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

Predicting resilience through the lens of competing adjustments to vegetation function

There is a pressing need to better understand ecosystem resilience to droughts and heatwaves. Eco-evolutionary optimization approaches have been proposed as means to build this understanding in land surface models and improve their predictive capability, but competing approaches are yet to be tested together. Here, we coupled approaches that optimize canopy gas exchange and leaf nitrogen investment, respectively, extending both approaches to account for hydraulic impairment. We assessed model predictions using observations from a native Eucalyptus woodland that experienced repeated droughts and heatwaves between 2013 and 2020, whilst exposed to an elevated [CO2] treatment. Our combined approaches improved predictions of transpiration and enhanced the simulated magnitude of the CO2 fertilization effect on gross primary productivity. The competing approaches also worked consistently along axes of change in soil moisture, leaf area, and [CO2]. Despite predictions of a significant percentage loss of hydraulic conductivity due to embolism (PLC) in 2013, 2014, 2016, and 2017 (99th percentile PLC > 45%), simulated hydraulic legacy effects were small and short-lived (2 months). Our analysis suggests that leaf shedding and/or suppressed foliage growth formed a strategy to mitigate drought risk. Accounting for foliage responses to water availability has the potential to improve model predictions of ecosystem resilience. © 2022 The Authors. Plant, Cell & Environment published by John Wiley & Sons Ltd.MEBS, MDK, and AJP acknowledge support from the Australian Research Council (ARC) Centre of Excellence for Climate Extremes (CE170100023). MEBS was also supported by the UNSW Scientia PhD Scholarship Scheme. MDK and AJP acknowledge support from the ARC Discovery Grant (DP190101823) and MDK also acknowledges Eucalypt Australia and the NSW Research Attraction and Acceleration Program, which separately supported the EucFACE infrastructure. 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. BEM acknowledges support from the ARC Laureate Fellowship FL190100003. Finally, we thank the Editor, Dr Danielle Way, and two anonymous reviewers for their constructive comments. Open access publishing facilitated by University of New South Wales, as part of the Wiley - University of New South Wales agreement via the Council of Australian University Librarians. All model, analysis code, and data files are freely available from https://doi.org/10.5281/zenodo.6717290 (Sabot, 2022) and the code is also available from https://github.com/ManonSabot/Competing_Optimal_Adjustments. Previously published data sets used in this study can be accessed at: http://doi.org/10.4225/35/563159f223739 (Duursma et al., 2016). http://doi.org/10.4225/35/57ec5d4a2b78e (Ellsworth et al., 2017). http://doi.org/10.4225/35/55b6e313444ff (Gimeno et al., 2016). http://doi.org/10.4225/35/5ab9bd1e2f4fb (Gimeno et al., 2018). MEBS, MDK, and AJP acknowledge support from the Australian Research Council (ARC) Centre of Excellence for Climate Extremes (CE170100023). MEBS was also supported by the UNSW Scientia PhD Scholarship Scheme. MDK and AJP acknowledge support from the ARC Discovery Grant (DP190101823) and MDK also acknowledges Eucalypt Australia and the NSW Research Attraction and Acceleration Program, which separately supported the EucFACE infrastructure. 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. BEM acknowledges support from the ARC Laureate Fellowship FL190100003. Finally, we thank the Editor, Dr Danielle Way, and two anonymous reviewers for their constructive comments. Open access publishing facilitated by University of New South Wales, as part of the Wiley ‐ University of New South Wales agreement via the Council of Australian University Librarians

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

The concentration of ascorbic acid and glutathione in 13 provenances of Acacia melanoxylon

Climate change can negatively affect sensitive tree species, affecting their acclimation and adaptation strategies. A common garden experiment provides an opportunity to test whether responses of trees from different provenances are genetically driven and if this response is related to factors at the site of origin. We hypothesized that antioxidative defence systems and leaf mass area of Acacia melanoxylon R. Br. samples collected from different provenances will vary depending on local rainfall. Thirteen provenances of A. melanoxylon originating from different rainfall habitats (500-2000 mm) were grown for 5 years in a common garden. For 2 years, phyllode samples were collected during winter and summer, for measurements of leaf mass area and concentrations of glutathione and ascorbic acid. Leaf mass area varied between seasons, years and provenances of A. melanoxylon, and an increase was associated with decreasing rainfall at the site of origin. Ascorbic acid and glutathione concentrations varied between seasons, years (i.e., environmental factors) and among provenances of A. melanoxylon. In general, glutathione and ascorbic acid concentrations were higher in winter compared with summer. Ascorbic acid and glutathione were different among provenances, but this was not associated with rainfall at the site of origin. © 2016 The Author

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

Predicting resilience through the lens of competing adjustments to vegetation function

