Carbon-phosphorus cycle models overestimate CO2 enrichment response in a mature Eucalyptus forest.

The importance of phosphorus (P) in regulating ecosystem responses to climate change has fostered P-cycle implementation in land surface models, but their CO2 effects predictions have not been evaluated against measurements. Here, we perform a data-driven model evaluation where simulations of eight widely used P-enabled models were confronted with observations from a long-term free-air CO2 enrichment experiment in a mature, P-limited Eucalyptus forest. We show that most models predicted the correct sign and magnitude of the CO2 effect on ecosystem carbon (C) sequestration, but they generally overestimated the effects on plant C uptake and growth. We identify leaf-to-canopy scaling of photosynthesis, plant tissue stoichiometry, plant belowground C allocation, and the subsequent consequences for plant-microbial interaction as key areas in which models of ecosystem C-P interaction can be improved. Together, this data-model intercomparison reveals data-driven insights into the performance and functionality of P-enabled models and adds to the existing evidence that the global CO2-driven carbon sink is overestimated by models.

Environmental correlates of the forest carbon distribution in the Central Himalayas.

Understanding the biophysical limitations on forest carbon across diverse ecological regions is crucial for accurately assessing and managing forest carbon stocks. This study investigates the role of climate and disturbance on the spatial variation of two key forest carbon pools: aboveground carbon (AGC) and soil organic carbon (SOC). Using plot-level carbon pool estimates from Nepal's national forest inventory and structural equation modelling, we explore the relationship of forest carbon stocks to broad-scale climatic water and energy availability and fine-scale terrain and disturbance. The forest AGC and SOC models explained 25% and 59% of the observed spatial variation in forest AGC and SOC, respectively. Among the evaluated variables, disturbance exhibited the strongest negative correlation with AGC, while the availability of climatic energy demonstrated the strongest negative correlation with SOC. Disturbances such as selective logging and firewood collection result in immediate forest carbon loss, while soil carbon changes take longer to respond. The lower decomposition rates in the high-elevation region, due to lower temperatures, preserve organic matter and contribute to the high SOC stocks observed there. These results highlight the critical role of climate and disturbance regimes in shaping landscape patterns of forest carbon stocks. Understanding the underlying drivers of these patterns is crucial for forest carbon management and conservation across diverse ecological zones including the Central Himalayas.

Microbial competition for phosphorus limits the CO2 response of a mature forest.

The capacity for terrestrial ecosystems to sequester additional carbon (C) with rising CO2 concentrations depends on soil nutrient availability1,2. Previous evidence suggested that mature forests growing on phosphorus (P)-deprived soils had limited capacity to sequester extra biomass under elevated CO2 (refs. 3-6), but uncertainty about ecosystem P cycling and its CO2 response represents a crucial bottleneck for mechanistic prediction of the land C sink under climate change7. Here, by compiling the first comprehensive P budget for a P-limited mature forest exposed to elevated CO2, we show a high likelihood that P captured by soil microorganisms constrains ecosystem P recycling and availability for plant uptake. Trees used P efficiently, but microbial pre-emption of mineralized soil P seemed to limit the capacity of trees for increased P uptake and assimilation under elevated CO2 and, therefore, their capacity to sequester extra C. Plant strategies to stimulate microbial P cycling and plant P uptake, such as increasing rhizosphere C release to soil, will probably be necessary for P-limited forests to increase C capture into new biomass. Our results identify the key mechanisms by which P availability limits CO2 fertilization of tree growth and will guide the development of Earth system models to predict future long-term C storage.

The AusTraits plant dictionary.

Traits with intuitive names, a clear scope and explicit description are essential for all trait databases. The lack of unified, comprehensive, and machine-readable plant trait definitions limits the utility of trait databases, including reanalysis of data from a single database, or analyses that integrate data across multiple databases. Both can only occur if researchers are confident the trait concepts are consistent within and across sources. Here we describe the AusTraits Plant Dictionary (APD), a new data source of terms that extends the trait definitions included in a recent trait database, AusTraits. The development process of the APD included three steps: review and formalisation of the scope of each trait and the accompanying trait description; addition of trait metadata; and publication in both human and machine-readable forms. Trait definitions include keywords, references, and links to related trait concepts in other databases, enabling integration of AusTraits with other sources. The APD will both improve the usability of AusTraits and foster the integration of trait data across global and regional plant trait databases.

