Lucy Rowland

Death from drought in tropical forests is triggered by hydraulics not carbon starvation

Drought threatens tropical rainforests over seasonal to decadal timescales, but the drivers of tree mortality following drought remain poorly understood. It has been suggested that reduced availability of non-structural carbohydrates (NSC) critically increases mortality risk through insufficient carbon supply to metabolism (‘carbon starvation’). However, little is known about how NSC stores are affected by drought, especially over the long term, and whether they are more important than hydraulic processes in determining drought-induced mortality. Using data from the world’s longest-running experimental drought study in tropical rainforest (in the Brazilian Amazon), we test whether carbon starvation or deterioration of the water-conducting pathways from soil to leaf trigger tree mortality. Biomass loss from mortality in the experimentally droughted forest increased substantially after >10 years of reduced soil moisture availability. The mortality signal was dominated by the death of large trees, which were at a much greater risk of hydraulic deterioration than smaller trees. However, we find no evidence that the droughted trees suffered carbon starvation, as their NSC concentrations were similar to those of non-droughted trees, and growth rates did not decline in either living or dying trees. Our results indicate that hydraulics, rather than carbon starvation, triggers tree death from drought in tropical rainforest.

Confronting model predictions of carbon fluxes with measurements of Amazon forests subjected to experimental drought

Considerable uncertainty surrounds the fate of Amazon rainforests in response to climate change. Here, carbon (C) flux predictions of five terrestrial biosphere models (Community Land Model version 3.5 (CLM3.5), Ecosystem Demography model version 2.1 (ED2), Integrated BIosphere Simulator version 2.6.4 (IBIS), Joint UK Land Environment Simulator version 2.1 (JULES) and Simple Biosphere model version 3 (SiB3)) and a hydrodynamic terrestrial ecosystem model (the Soil-Plant-Atmosphere (SPA) model) were evaluated against measurements from two large-scale Amazon drought experiments. Model predictions agreed with the observed C fluxes in the control plots of both experiments, but poorly replicated the responses to the drought treatments. Most notably, with the exception of ED2, the models predicted negligible reductions in aboveground biomass in response to the drought treatments, which was in contrast to an observed c. 20% reduction at both sites. For ED2, the timing of the decline in aboveground biomass was accurate, but the magnitude was too high for one site and too low for the other. Three key findings indicate critical areas for future research and model development. First, the models predicted declines in autotrophic respiration under prolonged drought in contrast to measured increases at one of the sites. Secondly, models lacking a phenological response to drought introduced bias in the sensitivity of canopy productivity and respiration to drought. Thirdly, the phenomenological water-stress functions used by the terrestrial biosphere models to represent the effects of soil moisture on stomatal conductance yielded unrealistic diurnal and seasonal responses to drought.

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.

Ecosystem respiration and net primary productivity after 8–10 years of experimental through-fall reduction in an eastern Amazon forest

Background: There is much interest in how the Amazon rainforest may respond to future rainfall reduction. However, there are relatively few ecosystem-scale studies to inform this debate. Aims: We described the carbon cycle in a 1 ha rainforest plot subjected to 8–10 consecutive years of ca. 50% through-fall reduction (TFR) and compare these results with those from a nearby, unmodified control plot in eastern Amazonia. Methods: We quantified the components of net primary productivity (NPP), autotrophic (R a) and heterotrophic respiration, and estimate gross primary productivity (GPP, the sum of NPP and R a) and carbon-use efficiency (CUE, the ratio of NPP/GPP). Results: The TFR forest exhibited slightly lower NPP but slightly higher R a, such that forest CUE was 0.29 ± 0.04 on the control plot but 0.25 ± 0.03 on the TFR plot. Compared with four years earlier, TFR plot leaf area index and small tree growth recovered and soil heterotrophic respiration had risen. Conclusions: This analysis tested and extended the key findings of a similar analysis 4 years earlier in the TFR treatment. The results indicated that, while the forest recovered from extended drought in some respects, it maintained higher overall R a relative to the undroughted control, potentially causing the droughted forest to act as a net source of CO2.

Evidence for strong seasonality in the carbon storage and carbon use efficiency of an Amazonian forest

The relative contribution of gross primary production and ecosystem respiration to seasonal changes in the net carbon flux of tropical forests remains poorly quantified by both modelling and field studies. We use data assimilation to combine nine ecological time series from an eastern Amazonian forest, with mass balance constraints from an ecosystem carbon cycle model. The resulting analysis quantifies, with uncertainty estimates, the seasonal changes in the net carbon flux of a tropical rainforest which experiences a pronounced dry season. We show that the carbon accumulation in this forest was four times greater in the dry season than in the wet season and that this was accompanied by a 5% increase in the carbon use efficiency. This seasonal response was caused by a dry season increase in gross primary productivity, in response to radiation and a similar magnitude decrease in heterotrophic respiration, in response to drying soils. The analysis also predicts increased carbon allocation to leaves and wood in the wet season, and greater allocation to fine roots in the dry season. This study demonstrates implementation of seasonal variations in parameters better enables models to simulate observed patterns in data. In particular, we highlight the necessity to simulate the seasonal patterns of heterotrophic respiration to accurately simulate the net carbon flux seasonal tropical forest.

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

Abstract 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 (g s) and photosynthesis can increase rapidly, potentially compensating for reduced assimilate supply at other times. Average leaf dark respiration (R d) was elevated in the TFE‐treated forest trees relative to the control by 28.2 ± 2.8% (mean ± one standard error). This mean R d value was dominated by a 48.5 ± 3.6% increase in the R d 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.

