs with increasing D at the leaf scale. To explain this decrease in A and gs, two alternative hypotheses were tested: hydraulic limitation (i.e., plants reduce gs and/or A due to insufficient water supply) and non-stomatal limitation (i.e., downregulation of photosynthetic capacity). We found that the model that incorporated a non-stomatal limitation captured the observations with high fidelity and required the fewest number of parameters. Whilst the model incorporating hydraulic limitation captured the observed A and gs, it did so via a physical mechanism that is incorrect. We then incorporated a non-stomatal limitation into the stand model, MAESPA, to examine its impact on canopy transpiration and gross primary production. Accounting for a non-stomatal limitation reduced the predicted transpiration by ~19%, improving the correspondence with sap flow measurements, and gross primary production by ~14%. Given the projected global increases in D associated with future warming, these findings suggest that models may need to incorporate non-stomatal limitation to accurately simulate A and gs in the future with high D. Further data on non-stomatal limitation at high D should be a priority, in order to determine the generality of our results and develop a widely applicable model. © The Author(s) 2019. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: [email protected]. was supported by a PhD scholarship from Hawkesbury Institute for the Environment, Western Sydney University. M.G.D.K. acknowledges funding from the Australian Research Council (ARC) Centre of Excellence for Climate Extremes (CE170100023), the ARC Discovery Grant (DP190101823) and support from the NSW Research Attraction and Acceleration Program. EucFACE was built as an initiative of the Australian Government as part of the Nation-building Economic Stimulus Package and is supported by the Australian Commonwealth in collaboration with Western Sydney University. It is also part of a Terrestrial Ecosystem Research Network Super-site facility

The fate of carbon in a mature forest under carbon dioxide enrichment

Atmospheric carbon dioxide enrichment (eCO2) can enhance plant carbon uptake and growth1 5, thereby providing an important negative feedback to climate change by slowing the rate of increase of the atmospheric CO2 concentration6. Although evidence gathered from young aggrading forests has generally indicated a strong CO2 fertilization effect on biomass growth3 5, it is unclear whether mature forests respond to eCO2 in a similar way. In mature trees and forest stands7 10, photosynthetic uptake has been found to increase under eCO2 without any apparent accompanying growth response, leaving the fate of additional carbon fixed under eCO2 unclear4,5,7 11. Here using data from the first ecosystem-scale Free-Air CO2 Enrichment (FACE) experiment in a mature forest, we constructed a comprehensive ecosystem carbon budget to track the fate of carbon as the forest responded to four years of eCO2 exposure. We show that, although the eCO2 treatment of +150 parts per million (+38 per cent) above ambient levels induced a 12 per cent (+247 grams of carbon per square metre per year) increase in carbon uptake through gross primary production, this additional carbon uptake did not lead to increased carbon sequestration at the ecosystem level. Instead, the majority of the extra carbon was emitted back into the atmosphere via several respiratory fluxes, with increased soil respiration alone accounting for half of the total uptake surplus. Our results call into question the predominant thinking that the capacity of forests to act as carbon sinks will be generally enhanced under eCO2, and challenge the efficacy of climate mitigation strategies that rely on ubiquitous CO2 fertilization as a driver of increased carbon sinks in global forests. © 2020, The Author(s), under exclusive licence to Springer Nature Limited

Low sensitivity of gross primary production to elevated CO2 in a mature eucalypt woodland

The response of mature forest ecosystems to a rising atmospheric carbon dioxide concentration (span classCombining double low line"inline-formula"iC/ia/span) is a major uncertainty in projecting the future trajectory of the Earth's climate. Although leaf-level net photosynthesis is typically stimulated by exposure to elevated span classCombining double low line"inline-formula"iC/ia/span (espan classCombining double low line"inline-formula"iC/ia/span), it is unclear how this stimulation translates into carbon cycle responses at the ecosystem scale. Here we estimate a key component of the carbon cycle, the gross primary productivity (GPP), of a mature native eucalypt forest exposed to free-air span classCombining double low line"inline-formula"CO2/span enrichment (the EucFACE experiment). In this experiment, light-saturated leaf photosynthesis increased by 19andthinsp;% in response to a 38andthinsp;% increase in span classCombining double low line"inline-formula"iC/ia/span. We used the process-based forest canopy model, MAESPA, to upscale these leaf-level measurements of photosynthesis with canopy structure to estimate the GPP and its response to espan classCombining double low line"inline-formula"iC/ia/span. We assessed the direct impact of espan classCombining double low line"inline-formula"iC/ia/span, as well as the indirect effect of photosynthetic acclimation to espan classCombining double low line"inline-formula"iC/ia/span and variability among treatment plots using different model scenarios./p At the canopy scale, MAESPA estimated a GPP of 1574andthinsp;gandthinsp;Candthinsp;mspan classCombining double low line"inline-formula"-2/spanandthinsp;yrspan classCombining double low line"inline-formula"-1/span under ambient conditions across 4 years and a direct increase in the GPP of span classCombining double low line"inline-formula"+/span11andthinsp;% in response to espan classCombining double low line"inline-formula"iC/ia/span. The smaller canopy-scale response simulated by the model, as compared with the leaf-level response, could be attributed to the prevalence of RuBP regeneration limitation of leaf photosynthesis within the canopy. Photosynthetic acclimation reduced this estimated response to 10andthinsp;%. After taking the baseline variability in the leaf area index across plots in account, we estimated a field GPP response to espan classCombining double low line"inline-formula"iC/ia/span of 6andthinsp;% with a 95andthinsp;% confidence interval (span classCombining double low line"inline-formula"-/span2andthinsp;%, 14andthinsp;%). These findings highlight that the GPP response of mature forests to espan classCombining double low line"inline-formula"iC/ia/span is likely to be considerably lower than the response of light-saturated leaf photosynthesis. Our results provide an important context for interpreting the espan classCombining double low line"inline-formula"iC/ia/span responses of other components of the ecosystem carbon cycle. © Author(s) 2020.Martin G. De Kauwe was supported by the NSW Research Attraction and Acceleration Program (RAAP). Euc-FACE was built as an initiative of the Australian Government as part of the Nation Building Economic Stimulus Plan and is supported by the Australian Commonwealth in collaboration with Western Sydney University

