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.

Fine root dynamics across pantropical rainforest ecosystems.

Fine roots constitute a significant component of the net primary productivity (NPP) of forest ecosystems but are much less studied than aboveground NPP. Comparisons across sites and regions are also hampered by inconsistent methodologies, especially in tropical areas. Here, we present a novel dataset of fine root biomass, productivity, residence time, and allocation in tropical old-growth rainforest sites worldwide, measured using consistent methods, and examine how these variables are related to consistently determined soil and climatic characteristics. Our pantropical dataset spans intensive monitoring plots in lowland (wet, semi-deciduous, and deciduous) and montane tropical forests in South America, Africa, and Southeast Asia (n = 47). Large spatial variation in fine root dynamics was observed across montane and lowland forest types. In lowland forests, we found a strong positive linear relationship between fine root productivity and sand content, this relationship was even stronger when we considered the fractional allocation of total NPP to fine roots, demonstrating that understanding allocation adds explanatory power to understanding fine root productivity and total NPP. Fine root residence time was a function of multiple factors: soil sand content, soil pH, and maximum water deficit, with longest residence times in acidic, sandy, and water-stressed soils. In tropical montane forests, on the other hand, a different set of relationships prevailed, highlighting the very different nature of montane and lowland forest biomes. Root productivity was a strong positive linear function of mean annual temperature, root residence time was a strong positive function of soil nitrogen content in montane forests, and lastly decreasing soil P content increased allocation of productivity to fine roots. In contrast to the lowlands, environmental conditions were a better predictor for fine root productivity than for fractional allocation of total NPP to fine roots, suggesting that root productivity is a particularly strong driver of NPP allocation in tropical mountain regions.

New insights into large tropical tree mass and structure from direct harvest and terrestrial lidar.

A large portion of the terrestrial vegetation carbon stock is stored in the above-ground biomass (AGB) of tropical forests, but the exact amount remains uncertain, partly owing to the lack of measurements. To date, accessible peer-reviewed data are available for just 10 large tropical trees in the Amazon that have been harvested and directly measured entirely via weighing. Here, we harvested four large tropical rainforest trees (stem diameter: 0.6-1.2 m, height: 30-46 m, AGB: 3960-18 584 kg) in intact old-growth forest in East Amazonia, and measured above-ground green mass, moisture content and woody tissue density. We first present rare ecological insights provided by these data, including unsystematic intra-tree variations in density, with both height and radius. We also found the majority of AGB was usually found in the crown, but varied from 42 to 62%. We then compare non-destructive approaches for estimating the AGB of these trees, using both classical allometry and new lidar-based methods. Terrestrial lidar point clouds were collected pre-harvest, on which we fitted cylinders to model woody structure, enabling retrieval of volume-derived AGB. Estimates from this approach were more accurate than allometric counterparts (mean tree-scale relative error: 3% versus 15%), and error decreased when up-scaling to the cumulative AGB of the four trees (1% versus 15%). Furthermore, while allometric error increased fourfold with tree size over the diameter range, lidar error remained constant. This suggests error in these lidar-derived estimates is random and additive. Were these results transferable across forest scenes, terrestrial lidar methods would reduce uncertainty in stand-scale AGB estimates, and therefore advance our understanding of the role of tropical forests in the global carbon cycle.

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.

Small tropical forest trees have a greater capacity to adjust carbon metabolism to long-term drought than large canopy trees.

The response of small understory trees to long-term drought is vital in determining the future composition, carbon stocks and dynamics of tropical forests. Long-term drought is, however, also likely to expose understory trees to increased light availability driven by drought-induced mortality. Relatively little is known about the potential for understory trees to adjust their physiology to both decreasing water and increasing light availability. We analysed data on maximum photosynthetic capacity (Jmax , Vcmax ), leaf respiration (Rleaf ), leaf mass per area (LMA), leaf thickness and leaf nitrogen and phosphorus concentrations from 66 small trees across 12 common genera at the world's longest running tropical rainfall exclusion experiment and compared responses to those from 61 surviving canopy trees. Small trees increased Jmax , Vcmax , Rleaf and LMA (71, 29, 32, 15% respectively) in response to the drought treatment, but leaf thickness and leaf nutrient concentrations did not change. Small trees were significantly more responsive than large canopy trees to the drought treatment, suggesting greater phenotypic plasticity and resilience to prolonged drought, although differences among taxa were observed. Our results highlight that small tropical trees have greater capacity to respond to ecosystem level changes and have the potential to regenerate resilient forests following future droughts.

