Basin-wide variation in tree hydraulic safety margins predicts the carbon balance of Amazon forests.

Tropical forests face increasing climate risk1,2, yet our ability to predict their response to climate change is limited by poor understanding of their resistance to water stress. Although xylem embolism resistance thresholds (for example, [Formula: see text]50) and hydraulic safety margins (for example, HSM50) are important predictors of drought-induced mortality risk3-5, little is known about how these vary across Earth's largest tropical forest. Here, we present a pan-Amazon, fully standardized hydraulic traits dataset and use it to assess regional variation in drought sensitivity and hydraulic trait ability to predict species distributions and long-term forest biomass accumulation. Parameters [Formula: see text]50 and HSM50 vary markedly across the Amazon and are related to average long-term rainfall characteristics. Both [Formula: see text]50 and HSM50 influence the biogeographical distribution of Amazon tree species. However, HSM50 was the only significant predictor of observed decadal-scale changes in forest biomass. Old-growth forests with wide HSM50 are gaining more biomass than are low HSM50 forests. We propose that this may be associated with a growth-mortality trade-off whereby trees in forests consisting of fast-growing species take greater hydraulic risks and face greater mortality risk. Moreover, in regions of more pronounced climatic change, we find evidence that forests are losing biomass, suggesting that species in these regions may be operating beyond their hydraulic limits. Continued climate change is likely to further reduce HSM50 in the Amazon6,7, with strong implications for the Amazon carbon sink.

Direct evidence for phosphorus limitation on Amazon forest productivity.

The productivity of rainforests growing on highly weathered tropical soils is expected to be limited by phosphorus availability1. Yet, controlled fertilization experiments have been unable to demonstrate a dominant role for phosphorus in controlling tropical forest net primary productivity. Recent syntheses have demonstrated that responses to nitrogen addition are as large as to phosphorus2, and adaptations to low phosphorus availability appear to enable net primary productivity to be maintained across major soil phosphorus gradients3. Thus, the extent to which phosphorus availability limits tropical forest productivity is highly uncertain. The majority of the Amazonia, however, is characterized by soils that are more depleted in phosphorus than those in which most tropical fertilization experiments have taken place2. Thus, we established a phosphorus, nitrogen and base cation addition experiment in an old growth Amazon rainforest, with a low soil phosphorus content that is representative of approximately 60% of the Amazon basin. Here we show that net primary productivity increased exclusively with phosphorus addition. After 2 years, strong responses were observed in fine root (+29%) and canopy productivity (+19%), but not stem growth. The direct evidence of phosphorus limitation of net primary productivity suggests that phosphorus availability may restrict Amazon forest responses to CO2 fertilization4, with major implications for future carbon sequestration and forest resilience to climate change.

Author Correction: Soil carbon loss by experimental warming in a tropical forest.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Soil carbon loss by experimental warming in a tropical forest.

Tropical soils contain one-third of the carbon stored in soils globally1, so destabilization of soil organic matter caused by the warming predicted for tropical regions this century2 could accelerate climate change by releasing additional carbon dioxide (CO2) to the atmosphere3-6. Theory predicts that warming should cause only modest carbon loss from tropical soils relative to those at higher latitudes5,7, but there have been no warming experiments in tropical forests to test this8. Here we show that in situ experimental warming of a lowland tropical forest soil on Barro Colorado Island, Panama, caused an unexpectedly large increase in soil CO2 emissions. Two years of warming of the whole soil profile by four degrees Celsius increased CO2 emissions by 55 per cent compared to soils at ambient temperature. The additional CO2 originated from heterotrophic rather than autotrophic sources, and equated to a loss of 8.2 ± 4.2 (one standard error) tonnes of carbon per hectare per year from the breakdown of soil organic matter. During this time, we detected no acclimation of respiration rates, no thermal compensation or change in the temperature sensitivity of enzyme activities, and no change in microbial carbon-use efficiency. These results demonstrate that soil carbon in tropical forests is highly sensitive to warming, creating a potentially substantial positive feedback to climate change.

