Steel Silva Vasconcelos

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.

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.

Effects of water and nutrient availability on fine root growth in eastern Amazonian forest regrowth, Brazil

*Fine root dynamics is widely recognized as an important biogeochemical process, but there are few data on fine root growth and its response to soil resource availability, especially for tropical forests. *We evaluated the response of fine root dynamics to altered availability of soil water and nutrients in a 20-yr-old forest regrowth in eastern Amazonia. In one experiment the dry season reduction in soil moisture was alleviated by irrigation. In the other experiment, nutrient supply was reduced by litter removal. We used the ingrowth core technique to measure fine root mass growth, length growth, mortality and specific root length. *Dry-season irrigation had no significant effect on mass and length of live and dead roots, whereas litter removal reduced mass and length of live roots. For both irrigation and litter removal experiments, root growth was significantly greater in the dry season than in the wet season. *Increased root growth was associated with decreased soil water availability. However, root growth did not increase in response to nutrient reduction in litter removal plots. Overall, our results suggest that belowground allocation may differ according to the type of soil resource limitation.

DROUGHT CONSTRAINTS ON LEAF GAS EXCHANGE BY MICONIA CILIATA (MELASTOMATACEAE) IN THE UNDERSTORY OF AN EASTERN AMAZONIAN REGROWTH FOREST STAND

Analyses of the effects of drought stress on Amazonian regrowth stands are lacking. We measured leaf gas exchange and leaf water potential of Miconia ciliata (Melastomataceae) in a dry-season irrigation experiment in 14-yr-old regrowth. In the dry season, irrigated plants maintained significantly higher leaf water potentials, photosynthetic capacity at light saturation (A(max)), stomatal conductance (g(s)), internal CO(2) concentration (C(i)), and lower A(max)/g(s) than control plants. The degree of dry-season down-regulation of control plant A(max), along with its fast recovery following rain, reveals the importance of occasional dry-season rains to the carbon budget of M. ciliata. During the wet season, we observed higher A(max) for control plants than for plants that had been irrigated during the dry season. We hypothesize that reduced drought constraints on photosynthesis of irrigated plants advanced the flowering and fruiting phenology of irrigated plants into the dry season. Flowers and fruits of control plants developed later, during the wet season, potentially stimulating a compensatory reproductive photosynthesis response in nearby leaves. The relative drought intolerance of M. ciliata may be a deciding factor in its ability to survive through the dynamic successional development of the regrowth stand studied.

Effects of seasonality, litter removal and dry-season irrigation on litterfall quantity and quality in eastern Amazonian forest regrowth, Brazil

Litterfall quantity and quality may respond to alterations in resource availability expected with ongoing land-use and climate changes. Here, we quantify the effects of altered resource availability on non-woody litterfall quantityandquality(nitrogenandphosphorusconcentrations)ineasternAmazonianforestregrowth(Brazil)through two multi-year experimental manipulations: (1) daily irrigation (5mm d −1 ) during the dry season; and (2) fortnightly litterremoval.Consistentwithothertropicalforestdatalitterfallexhibitedseasonalpatterns,increasingwiththeonset of the dry season and declining with the onset of the rainy season. Irrigation did not affect litterfall mass and had little impactonnitrogen(N)orphosphorus(P)concentrationsandreturn,exceptfordecreasinglitterPconcentrationatthe end of two irrigation periods. Litter removal did not alter litterfall mass or P concentration, but progressively reduced litterfall N during the course of the experiment. Overall, these results suggest significant resistance to altered resource availabilitywithintheboundsofourexperimentaltreatments;ourfindingsmayhelptoconstraincarbonandnutrient cycling predictions for tropical forests in response to land-use and climate changes.

Biomass equations for forest regrowth in the eastern Amazon using randomized branch sampling

Forest regrowth occupies an extensive and increasing area in the Amazon basin, but accurate assessment of the impact of regrowth on carbon and nutrient cycles has been hampered by a paucity of available allometric equations. We develop pooled and species-specific equations for total aboveground biomass for a study site in the eastern Amazon that had been abandoned for 15 years. Field work was conducted using randomized branch sampling, a rapid technique that has seen little use in tropical forests. High consistency of sample paths in randomized branch sampling, as measured by the standard error of individual paths (14%), suggests the method may provide substantial efficiencies when compared to traditional procedures. The best fitting equations in this study used the traditional form Y=a×DBH b , where Y is biomass, DBH is diameter at breast height, and a and b are both species-specific parameters. Species-specific equations of the form Y=a(BA×H), where Y is biomass, BA is tree basal area, H is tree height, and a is a species-specific parameter, fit almost as well. Comparison with previously published equations indicated errors from -33% to +29% would have occurred using off-site relationships. We also present equations for stemwood, twigs, and foliage as biomass components.

Nitrogênio mineral e microbiano do solo em sistemas agroflorestais com palma de óleo na Amazônia oriental

The success of oil palm (Elaeis guineensis Jacq.)-based agroforestry systems (oil palm-AFS) depends on sustainable soil management, especially of soil chemical and microbiological characteristics. Our objective was to evaluate the impact of oil palm-AFS on soil mineral and microbial nitrogen (N) in contrasting rainfall seasons. We evaluated different soil nitrogen (N) forms (microbial-N, nitrate, ammonium) and soil carbon concentration in oil palm-AFS with low and high diversity of species planted, which were compared with an adjacent 13-yr-old secondary forest. Most variables (total N, C:N ratio, microbial-N, microbial-N:total N ratio, ammonium, and net nitrification rate) varied only in response to rainfall seasonality. Soil C was significantly higher in the high diversity AFS (15.6 mg g-1) than in the secondary forest (13.0 mg g-1). In the rainy season, nitrate concentration (5.1 mg N kg-1 soil) was higher in the high diversity AFS than in other vegetation types; consequently, the average soil ammonium concentration (9.6 mg N kg-1 soil) was significantly lower in the high diversity AFS. Net N mineralization in the low diversity AFS (0.1 mg N kg-1 soil day-1) in the dry season was significantly lower than in other vegetation types. The soil variables were more sensitive to the rainfall seasonality than to the conversion of secondary forest to oil palm-based agroforestry systems.

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.

Temporal variation of soil CO2 efflux in oil palm-based agroforestry systems in eastern Amazon

The soil carbon dioxide (CO2) efflux dynamics and its controlling factors of Amazonian agroforestry systems are poorly understood. The objective of this study was to evaluate the temporal variation of soil CO2 efflux in oil palm-based agroforestry systems and the relation between efflux and biotic (microbial and total soil carbon, microbial respiration, fine roots, individual components of agroforestry systems (AFS)) and abiotic factors (soil moisture and temperature). The measurements were taken during the less rainy (December 2010) and rainy (May 2011) periods. The soil CO2 efflux was highest during the rainy season, probably due to increased microbial activity influenced by climatic factors coupled with biotic factors. The soil CO2efflux correlated positively with soil moisture and microbial biomass carbon and negatively with soil temperature and metabolic quotient, but these correlations were weak. The soil CO2 efflux was sensitive to the type of agroforestry system and to rainfall seasonality.