Optimal Carbon Storage During Drought.

Allocation of non-structural carbohydrates (NSC) to storage allows plants to maintain a carbon pool in anticipation of future stress. However, to do so, plants must forego use of the carbon for growth, creating a trade-off between storage and growth. It is possible that plants actively regulate the storage pool to maximise fitness in a stress-prone environment. Here, we attempt to identify the patterns of growth and storage that would result during drought stress under the hypothesis that plants actively regulate carbon storage. We use optimal control theory to calculate the optimal allocation to storage and utilisation of stored carbon over a single drought stress period. We examine two fitness objectives representing alternative life strategies: prioritisation of growth (MaxM) and prioritisation of storage (MaxS), as well as strategies in between these extremes. We find that optimal carbon storage consists of three discrete phases: 'growth', 'storage without growth', and the 'stress' phase where there is no carbon source. This trajectory can be defined by the time point when the plant switches from growth to storage. Growth-prioritising plants switch later and fully deplete their stored carbon over the stress period, while storage-prioritising plants either do not grow or switch early in the drought period. The switch time almost always occurs before soil water is depleted, meaning that growth stops before photosynthesis. We conclude that the common observation of increasing carbon storage during drought could be interpreted as an active process that optimises plant performance during stress.

Higher global gross primary productivity under future climate with more advanced representations of photosynthesis.

Gross primary productivity (GPP) is the key determinant of land carbon uptake, but its representation in terrestrial biosphere models (TBMs) does not reflect our latest physiological understanding. We implemented three empirically well supported but often omitted mechanisms into the TBM CABLE-POP: photosynthetic temperature acclimation, explicit mesophyll conductance, and photosynthetic optimization through redistribution of leaf nitrogen. We used the RCP8.5 climate scenario to conduct factorial model simulations characterizing the individual and combined effects of the three mechanisms on projections of GPP. Simulated global GPP increased more strongly (up to 20% by 2070-2099) in more comprehensive representations of photosynthesis compared to the model lacking the three mechanisms. The experiments revealed non-additive interactions among the mechanisms as combined effects were stronger than the sum of the individual effects. The modeled responses are explained by changes in the photosynthetic sensitivity to temperature and CO2 caused by the added mechanisms. Our results suggest that current TBMs underestimate GPP responses to future CO2 and climate conditions.

Decoupling between stomatal conductance and photosynthesis occurs under extreme heat in broadleaf tree species regardless of water access.

High air temperatures increase atmospheric vapor pressure deficit (VPD) and the severity of drought, threatening forests worldwide. Plants regulate stomata to maximize carbon gain and minimize water loss, resulting in a close coupling between net photosynthesis (Anet ) and stomatal conductance (gs ). However, evidence for decoupling of gs from Anet under extreme heat has been found. Such a response both enhances survival of leaves during heat events but also quickly depletes available water. To understand the prevalence and significance of this decoupling, we measured leaf gas exchange in 26 tree and shrub species growing in the glasshouse or at an urban site in Sydney, Australia on hot days (maximum Tair > 40°C). We hypothesized that on hot days plants with ample water access would exhibit reduced Anet and use transpirational cooling leading to stomatal decoupling, whereas plants with limited water access would rely on other mechanisms to avoid lethal temperatures. Instead, evidence for stomatal decoupling was found regardless of plant water access. Transpiration of well-watered plants was 23% higher than model predictions during heatwaves, which effectively cooled leaves below air temperature. For hotter, droughted plants, the increase in transpiration during heatwaves was even more pronounced-gs was 77% higher than model predictions. Stomatal decoupling was found for most broadleaf evergreen and broadleaf deciduous species at the urban site, including some wilted trees with limited water access. Decoupling may simply be a passive consequence of the physical effects of high temperature on plant leaves through increased cuticular conductance of water vapor, or stomatal decoupling may be an adaptive response that is actively regulated by stomatal opening under high temperatures. This temperature response is not yet included in any land surface model, suggesting that model predictions of evapotranspiration may be underpredicted at high temperature and high VPD.