Variable thermal plasticity of leaf functional traits in Andean tropical montane forests.

Tropical montane forests (TMFs) are biodiversity hotspots and provide vital ecosystem services, but they are disproportionately vulnerable to climate warming. In the Andes, cold-affiliated species from high elevations are being displaced at the hot end of their thermal distributions by warm-affiliated species migrating upwards from lower elevations, leading to compositional shifts. Leaf functional traits are strong indicators of plant performance and at the community level have been shown to vary along elevation gradients, reflecting plant adaptations to different environmental niches. However, the plastic response of such traits to relatively rapid temperature change in Andean TMF species remains unknown. We used three common garden plantations within a thermosequence in the Colombian Andes to investigate the warming and cooling responses of key leaf functional traits in eight cold- and warm-affiliated species with variable thermal niches. Cold-affiliated species shifted their foliar nutrient concentrations when exposed to warming, while all other traits did not significantly change; contrastingly, warm-affiliated species were able to adjust structural, nutrient and water-use efficiency traits from acquisitive to conservative strategies in response to cooling. Our findings suggest that cold-affiliated species will struggle to acclimate functional traits to warming, conferring warm-affiliated species a competitive advantage under climate change.

New tree height allometries derived from terrestrial laser scanning reveal substantial discrepancies with forest inventory methods in tropical rainforests.

Tree allometric models, essential for monitoring and predicting terrestrial carbon stocks, are traditionally built on global databases with forest inventory measurements of stem diameter (D) and tree height (H). However, these databases often combine H measurements obtained through various measurement methods, each with distinct error patterns, affecting the resulting H:D allometries. In recent decades, terrestrial laser scanning (TLS) has emerged as a widely accepted method for accurate, non-destructive tree structural measurements. This study used TLS data to evaluate the prediction accuracy of forest inventory-based H:D allometries and to develop more accurate pantropical allometries. We considered 19 tropical rainforest plots across four continents. Eleven plots had forest inventory and RIEGL VZ-400(i) TLS-based D and H data, allowing accuracy assessment of local forest inventory-based H:D allometries. Additionally, TLS-based data from 1951 trees from all 19 plots were used to create new pantropical H:D allometries for tropical rainforests. Our findings reveal that in most plots, forest inventory-based H:D allometries underestimated H compared with TLS-based allometries. For 30-metre-tall trees, these underestimations varied from -1.6 m (-5.3%) to -7.5 m (-25.4%). In the Malaysian plot with trees reaching up to 77 m in height, the underestimation was as much as -31.7 m (-41.3%). We propose a TLS-based pantropical H:D allometry, incorporating maximum climatological water deficit for site effects, with a mean uncertainty of 19.1% and a mean bias of -4.8%. While the mean uncertainty is roughly 2.3% greater than that of the Chave2014 model, this model demonstrates more consistent uncertainties across tree size and delivers less biased estimates of H (with a reduction of 8.23%). In summary, recognizing the errors in H measurements from forest inventory methods is vital, as they can propagate into the allometries they inform. This study underscores the potential of TLS for accurate H and D measurements in tropical rainforests, essential for refining tree allometries.

Acclimation of photosynthetic capacity and foliar respiration in Andean tree species to temperature change.

Climate warming is causing compositional changes in Andean tropical montane forests (TMFs). These shifts are hypothesised to result from differential responses to warming of cold- and warm-affiliated species, with the former experiencing mortality and the latter migrating upslope. The thermal acclimation potential of Andean TMFs remains unknown. Along a 2000 m Andean altitudinal gradient, we planted individuals of cold- and warm-affiliated species (under common soil and irrigation), exposing them to the hot and cold extremes of their thermal niches, respectively. We measured the response of net photosynthesis (Anet ), photosynthetic capacity and leaf dark respiration (Rdark ) to warming/cooling, 5 months after planting. In all species, Anet and photosynthetic capacity at 25°C were highest when growing at growth temperatures (Tg ) closest to their thermal means, declining with warming and cooling in cold-affiliated and warm-affiliated species, respectively. When expressed at Tg , photosynthetic capacity and Rdark remained unchanged in cold-affiliated species, but the latter decreased in warm-affiliated counterparts. Rdark at 25°C increased with temperature in all species, but remained unchanged when expressed at Tg . Both species groups acclimated to temperature, but only warm-affiliated species decreased Rdark to photosynthetic capacity ratio at Tg as temperature increased. This could confer them a competitive advantage under future warming.