Tropical forests are approaching critical temperature thresholds

The critical temperature beyond which photosynthetic machinery in tropical trees begins to fail averages approximately 46.7 °C (Tcrit)1. However, it remains unclear whether leaf temperatures experienced by tropical vegetation approach this threshold or soon will under climate change. Here we found that pantropical canopy temperatures independently triangulated from individual leaf thermocouples, pyrgeometers and remote sensing (ECOSTRESS) have midday peak temperatures of approximately 34 °C during dry periods, with a long high-temperature tail that can exceed 40 °C. Leaf thermocouple data from multiple sites across the tropics suggest that even within pixels of moderate temperatures, upper canopy leaves exceed Tcrit 0.01% of the time. Furthermore, upper canopy leaf warming experiments (+2, 3 and 4 °C in Brazil, Puerto Rico and Australia, respectively) increased leaf temperatures non-linearly, with peak leaf temperatures exceeding Tcrit 1.3% of the time (11% for more than 43.5 °C, and 0.3% for more than 49.9 °C). Using an empirical model incorporating these dynamics (validated with warming experiment data), we found that tropical forests can withstand up to a 3.9 ± 0.5 °C increase in air temperatures before a potential tipping point in metabolic function, but remaining uncertainty in the plasticity and range of Tcrit in tropical trees and the effect of leaf death on tree death could drastically change this prediction. The 4.0 °C estimate is within the ‘worst-case scenario’ (representative concentration pathway (RCP) 8.5) of climate change predictions2 for tropical forests and therefore it is still within our power to decide (for example, by not taking the RCP 6.0 or 8.5 route) the fate of these critical realms of carbon, water and biodiversity

Global photosynthetic capacity is optimized to the environment

Earth system models (ESMs) use photosynthetic capacity, indexed by the maximum Rubisco carboxylation rate (V-cmax), to simulate carbon assimilation and typically rely on empirical estimates, including an assumed dependence on leaf nitrogen determined from soil fertility. In contrast, new theory, based on biochemical coordination and co-optimization of carboxylation and water costs for photosynthesis, suggests that optimal V-cmax can be predicted from climate alone, irrespective of soil fertility. Here, we develop this theory and find it captures 64% of observed variability in a global, field-measured V-cmax dataset for C-3 plants. Soil fertility indices explained substantially less variation (32%). These results indicate that environmentally regulated biophysical constraints and light availability are the first-order drivers of global photosynthetic capacity. Through acclimation and adaptation, plants efficiently utilize resources at the leaf level, thus maximizing potential resource use for growth and reproduction. Our theory offers a robust strategy for dynamically predicting photosynthetic capacity in ESMs

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

Summary: Leaf dark respiration (R dark ) is an important yet poorly quantified component of the global carbon cycle. Given this, we analyzed a new global database of R dark 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 R dark . Area-based R dark 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, R dark at a standard T (25°C, R dark 25 ) 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 R dark 25 at a given photosynthetic capacity (V cmax 25 ) or leaf nitrogen concentration ([N]) than species at warmer sites. R dark 25 values at any given V cmax 25 or [N] were higher in herbs than in woody plants. The results highlight variation in R dark 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 R dark in terrestrial biosphere models (TBMs) and associated land-surface components of Earth system models (ESMs). © 2015 New Phytologist Trust

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

Leaf dark respiration (R-dark) is an important yet poorly quantified component of the global carbon cycle. Given this, we analyzed a new global database of R-dark 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 R-dark. Area-based R-dark at the prevailing average daily growth temperature (T) of each siteincreased only twofold from the Arctic to the tropics, despite a 20 degrees C increase in growing T (8-28 degrees C). By contrast, R-dark at a standard T (25 degrees C, R-dark(25)) 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 R-dark(25) at a given photosynthetic capacity (V-cmax(25)) or leaf nitrogen concentration ([N]) than species at warmer sites. R-dark(25) values at any given V-cmax(25) or [N] were higher in herbs than in woody plants. The results highlight variation in R-dark 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 R-dark in terrestrial biosphere models (TBMs) and associated land-surface components of Earth system models (ESMs)