There is a pressing need to better understand ecosystem resilience to droughts and heatwaves. Eco-evolutionary optimization approaches have been proposed as means to build this understanding in land surface models and improve their predictive capability, but competing approaches are yet to be tested together. Here, we coupled approaches that optimize canopy gas exchange and leaf nitrogen investment, respectively, extending both approaches to account for hydraulic impairment. We assessed model predictions using observations from a native Eucalyptus woodland that experienced repeated droughts and heatwaves between 2013 and 2020, whilst exposed to an elevated [CO2] treatment. Our combined approaches improved predictions of transpiration and enhanced the simulated magnitude of the CO2 fertilization effect on gross primary productivity. The competing approaches also worked consistently along axes of change in soil moisture, leaf area, and [CO2]. Despite predictions of a significant percentage loss of hydraulic conductivity due to embolism (PLC) in 2013, 2014, 2016, and 2017 (99th percentile PLC > 45%), simulated hydraulic legacy effects were small and short-lived (2 months). Our analysis suggests that leaf shedding and/or suppressed foliage growth formed a strategy to mitigate drought risk. Accounting for foliage responses to water availability has the potential to improve model predictions of ecosystem resilience

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 (C-a) 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 Ca (eC(a)), 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 CO2 enrichment (the EucFACE experiment). In this experiment, light-saturated leaf photosynthesis increased by 19% in response to a 38% increase in C-a. 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 eC(a). We assessed the direct impact of eC(a), as well as the indirect effect of photosynthetic acclimation to eC(a) and variability among treatment plots using different model scenarios. At the canopy scale, MAESPA estimated a GPP of 1574 gCm(-2) yr(-1) under ambient conditions across 4 years and a direct increase in the GPP of C11% in response to eC(a). 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 10 %. After taking the baseline variability in the leaf area index across plots in account, we estimated a field GPP response to eC(a) of 6% with a 95% confidence interval (-2 %, 14 %). These findings highlight that the GPP response of mature forests to eC(a) is likely to be considerably lower than the response of light-saturated leaf photosynthesis. Our results provide an important context for interpreting the eC(a) responses of other components of the ecosystem carbon cycle

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 (Ca) 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 Ca (eCa), 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 CO2 enrichment (the EucFACE experiment). In this experiment, light-saturated leaf photosynthesis increased by 19 % in response to a 38 % increase in Ca. 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 eCa. We assessed the direct impact of eCa, as well as the indirect effect of photosynthetic acclimation to eCa and variability among treatment plots using different model scenarios. At the canopy scale, MAESPA estimated a GPP of 1574 g C m−2 yr−1 under ambient conditions across 4 years and a direct increase in the GPP of +11 % in response to eCa. 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 10 %. After taking the baseline variability in the leaf area index across plots in account, we estimated a field GPP response to eCa of 6 % with a 95 % confidence interval (−2 %, 14 %). These findings highlight that the GPP response of mature forests to eCa is likely to be considerably lower than the response of light-saturated leaf photosynthesis. Our results provide an important context for interpreting the eCa responses of other components of the ecosystem carbon cycle

Seedlings of two Acacia species from contrasting habitats show different photoprotective and antioxidative responses to drought and heatwaves

International audienceAbstractKey messageTwoAcaciaspecies adapted to contrasting habitats showed different response of photoprotective and antioxidative defence systems to imposed drought and heatwave.ContextPredicted increases in drought frequency and intense heatwaves are expected to lead to dieback of sensitive tree species. Stomatal closure restricts CO2 input into the leaf, resulting in imbalances between light energy-driven electron transport rate and electron consumption in the Calvin cycle. Reactive oxygen species formed under these circumstances have to be kept under control by photoprotective and antioxidative defence systems.AimsWe hypothesised that these defence systems behave differently in tree species from contrasting habitats.MethodsAcacia aneura (adapted to arid habitats) and Acacia melanoxylon (adapted to humid habitats) were exposed to two water treatments for 50 days including two short heatwave periods. Responses were assessed by gas exchange, chlorophyll fluorescence and concentrations of antioxidants (phyllodes, roots).ResultsPhotosynthesis and quantum yield of photochemistry decreased significantly in both Acacia species, especially after water was withheld in combination with the second heatwave episode. In phyllodes, the concentration of antioxidants remained unchanged until exposure to severe drought and heatwave conditions (except for A. melanoxylon where changes in glutathione concentration were observed prior to exposure to severe stress), but after water was withheld and the second heatwave occurred, oxidised forms of glutathione increased. After exposure to the second heatwave, well-watered seedlings of A. melanoxylon but not A. aneura increased ascorbic acid concentration in phyllodes. Under well-watered conditions, Acacia species also showed increased concentration of antioxidants in roots following heatwaves.ConclusionsBoth Acacia species showed photodamage to photosystem II (PSII) after water was withheld and the second heatwave imposed, but with more gradual response in A. aneura. Total concentration of investigated antioxidants increased in response to the first (A. melanoxylon) and second (A. aneura) heatwaves rather than drought stress alone