Vapour pressure deficit modulates hydraulic function and structure of tropical rainforests under nonlimiting soil water supply.

Atmospheric conditions are expected to become warmer and drier in the future, but little is known about how evaporative demand influences forest structure and function independently from soil moisture availability, and how fast-response variables (such as canopy water potential and stomatal conductance) may mediate longer-term changes in forest structure and function in response to climate change. We used two tropical rainforest sites with different temperatures and vapour pressure deficits (VPD), but nonlimiting soil water supply, to assess the impact of evaporative demand on ecophysiological function and forest structure. Common species between sites allowed us to test the extent to which species composition, relative abundance and intraspecific variability contributed to site-level differences. The highest VPD site had lower midday canopy water potentials, canopy conductance (gc ), annual transpiration, forest stature, and biomass, while the transpiration rate was less sensitive to changes in VPD; it also had different height-diameter allometry (accounting for 51% of the difference in biomass between sites) and higher plot-level wood density. Our findings suggest that increases in VPD, even in the absence of soil water limitation, influence fast-response variables, such as canopy water potentials and gc , potentially leading to longer-term changes in forest stature resulting in reductions in biomass.

Rooting depth and xylem vulnerability are independent woody plant traits jointly selected by aridity, seasonality, and water table depth.

Evolutionary radiations of woody taxa within arid environments were made possible by multiple trait innovations including deep roots and embolism-resistant xylem, but little is known about how these traits have coevolved across the phylogeny of woody plants or how they jointly influence the distribution of species. We synthesized global trait and vegetation plot datasets to examine how rooting depth and xylem vulnerability across 188 woody plant species interact with aridity, precipitation seasonality, and water table depth to influence species occurrence probabilities across all biomes. Xylem resistance to embolism and rooting depth are independent woody plant traits that do not exhibit an interspecific trade-off. Resistant xylem and deep roots increase occurrence probabilities in arid, seasonal climates over deep water tables. Resistant xylem and shallow roots increase occurrence probabilities in arid, nonseasonal climates over deep water tables. Vulnerable xylem and deep roots increase occurrence probabilities in arid, nonseasonal climates over shallow water tables. Lastly, vulnerable xylem and shallow roots increase occurrence probabilities in humid climates. Each combination of trait values optimizes occurrence probabilities in unique environmental conditions. Responses of deeply rooted vegetation may be buffered if evaporative demand changes faster than water table depth under climate change.

Ghosts of dry seasons past: Legacy of severe drought enhances mangrove salinity tolerance through coordinated cellular osmotic and elastic adjustments.

The incidence and severity of global mangrove mortality due to drought is increasing. Yet, little is understood of the capacity of mangroves to show long-term acclimation of leaf water relations to severe drought. We tested for differences between mid-dry season leaf water relations in two cooccurring mangroves, Aegiceras corniculatum and Rhizophora stylosa before a severe drought (a heatwave combined with low rainfall) and after its relief by the wet season. Consistent with ecological stress memory, the legacy of severe drought enhanced salinity tolerance in the subsequent dry season through coordinated adjustments that reduced the leaf water potential at the turgor loss point and increased cell wall rigidity. These adjustments enabled maintenance of turgor and relative water content with increasing salinity. As most canopy growth occurs during the wet season, acclimation to the 'memory' of higher salinity in the previous dry season enables greater leaf function with minimal adjustments, as long-lived leaves progress from wet through dry seasons. However, declining turgor safety margins - the difference between soil water potential and leaf water potential at turgor loss - implied increasing limitation to water use with increasing salinity. Thus, plasticity in leaf water relations contributes fundamentally to mangrove function under varying salinity regimes.