Mapping soil organic carbon stocks in Nepal's forests.

Comprehensive forest carbon accounting requires reliable estimation of soil organic carbon (SOC) stocks. Despite being an important carbon pool, limited information is available on SOC stocks in global forests, particularly for forests in mountainous regions, such as the Central Himalayas. The availability of consistently measured new field data enabled us to accurately estimate forest soil organic carbon (SOC) stocks in Nepal, addressing a previously existing knowledge gap. Our method involved modelling plot-based estimates of forest SOC using covariates related to climate, soil, and topographic position. Our quantile random forest model resulted in the high spatial resolution prediction of Nepal's national forest SOC stock together with prediction uncertainties. Our spatially explicit forest SOC map showed the high SOC levels in high-elevation forests and a significant underrepresentation of these stocks in global-scale assessments. Our results offer an improved baseline on the distribution of total carbon in the forests of the Central Himalayas. The benchmark maps of predicted forest SOC and associated errors, along with our estimate of 494 million tonnes (SE = 16) of total SOC in the topsoil (0-30 cm) of forested areas in Nepal, carry important implications for understanding the spatial variability of forest SOC in mountainous regions with complex terrains.

Optimal stomatal theory predicts CO2 responses of stomatal conductance in both gymnosperm and angiosperm trees.

Optimal stomatal theory predicts that stomata operate to maximise photosynthesis (Anet ) and minimise transpirational water loss to achieve optimal intrinsic water-use efficiency (iWUE). We tested whether this theory can predict stomatal responses to elevated atmospheric CO2 (eCO2 ), and whether it can capture differences in responsiveness among woody plant functional types (PFTs). We conducted a meta-analysis of tree studies of the effect of eCO2 on iWUE and its components Anet and stomatal conductance (gs ). We compared three PFTs, using the unified stomatal optimisation (USO) model to account for confounding effects of leaf-air vapour pressure difference (D). We expected smaller gs , but greater Anet , responses to eCO2 in gymnosperms compared with angiosperm PFTs. We found that iWUE increased in proportion to increasing eCO2 in all PFTs, and that increases in Anet had stronger effects than reductions in gs . The USO model correctly captured stomatal behaviour with eCO2 across most datasets. The chief difference among PFTs was a lower stomatal slope parameter (g1 ) for the gymnosperm, compared with angiosperm, species. Land surface models can use the USO model to describe stomatal behaviour under changing atmospheric CO2 conditions.

Canopy dieback and recovery in Australian native forests following extreme drought.

In 2019, south-eastern Australia experienced its driest and hottest year on record, resulting in massive canopy dieback events in eucalypt dominated forests. A subsequent period of high precipitation in 2020 provided a rare opportunity to quantify the impacts of extreme drought and consequent recovery. We quantified canopy health and hydraulic impairment (native percent loss of hydraulic conductivity, PLC) of 18 native tree species growing at 15 sites that were heavily impacted by the drought both during and 8-10 months after the drought. Most species exhibited high PLC during drought (PLC:65.1 ± 3.3%), with no clear patterns across sites or species. Heavily impaired trees (PLC > 70%) showed extensive canopy browning. In the post-drought period, most surviving trees exhibited hydraulic recovery (PLC:26.1 ± 5.1%), although PLC remained high in some trees (50-70%). Regained hydraulic function (PLC < 50%) corresponded to decreased canopy browning indicating improved tree health. Similar drought (37.1 ± 4.2%) and post-drought (35.1 ± 4.4%) percentages of basal area with dead canopy suggested that trees with severely compromised canopies immediately after drought were not able to recover. This dataset provides insights into the impacts of severe natural drought on the health of mature trees, where hydraulic failure is a major contributor in canopy dieback and tree mortality during extreme drought events.

Convergence in phosphorus constraints to photosynthesis in forests around the world.