Plasticity in leaf-level water relations of tropical rainforest trees in response to experimental drought

Summary The tropics are predicted to become warmer and drier, and understanding the sensitivity of tree species to drought is important for characterizing the risk to forests of climate change. This study makes use of a long‐term drought experiment in the Amazon rainforest to evaluate the role of leaf‐level water relations, leaf anatomy and their plasticity in response to drought in six tree genera. The variables (osmotic potential at full turgor, turgor loss point, capacitance, elastic modulus, relative water content and saturated water content) were compared between seasons and between plots (control and through‐fall exclusion) enabling a comparison between short‐ and long‐term plasticity in traits. Leaf anatomical traits were correlated with water relation parameters to determine whether water relations differed among tissues. The key findings were: osmotic adjustment occurred in response to the long‐term drought treatment; species resistant to drought stress showed less osmotic adjustment than drought‐sensitive species; and water relation traits were correlated with tissue properties, especially the thickness of the abaxial epidermis and the spongy mesophyll. These findings demonstrate that cell‐level water relation traits can acclimate to long‐term water stress, and highlight the limitations of extrapolating the results of short‐term studies to temporal scales associated with climate change.

Seasonal trends of Amazonian rainforest phenology, net primary productivity, and carbon allocation

The seasonality of solar irradiance and precipitation may regulate seasonal variations in tropical forests carbon cycling. Controversy remains over their importance as drivers of seasonal dynamics of net primary productivity in tropical forests. We use ground data from nine lowland Amazonian forest plots collected over 3 years to quantify the monthly primary productivity (NPP) of leaves, reproductive material, woody material, and fine roots over an annual cycle. We distinguish between forests that do not experience substantial seasonal moisture stress (“humid sites”) and forests that experience a stronger dry season (“dry sites”). We find that forests from both precipitation regimes maximize leaf NPP over the drier season, with a peak in production in August at both humid (mean 0.39 ± 0.03 Mg C ha−1 month−1 in July, n = 4) and dry sites (mean 0.49 ± 0.03 Mg C ha−1 month−1 in September, n = 8). We identify two distinct seasonal carbon allocation patterns (the allocation of NPP to a specific organ such as wood leaves or fine roots divided by total NPP). The forests monitored in the present study show evidence of either (i) constant allocation to roots and a seasonal trade-off between leaf and woody material or (ii) constant allocation to wood and a seasonal trade-off between roots and leaves. Finally, we find strong evidence of synchronized flowering at the end of the dry season in both precipitation regimes. Flower production reaches a maximum of 0.047 ± 0.013 and 0.031 ± 0.004 Mg C ha−1 month−1 in November, in humid and dry sites, respectively. Fruitfall production was staggered throughout the year, probably reflecting the high variation in varying times to development and loss of fruit among species. (Less)

Scaling leaf respiration with nitrogen and phosphorus in tropical forests across two continents

Summary Leaf dark respiration (R dark) represents an important component controlling the carbon balance in tropical forests. Here, we test how nitrogen (N) and phosphorus (P) affect R dark and its relationship with photosynthesis using three widely separated tropical forests which differ in soil fertility. R dark was measured on 431 rainforest canopy trees, from 182 species, in French Guiana, Peru and Australia. The variation in R dark was examined in relation to leaf N and P content, leaf structure and maximum photosynthetic rates at ambient and saturating atmospheric CO 2 concentration. We found that the site with the lowest fertility (French Guiana) exhibited greater rates of R dark per unit leaf N, P and photosynthesis. The data from Australia, for which there were no phylogenetic overlaps with the samples from the South American sites, yielded the most distinct relationships of R dark with the measured leaf traits. Our data indicate that no single universal scaling relationship accounts for variation in R dark across this large biogeographical space. Variability between sites in the absolute rates of R dark and the R dark : photosynthesis ratio were driven by variations in N‐ and P‐use efficiency, which were related to both taxonomic and environmental variability.

Limited acclimation in leaf anatomy to experimental drought in tropical rainforest trees.

Dry periods are predicted to become more frequent and severe in the future in some parts of the tropics, including Amazonia, potentially causing reduced productivity, higher tree mortality and increased emissions of stored carbon. Using a long-term (12 year) through-fall exclusion (TFE) experiment in the tropics, we test the hypothesis that trees produce leaves adapted to cope with higher levels of water stress, by examining the following leaf characteristics: area, thickness, leaf mass per area, vein density, stomatal density, the thickness of palisade mesophyll, spongy mesophyll and both of the epidermal layers, internal cavity volume and the average cell sizes of the palisade and spongy mesophyll. We also test whether differences in leaf anatomy are consistent with observed differential drought-induced mortality responses among taxa, and look for relationships between leaf anatomy, and leaf water relations and gas exchange parameters. Our data show that trees do not produce leaves that are more xeromorphic in response to 12 years of soil moisture deficit. However, the drought treatment did result in increases in the thickness of the adaxial epidermis (TFE: 20.5 ± 1.5 µm, control: 16.7 ± 1.0 µm) and the internal cavity volume (TFE: 2.43 ± 0.50 mm3 cm−2, control: 1.77 ± 0.30 mm3 cm−2). No consistent differences were detected between drought-resistant and drought-sensitive taxa, although interactions occurred between drought-sensitivity status and drought treatment for the palisade mesophyll thickness (P = 0.034) and the cavity volume of the leaves (P = 0.025). The limited response to water deficit probably reflects a tight co-ordination between leaf morphology, water relations and photosynthetic properties. This suggests that there is little plasticity in these aspects of plant anatomy in these taxa, and that phenotypic plasticity in leaf traits may not facilitate the acclimation of Amazonian trees to the predicted future reductions in dry season water availability.