Long-term drought effects on the thermal sensitivity of Amazon forest trees.

The continued functioning of tropical forests under climate change depends on their resilience to drought and heat. However, there is little understanding of how tropical forests will respond to combinations of these stresses, and no field studies to date have explicitly evaluated whether sustained drought alters sensitivity to temperature. We measured the temperature response of net photosynthesis, foliar respiration and the maximum quantum efficiency of photosystem II (Fv /Fm ) of eight hyper-dominant Amazonian tree species at the world's longest-running tropical forest drought experiment, to investigate the effect of drought on forest thermal sensitivity. Despite a 0.6°C-2°C increase in canopy air temperatures following long-term drought, no change in overall thermal sensitivity of net photosynthesis or respiration was observed. However, photosystem II tolerance to extreme-heat damage (T50 ) was reduced from 50.0 ± 0.3°C to 48.5 ± 0.3°C under drought. Our results suggest that long-term reductions in precipitation, as projected across much of Amazonia by climate models, are unlikely to greatly alter the response of tropical forests to rising mean temperatures but may increase the risk of leaf thermal damage during heatwaves.

Induced drought strongly affects richness and composition of ground-dwelling ants in the eastern Amazon.

Species loss in tropical regions is forecast to occur under environmental change scenarios of low precipitation. One of the main questions is how drought will affect invertebrates, a key group for ecosystem functioning. We use 1 year of data from a long-term rainwater exclusion experiment in primary Amazonian rainforest to test whether induced water stress and covarying changes in soil moisture, soil respiration, and tree species richness, diversity, size, and total biomass affected species richness and composition (relative abundance) of ground-dwelling ants. Data on ant abundance and environmental variables were collected at two sites (control and experimental) in the Eastern Amazon. Since 2002, drought has been induced in the experimental plot by excluding 50% of normal rainfall. Ant species richness in the experiment plot was reduced and some generalist species responded positively. Ant species richness also increased in the experimental plot with increasing diversity of the plant species of the leaf litter. The relative abundance of ants differed between plots. The experimental plot was characterized by a higher frequency of generalist and other species that appeared to be favored by the reduction in rainfall. Between-plot comparisons suggested loss and changes in ant species composition in tropical forests were affected by increasing dryness. These changes could ultimately lead to cascading effects on ecosystem processes and the services they mediate.

Forest system hydraulic conductance: partitioning tree and soil components.

Soil-leaf hydraulic conductance determines canopy-atmosphere coupling in vegetation models, but it is typically derived from ex-situ measurements of stem segments and soil samples. Using a novel approach, we derive robust in-situ estimates for whole-tree conductance (ktree ), 'functional' soil conductance (ksoil ), and 'system' conductance (ksystem , water table to canopy), at two climatically different tropical rainforest sites. Hydraulic 'functional rooting depth', determined for each tree using profiles of soil water potential (Ψsoil ) and sap flux data, enabled a robust determination of ktree and ksoil . ktree was compared across species, size classes, seasons, height above nearest drainage (HAND), two field sites, and to alternative representations of ktree ; ksoil was analysed with respect to variations in site, season and HAND. ktree was lower and changed seasonally at the site with higher vapour pressure deficit (VPD) and rainfall; ktree differed little across species but scaled with tree circumference; rsoil (1/ksoil ) ranged from 0 in the wet season to 10× less than rtree (1/ktree ) in the dry season. VPD and not rainfall may influence plot-level k; leaf water potentials and sap flux can be used to determine ktree , ksoil and ksystem ; Ψsoil profiles can provide mechanistic insights into ecosystem-level water fluxes.

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 ant community responses to experimental soil warming.