Tropical forests take up more carbon (C) from the atmosphere per annum by photosynthesis than any other type of vegetation. Phosphorus (P) limitations to C uptake are paramount for tropical and subtropical forests around the globe. Yet the generality of photosynthesis-P relationships underlying these limitations are in question, and hence are not represented well in terrestrial biosphere models. Here we demonstrate the dependence of photosynthesis and underlying processes on both leaf N and P concentrations. The regulation of photosynthetic capacity by P was similar across four continents. Implementing P constraints in the ORCHIDEE-CNP model, gross photosynthesis was reduced by 36% across the tropics and subtropics relative to traditional N constraints and unlimiting leaf P. Our results provide a quantitative relationship for the P dependence for photosynthesis for the front-end of global terrestrial C models that is consistent with canopy leaf measurements.

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.

The Role of Hydraulic Failure in a Massive Mangrove Die-Off Event.

Between late 2015 and early 2016, more than 7,000 ha of mangrove forest died along the coastline of the Gulf of Carpentaria, in northern Australia. This massive die-off was preceded by a strong 2015/2016 El Niño event, resulting in lower precipitation, a drop in sea level and higher than average temperatures in northern Australia. In this study, we investigated the role of hydraulic failure in the mortality and recovery of the dominant species, Avicennia marina, 2 years after the mortality event. We measured predawn water potential (Ψpd) and percent loss of stem hydraulic conductivity (PLC) in surviving individuals across a gradient of impact. We also assessed the vulnerability to drought-induced embolism (Ψ50) for the species. Areas with severe canopy dieback had higher native PLC (39%) than minimally impacted areas (6%), suggesting that hydraulic recovery was ongoing. The high resistance of A. marina to water-stress-induced embolism (Ψ50 = -9.6 MPa), indicates that severe water stress (Ψpd < -10 MPa) would have been required to cause mortality in this species. Our data indicate that the natural gradient of water-stress enhanced the impact of El Niño, leading to hydraulic failure and mortality in A. marina growing on severely impacted (SI) zones. It is likely that lowered sea levels and less frequent inundation by seawater, combined with lower inputs of fresh water, high evaporative demand and high temperatures, led to the development of hyper-salinity and extreme water stress during the 2015/16 summer.

Towards species-level forecasts of drought-induced tree mortality risk.

Predicting species-level responses to drought at the landscape scale is critical to reducing uncertainty in future terrestrial carbon and water cycle projections. We embedded a stomatal optimisation model in the Community Atmosphere Biosphere Land Exchange (CABLE) land surface model and parameterised the model for 15 canopy dominant eucalypt tree species across South-Eastern Australia (mean annual precipitation range: 344-1424 mm yr-1 ). We conducted three experiments: applying CABLE to the 2017-2019 drought; a 20% drier drought; and a 20% drier drought with a doubling of atmospheric carbon dioxide (CO2 ). The severity of the drought was highlighted as for at least 25% of their distribution ranges, 60% of species experienced leaf water potentials beyond the water potential at which 50% of hydraulic conductivity is lost due to embolism. We identified areas of severe hydraulic stress within-species' ranges, but we also pinpointed resilience in species found in predominantly semiarid areas. The importance of the role of CO2 in ameliorating drought stress was consistent across species. Our results represent an important advance in our capacity to forecast the resilience of individual tree species, providing an evidence base for decision-making around the resilience of restoration plantings or net-zero emission strategies.

Tropical rainforest species have larger increases in temperature optima with warming than warm-temperate rainforest trees.