Amazonia trees have limited capacity to acclimate plant hydraulic properties in response to long-term drought.

The fate of tropical forests under future climate change is dependent on the capacity of their trees to adjust to drier conditions. The capacity of trees to withstand drought is likely to be determined by traits associated with their hydraulic systems. However, data on whether tropical trees can adjust hydraulic traits when experiencing drought remain rare. We measured plant hydraulic traits (e.g. hydraulic conductivity and embolism resistance) and plant hydraulic system status (e.g. leaf water potential, native embolism and safety margin) on >150 trees from 12 genera (36 species) and spanning a stem size range from 14 to 68 cm diameter at breast height at the world's only long-running tropical forest drought experiment. Hydraulic traits showed no adjustment following 15 years of experimentally imposed moisture deficit. This failure to adjust resulted in these drought-stressed trees experiencing significantly lower leaf water potentials, and higher, but variable, levels of native embolism in the branches. This result suggests that hydraulic damage caused by elevated levels of embolism is likely to be one of the key drivers of drought-induced mortality following long-term soil moisture deficit. We demonstrate that some hydraulic traits changed with tree size, however, the direction and magnitude of the change was controlled by taxonomic identity. Our results suggest that Amazonian trees, both small and large, have limited capacity to acclimate their hydraulic systems to future droughts, potentially making them more at risk of drought-induced mortality.

Foliar water uptake in Amazonian trees: Evidence and consequences.

The absorption of atmospheric water directly into leaves enables plants to alleviate the water stress caused by low soil moisture, hydraulic resistance in the xylem and the effect of gravity on the water column, while enabling plants to scavenge small inputs of water from leaf-wetting events. By increasing the availability of water, and supplying it from the top of the canopy (in a direction facilitated by gravity), foliar uptake (FU) may be a significant process in determining how forests interact with climate, and could alter our interpretation of current metrics for hydraulic stress and sensitivity. FU has not been reported for lowland tropical rainforests; we test whether FU occurs in six common Amazonian tree genera in lowland Amazônia, and make a first estimation of its contribution to canopy-atmosphere water exchange. We demonstrate that FU occurs in all six genera and that dew-derived water may therefore be used to "pay" for some morning transpiration in the dry season. Using meteorological and canopy wetness data, coupled with empirically derived estimates of leaf conductance to FU (kfu ), we estimate that the contribution by FU to annual transpiration at this site has a median value of 8.2% (103 mm/year) and an interquartile range of 3.4%-15.3%, with the biggest sources of uncertainty being kfu and the proportion of time the canopy is wet. Our results indicate that FU is likely to be a common strategy and may have significant implications for the Amazon carbon budget. The process of foliar water uptake may also have a profound impact on the drought tolerance of individual Amazonian trees and tree species, and on the cycling of water and carbon, regionally and globally.

Modelling tropical forest responses to drought and El Niño with a stomatal optimization model based on xylem hydraulics.

The current generation of dynamic global vegetation models (DGVMs) lacks a mechanistic representation of vegetation responses to soil drought, impairing their ability to accurately predict Earth system responses to future climate scenarios and climatic anomalies, such as El Niño events. We propose a simple numerical approach to model plant responses to drought coupling stomatal optimality theory and plant hydraulics that can be used in dynamic global vegetation models (DGVMs). The model is validated against stand-scale forest transpiration (E) observations from a long-term soil drought experiment and used to predict the response of three Amazonian forest sites to climatic anomalies during the twentieth century. We show that our stomatal optimization model produces realistic stomatal responses to environmental conditions and can accurately simulate how tropical forest E responds to seasonal, and even long-term soil drought. Our model predicts a stronger cumulative effect of climatic anomalies in Amazon forest sites exposed to soil drought during El Niño years than can be captured by alternative empirical drought representation schemes. The contrasting responses between our model and empirical drought factors highlight the utility of hydraulically-based stomatal optimization models to represent vegetation responses to drought and climatic anomalies in DGVMs.This article is part of a discussion meeting issue 'The impact of the 2015/2016 El Niño on the terrestrial tropical carbon cycle: patterns, mechanisms and implications'.

ENSO Drives interannual variation of forest woody growth across the tropics.