Climate change is one of the primary agents of the global decline in insect abundance. Because of their narrow thermal ranges, tropical ectotherms are predicted to be most threatened by global warming, yet tests of this prediction are often confounded by other anthropogenic disturbances. We used a tropical forest soil warming experiment to directly test the effect of temperature increase on litter-dwelling ants. Two years of continuous warming led to a change in ant community between warming and control plots. Specifically, six ant genera were recorded only on warming plots, and one genus only on control plots. Wasmannia auropuctata, a species often invasive elsewhere but native to this forest, was more abundant in warmed plots. Ant recruitment at baits was best predicted by soil surface temperature and ant heat tolerance. These results suggest that heat tolerance is useful for predicting changes in daily foraging activity, which is directly tied to colony fitness. We show that a 2-year increase in temperature (of 2-4°C) can have a profound effect on the most abundant insects, potentially favouring species with invasive traits and moderate heat tolerances.

Acclimation of leaf respiration temperature responses across thermally contrasting biomes.

Short-term temperature response curves of leaf dark respiration (R-T) provide insights into a critical process that influences plant net carbon exchange. This includes how respiratory traits acclimate to sustained changes in the environment. Our study analysed 860 high-resolution R-T (10-70°C range) curves for: (a) 62 evergreen species measured in two contrasting seasons across several field sites/biomes; and (b) 21 species (subset of those sampled in the field) grown in glasshouses at 20°C : 15°C, 25°C : 20°C and 30°C : 25°C, day : night. In the field, across all sites/seasons, variations in R25 (measured at 25°C) and the leaf T where R reached its maximum (Tmax ) were explained by growth T (mean air-T of 30-d before measurement), solar irradiance and vapour pressure deficit, with growth T having the strongest influence. R25 decreased and Tmax increased with rising growth T across all sites and seasons with the single exception of winter at the cool-temperate rainforest site where irradiance was low. The glasshouse study confirmed that R25 and Tmax thermally acclimated. Collectively, the results suggest: (1) thermal acclimation of leaf R is common in most biomes; and (2) the high T threshold of respiration dynamically adjusts upward when plants are challenged with warmer and hotter climates.

Plant traits controlling growth change in response to a drier climate.

Plant traits are increasingly being used to improve prediction of plant function, including plant demography. However, the capability of plant traits to predict demographic rates remains uncertain, particularly in the context of trees experiencing a changing climate. Here we present data combining 17 plant traits associated with plant structure, metabolism and hydraulic status, with measurements of long-term mean, maximum and relative growth rates for 176 trees from the world's longest running tropical forest drought experiment. We demonstrate that plant traits can predict mean annual tree growth rates with moderate explanatory power. However, only combinations of traits associated more directly with plant functional processes, rather than more commonly employed traits like wood density or leaf mass per area, yield the power to predict growth. Critically, we observe a shift from growth being controlled by traits related to carbon cycling (assimilation and respiration) in well-watered trees, to traits relating to plant hydraulic stress in drought-stressed trees. We also demonstrate that even with a very comprehensive set of plant traits and growth data on large numbers of tropical trees, considerable uncertainty remains in directly interpreting the mechanisms through which traits influence performance in tropical forests.

Rapid responses of root traits and productivity to phosphorus and cation additions in a tropical lowland forest in Amazonia.

Soil nutrient availability can strongly affect root traits. In tropical forests, phosphorus (P) is often considered the main limiting nutrient for plants. However, support for the P paradigm is limited, and N and cations might also control tropical forests functioning. We used a large-scale experiment to determine how the factorial addition of nitrogen (N), P and cations affected root productivity and traits related to nutrient acquisition strategies (morphological traits, phosphatase activity, arbuscular mycorrhizal colonisation and nutrient contents) in a primary rainforest growing on low-fertility soils in Central Amazonia after 1 yr of fertilisation. Multiple root traits and productivity were affected. Phosphorus additions increased annual root productivity and root diameter, but decreased root phosphatase activity. Cation additions increased root productivity at certain times of year, also increasing root diameter and mycorrhizal colonisation. P and cation additions increased their element concentrations in root tissues. No responses were detected with N addition. Here we showed that rock-derived nutrients determined root functioning in low-fertility Amazonian soils, demonstrating not only the hypothesised importance of P, but also highlighting the role of cations. The changes in fine root traits and productivity indicated that even slow-growing tropical rainforests can respond rapidly to changes in resource availability.