While trees can acclimate to warming, there is concern that tropical rainforest species may be less able to acclimate because they have adapted to a relatively stable thermal environment. Here we tested whether the physiological adjustments to warming differed among Australian tropical, subtropical and warm-temperate rainforest trees. Photosynthesis and respiration temperature responses were quantified in six Australian rainforest seedlings of tropical, subtropical and warm-temperate climates grown across four growth temperatures in a glasshouse. Temperature-response models were fitted to identify mechanisms underpinning the response to warming. Tropical and subtropical species had higher temperature optima for photosynthesis (ToptA ) than temperate species. There was acclimation of ToptA to warmer growth temperatures. The rate of acclimation (0.35-0.78°C °C-1 ) was higher in tropical and subtropical than in warm-temperate trees and attributed to differences in underlying biochemical parameters, particularly increased temperature optima of Vcmax25 and Jmax25 . The temperature sensitivity of respiration (Q10 ) was 24% lower in tropical and subtropical compared with warm-temperate species. Overall, tropical and subtropical species had a similar capacity to acclimate to changes in growth temperature as warm-temperate species, despite being grown at higher temperatures. Quantifying the physiological acclimation in rainforests can improve accuracy of future climate predictions and assess their potential vulnerability to warming.

Bridge to the future: Important lessons from 20 years of ecosystem observations made by the OzFlux network.

In 2020, the Australian and New Zealand flux research and monitoring network, OzFlux, celebrated its 20th anniversary by reflecting on the lessons learned through two decades of ecosystem studies on global change biology. OzFlux is a network not only for ecosystem researchers, but also for those 'next users' of the knowledge, information and data that such networks provide. Here, we focus on eight lessons across topics of climate change and variability, disturbance and resilience, drought and heat stress and synergies with remote sensing and modelling. In distilling the key lessons learned, we also identify where further research is needed to fill knowledge gaps and improve the utility and relevance of the outputs from OzFlux. Extreme climate variability across Australia and New Zealand (droughts and flooding rains) provides a natural laboratory for a global understanding of ecosystems in this time of accelerating climate change. As evidence of worsening global fire risk emerges, the natural ability of these ecosystems to recover from disturbances, such as fire and cyclones, provides lessons on adaptation and resilience to disturbance. Drought and heatwaves are common occurrences across large parts of the region and can tip an ecosystem's carbon budget from a net CO2 sink to a net CO2 source. Despite such responses to stress, ecosystems at OzFlux sites show their resilience to climate variability by rapidly pivoting back to a strong carbon sink upon the return of favourable conditions. Located in under-represented areas, OzFlux data have the potential for reducing uncertainties in global remote sensing products, and these data provide several opportunities to develop new theories and improve our ecosystem models. The accumulated impacts of these lessons over the last 20 years highlights the value of long-term flux observations for natural and managed systems. A future vision for OzFlux includes ongoing and newly developed synergies with ecophysiologists, ecologists, geologists, remote sensors and modellers.

High safety margins to drought-induced hydraulic failure found in five pasture grasses.

Determining the relationship between reductions in stomatal conductance (gs ) and leaf water transport during dehydration is key to understanding plant drought responses. While numerous studies have analysed the hydraulic function of woody species, minimal research has been conducted on grasses. Here, we sought to characterize hydraulic vulnerability in five widely-occurring pasture grasses (including both C3 and C4 grasses) and determine whether reductions in gs and leaf hydraulic conductance (Kleaf ) during dehydration could be attributed to xylem embolism. Using the optical vulnerability (OV) technique, we found that all species were highly resistant to xylem embolism when compared to other herbaceous angiosperms, with 50% xylem embolism (PX50 ) occurring at xylem pressures ranging from -4.4 to -6.1 MPa. We observed similar reductions in gs and Kleaf under mild water stress for all species, occurring well before PX50 . The onset of xylem embolism (PX12 ) occurred consistently after stomatal closure and 90% reduction of Kleaf . Our results suggest that factors other than xylem embolism are responsible for the majority of reductions in gs and Kleaf during drought and reductions in the productivity of pasture species under moderate drought may not be driven by embolism.

Pastures and Climate Extremes: Impacts of Cool Season Warming and Drought on the Productivity of Key Pasture Species in a Field Experiment.