Meteorological extreme events such as El Niño events are expected to affect tropical forest net primary production (NPP) and woody growth, but there has been no large-scale empirical validation of this expectation. We collected a large high-temporal resolution dataset (for 1-13 years depending upon location) of more than 172 000 stem growth measurements using dendrometer bands from across 14 regions spanning Amazonia, Africa and Borneo in order to test how much month-to-month variation in stand-level woody growth of adult tree stems (NPPstem) can be explained by seasonal variation and interannual meteorological anomalies. A key finding is that woody growth responds differently to meteorological variation between tropical forests with a dry season (where monthly rainfall is less than 100 mm), and aseasonal wet forests lacking a consistent dry season. In seasonal tropical forests, a high degree of variation in woody growth can be predicted from seasonal variation in temperature, vapour pressure deficit, in addition to anomalies of soil water deficit and shortwave radiation. The variation of aseasonal wet forest woody growth is best predicted by the anomalies of vapour pressure deficit, water deficit and shortwave radiation. In total, we predict the total live woody production of the global tropical forest biome to be 2.16 Pg C yr-1, with an interannual range 1.96-2.26 Pg C yr-1 between 1996-2016, and with the sharpest declines during the strong El Niño events of 1997/8 and 2015/6. There is high geographical variation in hotspots of El Niño-associated impacts, with weak impacts in Africa, and strongly negative impacts in parts of Southeast Asia and extensive regions across central and eastern Amazonia. Overall, there is high correlation (r = -0.75) between the annual anomaly of tropical forest woody growth and the annual mean of the El Niño 3.4 index, driven mainly by strong correlations with anomalies of soil water deficit, vapour pressure deficit and shortwave radiation.This article is part of the discussion meeting issue 'The impact of the 2015/2016 El Niño on the terrestrial tropical carbon cycle: patterns, mechanisms and implications'.

Isoprene emission structures tropical tree biogeography and community assembly responses to climate.

The prediction of vegetation responses to climate requires a knowledge of how climate-sensitive plant traits mediate not only the responses of individual plants, but also shifts in the species and functional compositions of whole communities. The emission of isoprene gas - a trait shared by one-third of tree species - is known to protect leaf biochemistry under climatic stress. Here, we test the hypothesis that isoprene emission shapes tree species compositions in tropical forests by enhancing the tolerance of emitting trees to heat and drought. Using forest inventory data, we estimated the proportional abundance of isoprene-emitting trees (pIE) at 103 lowland tropical sites. We also quantified the temporal composition shifts in three tropical forests - two natural and one artificial - subjected to either anomalous warming or drought. Across the landscape, pIE increased with site mean annual temperature, but decreased with dry season length. Through time, pIE strongly increased under high temperatures, and moderately increased following drought. Our analysis shows that isoprene emission is a key plant trait determining species responses to climate. For species adapted to seasonal dry periods, isoprene emission may tradeoff with alternative strategies, such as leaf deciduousness. Community selection for isoprene-emitting species is a potential mechanism for enhanced forest resilience to climatic change.

Drought stress and tree size determine stem CO2 efflux in a tropical forest.

CO2 efflux from stems (CO2_stem ) accounts for a substantial fraction of tropical forest gross primary productivity, but the climate sensitivity of this flux remains poorly understood. We present a study of tropical forest CO2_stem from 215 trees across wet and dry seasons, at the world's longest running tropical forest drought experiment site. We show a 27% increase in wet season CO2_stem in the droughted forest relative to a control forest. This was driven by increasing CO2_stem in trees 10-40 cm diameter. Furthermore, we show that drought increases the proportion of maintenance to growth respiration in trees > 20 cm diameter, including large increases in maintenance respiration in the largest droughted trees, > 40 cm diameter. However, we found no clear taxonomic influence on CO2_stem and were unable to accurately predict how drought sensitivity altered ecosystem scale CO2_stem , due to substantial uncertainty introduced by contrasting methods previously employed to scale CO2_stem fluxes. Our findings indicate that under future scenarios of elevated drought, increases in CO2_stem may augment carbon losses, weakening or potentially reversing the tropical forest carbon sink. However, due to substantial uncertainties in scaling CO2_stem fluxes, stand-scale future estimates of changes in stem CO2 emissions remain highly uncertain.

Stand dynamics modulate water cycling and mortality risk in droughted tropical forest.

Transpiration from the Amazon rainforest generates an essential water source at a global and local scale. However, changes in rainforest function with climate change can disrupt this process, causing significant reductions in precipitation across Amazonia, and potentially at a global scale. We report the only study of forest transpiration following a long-term (>10 year) experimental drought treatment in Amazonian forest. After 15 years of receiving half the normal rainfall, drought-related tree mortality caused total forest transpiration to decrease by 30%. However, the surviving droughted trees maintained or increased transpiration because of reduced competition for water and increased light availability, which is consistent with increased growth rates. Consequently, the amount of water supplied as rainfall reaching the soil and directly recycled as transpiration increased to 100%. This value was 25% greater than for adjacent nondroughted forest. If these drought conditions were accompanied by a modest increase in temperature (e.g., 1.5°C), water demand would exceed supply, making the forest more prone to increased tree mortality.