Does economic optimisation explain LAI and leaf trait distributions across an Amazon soil moisture gradient?

Leaf area index (LAI) underpins terrestrial ecosystem functioning, yet our ability to predict LAI remains limited. Across Amazon forests, mean LAI, LAI seasonal dynamics and leaf traits vary with soil moisture stress. We hypothesise that LAI variation can be predicted via an optimality-based approach, using net canopy C export (NCE, photosynthesis minus the C cost of leaf growth and maintenance) as a fitness proxy. We applied a process-based terrestrial ecosystem model to seven plots across a moisture stress gradient with detailed in situ measurements, to determine nominal plant C budgets. For each plot, we then compared observations and simulations of the nominal (i.e. observed) C budget to simulations of alternative, experimental budgets. Experimental budgets were generated by forcing the model with synthetic LAI timeseries (across a range of mean LAI and LAI seasonality) and different leaf trait combinations (leaf mass per unit area, lifespan, photosynthetic capacity and respiration rate) operating along the leaf economic spectrum. Observed mean LAI and LAI seasonality across the soil moisture stress gradient maximised NCE, and were therefore consistent with optimality-based predictions. Yet, the predictive power of an optimality-based approach was limited due to the asymptotic response of simulated NCE to mean LAI and LAI seasonality. Leaf traits fundamentally shaped the C budget, determining simulated optimal LAI and total NCE. Long-lived leaves with lower maximum photosynthetic capacity maximised simulated NCE under aseasonal high mean LAI, with the reverse found for short-lived leaves and higher maximum photosynthetic capacity. The simulated leaf trait LAI trade-offs were consistent with observed distributions. We suggest that a range of LAI strategies could be equally economically viable at local level, though we note several ecological limitations to this interpretation (e.g. between-plant competition). In addition, we show how leaf trait trade-offs enable divergence in canopy strategies. Our results also allow an assessment of the usefulness of optimality-based approaches in simulating primary tropical forest functioning, evaluated against in situ data.

Detecting forest response to droughts with global observations of vegetation water content.

Droughts in a warming climate have become more common and more extreme, making understanding forest responses to water stress increasingly pressing. Analysis of water stress in trees has long focused on water potential in xylem and leaves, which influences stomatal closure and water flow through the soil-plant-atmosphere continuum. At the same time, changes of vegetation water content (VWC) are linked to a range of tree responses, including fluxes of water and carbon, mortality, flammability, and more. Unlike water potential, which requires demanding in situ measurements, VWC can be retrieved from remote sensing measurements, particularly at microwave frequencies using radar and radiometry. Here, we highlight key frontiers through which VWC has the potential to significantly increase our understanding of forest responses to water stress. To validate remote sensing observations of VWC at landscape scale and to better relate them to data assimilation model parameters, we introduce an ecosystem-scale analog of the pressure-volume curve, the non-linear relationship between average leaf or branch water potential and water content commonly used in plant hydraulics. The sources of variability in these ecosystem-scale pressure-volume curves and their relationship to forest response to water stress are discussed. We further show to what extent diel, seasonal, and decadal dynamics of VWC reflect variations in different processes relating the tree response to water stress. VWC can also be used for inferring belowground conditions-which are difficult to impossible to observe directly. Lastly, we discuss how a dedicated geostationary spaceborne observational system for VWC, when combined with existing datasets, can capture diel and seasonal water dynamics to advance the science and applications of global forest vulnerability to future droughts.