Shifts in the timing, intensity and/or frequency of climate extremes, such as severe drought and heatwaves, can generate sustained shifts in ecosystem function with important ecological and economic impacts for rangelands and managed pastures. The Pastures and Climate Extremes experiment (PACE) in Southeast Australia was designed to investigate the impacts of a severe winter/spring drought (60% rainfall reduction) and, for a subset of species, a factorial combination of drought and elevated temperature (ambient +3°C) on pasture productivity. The experiment included nine common pasture and Australian rangeland species from three plant functional groups (C3 grasses, C4 grasses and legumes) planted in monoculture. Winter/spring drought resulted in productivity declines of 45% on average and up to 74% for the most affected species (Digitaria eriantha) during the 6-month treatment period, with eight of the nine species exhibiting significant yield reductions. Despite considerable variation in species' sensitivity to drought, C4 grasses were more strongly affected by this treatment than C3 grasses or legumes. Warming also had negative effects on cool-season productivity, associated at least partially with exceedance of optimum growth temperatures in spring and indirect effects on soil water content. The combination of winter/spring drought and year-round warming resulted in the greatest yield reductions. We identified responses that were either additive (Festuca), or less-than-additive (Medicago), where warming reduced the magnitude of drought effects. Results from this study highlight the sensitivity of diverse pasture species to increases in winter and spring drought severity similar to those predicted for this region, and that anticipated benefits of cool-season warming are unlikely to be realized. Overall, the substantial negative impacts on productivity suggest that future, warmer, drier climates will result in shortfalls in cool-season forage availability, with profound implications for the livestock industry and natural grazer communities.

Mechanisms of xylem hydraulic recovery after drought in Eucalyptus saligna.

The mechanisms by which woody plants recover xylem hydraulic capacity after drought stress are not well understood, particularly with regard to the role of embolism refilling. We evaluated the recovery of xylem hydraulic capacity in young Eucalyptus saligna plants exposed to cycles of drought stress and rewatering. Plants were exposed to moderate and severe drought stress treatments, with recovery monitored at time intervals from 24 h to 6 months after rewatering. The percentage loss of xylem vessels due to embolism (PLV) was quantified at each time point using microcomputed tomography with stem water potential (Ψx ) and canopy transpiration (Ec ) measured before scans. Plants exposed to severe drought stress suffered high levels of embolism (47.38% ± 10.97% PLV) and almost complete canopy loss. No evidence of embolism refilling was observed at 24 h, 1 week, or 3 weeks after rewatering despite rapid recovery in Ψx . Recovery of hydraulic capacity was achieved over a 6-month period by growth of new xylem tissue, with canopy leaf area and Ec recovering over the same period. These findings indicate that E. saligna recovers slowly from severe drought stress, with potential for embolism to persist in the xylem for many months after rainfall events.

Adaptive plasticity in plant traits increases time to hydraulic failure under drought in a foundation tree.

The viability of forest trees, in response to climate change-associated drought, will depend on their capacity to survive through genetic adaptation and phenotypic plasticity in drought tolerance traits. Genotypes with enhanced plasticity for drought tolerance (adaptive plasticity) will have a greater ability to persist and delay the onset of hydraulic failure. By examining populations from different climate-origins grown under contrasting soil water availability, we tested for genotype (G), environment (E) and genotype-by-environment (G × E) effects on traits that determine the time it takes for saplings to desiccate from stomatal closure to 88% loss of stem hydraulic conductance (time to hydraulic failure, THF). Specifically, we hypothesized that: (i) THF is dependent on a G × E interaction, with longer THF for warm, dry climate populations in response to chronic water deficit treatment compared with cool, wet populations, and (ii) hydraulic and allometric traits explain the observed patterns in THF. Corymbia calophylla saplings from two populations originating from contrasting climates (warm-dry or cool-wet) were grown under well-watered and chronic soil water deficit treatments in large containers. Hydraulic and allometric traits were measured and then saplings were dried-down to critical levels of drought stress to estimate THF. Significant plasticity was detected in the warm-dry population in response to water-deficit, with enhanced drought tolerance compared with the cool-wet population. Projected leaf area and total plant water storage showed treatment variation, and minimum conductance showed significant population differences driving longer THF in trees from warm-dry origins grown in water-limited conditions. Our findings contribute information on intraspecific variation in key drought traits, including hydraulic and allometric determinants of THF. It highlights the need to quantify adaptive capacity in populations of forest trees in climate change-type drought to improve predictions of forest die-back.