After more than a decade of soil moisture deficit, tropical rainforest trees maintain photosynthetic capacity, despite increased leaf respiration.

Determining climate change feedbacks from tropical rainforests requires an understanding of how carbon gain through photosynthesis and loss through respiration will be altered. One of the key changes that tropical rainforests may experience under future climate change scenarios is reduced soil moisture availability. In this study we examine if and how both leaf photosynthesis and leaf dark respiration acclimate following more than 12 years of experimental soil moisture deficit, via a through-fall exclusion experiment (TFE) in an eastern Amazonian rainforest. We find that experimentally drought-stressed trees and taxa maintain the same maximum leaf photosynthetic capacity as trees in corresponding control forest, independent of their susceptibility to drought-induced mortality. We hypothesize that photosynthetic capacity is maintained across all treatments and taxa to take advantage of short-lived periods of high moisture availability, when stomatal conductance (gs ) and photosynthesis can increase rapidly, potentially compensating for reduced assimilate supply at other times. Average leaf dark respiration (Rd ) was elevated in the TFE-treated forest trees relative to the control by 28.2 ± 2.8% (mean ± one standard error). This mean Rd value was dominated by a 48.5 ± 3.6% increase in the Rd of drought-sensitive taxa, and likely reflects the need for additional metabolic support required for stress-related repair, and hydraulic or osmotic maintenance processes. Following soil moisture deficit that is maintained for several years, our data suggest that changes in respiration drive greater shifts in the canopy carbon balance, than changes in photosynthetic capacity.

The linkages between photosynthesis, productivity, growth and biomass in lowland Amazonian forests.

Understanding the relationship between photosynthesis, net primary productivity and growth in forest ecosystems is key to understanding how these ecosystems will respond to global anthropogenic change, yet the linkages among these components are rarely explored in detail. We provide the first comprehensive description of the productivity, respiration and carbon allocation of contrasting lowland Amazonian forests spanning gradients in seasonal water deficit and soil fertility. Using the largest data set assembled to date, ten sites in three countries all studied with a standardized methodology, we find that (i) gross primary productivity (GPP) has a simple relationship with seasonal water deficit, but that (ii) site-to-site variations in GPP have little power in explaining site-to-site spatial variations in net primary productivity (NPP) or growth because of concomitant changes in carbon use efficiency (CUE), and conversely, the woody growth rate of a tropical forest is a very poor proxy for its productivity. Moreover, (iii) spatial patterns of biomass are much more driven by patterns of residence times (i.e. tree mortality rates) than by spatial variation in productivity or tree growth. Current theory and models of tropical forest carbon cycling under projected scenarios of global atmospheric change can benefit from advancing beyond a focus on GPP. By improving our understanding of poorly understood processes such as CUE, NPP allocation and biomass turnover times, we can provide more complete and mechanistic approaches to linking climate and tropical forest carbon cycling.

Threshold Responses to Soil Moisture Deficit by Trees and Soil in Tropical Rain Forests: Insights from Field Experiments.

Many tropical rain forest regions are at risk of increased future drought. The net effects of drought on forest ecosystem functioning will be substantial if important ecological thresholds are passed. However, understanding and predicting these effects is challenging using observational studies alone. Field-based rainfall exclusion (canopy throughfall exclusion; TFE) experiments can offer mechanistic insight into the response to extended or severe drought and can be used to help improve model-based simulations, which are currently inadequate. Only eight TFE experiments have been reported for tropical rain forests. We examine them, synthesizing key results and focusing on two processes that have shown threshold behavior in response to drought: (1) tree mortality and (2) the efflux of carbon dioxdie from soil, soil respiration. We show that: (a) where tested using large-scale field experiments, tropical rain forest tree mortality is resistant to long-term soil moisture deficit up to a threshold of 50% of the water that is extractable by vegetation from the soil, but high mortality occurs beyond this value, with evidence from one site of increased autotrophic respiration, and (b) soil respiration reaches its peak value in response to soil moisture at significantly higher soil moisture content for clay-rich soils than for clay-poor soils. This first synthesis of tropical TFE experiments offers the hypothesis that low soil moisture-related thresholds for key stress responses in soil and vegetation may prove to be widely applicable across tropical rain forests despite the diversity of these forests.