Precipitation mediates sap flux sensitivity to evaporative demand in the neotropics.

Transpiration in humid tropical forests modulates the global water cycle and is a key driver of climate regulation. Yet, our understanding of how tropical trees regulate sap flux in response to climate variability remains elusive. With a progressively warming climate, atmospheric evaporative demand [i.e., vapor pressure deficit (VPD)] will be increasingly important for plant functioning, becoming the major control of plant water use in the twenty-first century. Using measurements in 34 tree species at seven sites across a precipitation gradient in the neotropics, we determined how the maximum sap flux velocity (vmax) and the VPD threshold at which vmax is reached (VPDmax) vary with precipitation regime [mean annual precipitation (MAP); seasonal drought intensity (PDRY)] and two functional traits related to foliar and wood economics spectra [leaf mass per area (LMA); wood specific gravity (WSG)]. We show that, even though vmax is highly variable within sites, it follows a negative trend in response to increasing MAP and PDRY across sites. LMA and WSG exerted little effect on vmax and VPDmax, suggesting that these widely used functional traits provide limited explanatory power of dynamic plant responses to environmental variation within hyper-diverse forests. This study demonstrates that long-term precipitation plays an important role in the sap flux response of humid tropical forests to VPD. Our findings suggest that under higher evaporative demand, trees growing in wetter environments in humid tropical regions may be subjected to reduced water exchange with the atmosphere relative to trees growing in drier climates.

Windthrows control biomass patterns and functional composition of Amazon forests.

Amazon forests account for ~25% of global land biomass and tropical tree species. In these forests, windthrows (i.e., snapped and uprooted trees) are a major natural disturbance, but the rates and mechanisms of recovery are not known. To provide a predictive framework for understanding the effects of windthrows on forest structure and functional composition (DBH ≥10 cm), we quantified biomass recovery as a function of windthrow severity (i.e., fraction of windthrow tree mortality on Landsat pixels, ranging from 0%-70%) and time since disturbance for terra-firme forests in the Central Amazon. Forest monitoring allowed insights into the processes and mechanisms driving the net biomass change (i.e., increment minus loss) and shifts in functional composition. Windthrown areas recovering for between 4-27 years had biomass stocks as low as 65.2-91.7 Mg/ha or 23%-38% of those in nearby undisturbed forests (~255.6 Mg/ha, all sites). Even low windthrow severities (4%-20% tree mortality) caused decadal changes in biomass stocks and structure. While rates of biomass increment in recovering vegetation were nearly double (6.3 ± 1.4 Mg ha-1  year-1 ) those of undisturbed forests (~3.7 Mg ha-1  year-1 ), biomass loss due to post-windthrow mortality was high (up to -7.5 ± 8.7 Mg ha-1  year-1 , 8.5 years since disturbance) and unpredictable. Consequently, recovery to 90% of "pre-disturbance" biomass takes up to 40 years. Resprouting trees contributed little to biomass recovery. Instead, light-demanding, low-density genera (e.g., Cecropia, Inga, Miconia, Pourouma, Tachigali, and Tapirira) were favored, resulting in substantial post-windthrow species turnover. Shifts in functional composition demonstrate that windthrows affect the resilience of live tree biomass by favoring soft-wooded species with shorter life spans that are more vulnerable to future disturbances. As the time required for forests to recover biomass is likely similar to the recurrence interval of windthrows triggering succession, windthrows have the potential to control landscape biomass/carbon dynamics and functional composition in Amazon forests.

Monoterpene 'thermometer' of tropical forest-atmosphere response to climate warming.

Tropical forests absorb large amounts of atmospheric CO2 through photosynthesis but elevated temperatures suppress this absorption and promote monoterpene emissions. Using 13 CO2 labeling, here we show that monoterpene emissions from tropical leaves derive from recent photosynthesis and demonstrate distinct temperature optima for five groups (Groups 1-5), potentially corresponding to different enzymatic temperature-dependent reaction mechanisms within ß-ocimene synthases. As diurnal and seasonal leaf temperatures increased during the Amazonian 2015 El Niño event, leaf and landscape monoterpene emissions showed strong linear enrichments of ß-ocimenes (+4.4% °C-1 ) at the expense of other monoterpene isomers. The observed inverse temperature response of α-pinene (-0.8% °C-1 ), typically assumed to be the dominant monoterpene with moderate reactivity, was not accurately simulated by current global emission models. Given that ß-ocimenes are highly reactive with respect to both atmospheric and biological oxidants, the results suggest that highly reactive ß-ocimenes may play important roles in the thermotolerance of photosynthesis by functioning as effective antioxidants within plants and as efficient atmospheric precursors of secondary organic aerosols. Thus, monoterpene composition may represent a new sensitive 'thermometer' of leaf oxidative stress and atmospheric reactivity, and therefore a new tool in future studies of warming impacts on tropical biosphere-atmosphere carbon-cycle feedbacks.

Landscape-scale consequences of differential tree mortality from catastrophic wind disturbance in the Amazon.

Wind disturbance can create large forest blowdowns, which greatly reduces live biomass and adds uncertainty to the strength of the Amazon carbon sink. Observational studies from within the central Amazon have quantified blowdown size and estimated total mortality but have not determined which trees are most likely to die from a catastrophic wind disturbance. Also, the impact of spatial dependence upon tree mortality from wind disturbance has seldom been quantified, which is important because wind disturbance often kills clusters of trees due to large treefalls killing surrounding neighbors. We examine (1) the causes of differential mortality between adult trees from a 300-ha blowdown event in the Peruvian region of the northwestern Amazon, (2) how accounting for spatial dependence affects mortality predictions, and (3) how incorporating both differential mortality and spatial dependence affect the landscape level estimation of necromass produced from the blowdown. Standard regression and spatial regression models were used to estimate how stem diameter, wood density, elevation, and a satellite-derived disturbance metric influenced the probability of tree death from the blowdown event. The model parameters regarding tree characteristics, topography, and spatial autocorrelation of the field data were then used to determine the consequences of non-random mortality for landscape production of necromass through a simulation model. Tree mortality was highly non-random within the blowdown, where tree mortality rates were highest for trees that were large, had low wood density, and were located at high elevation. Of the differential mortality models, the non-spatial models overpredicted necromass, whereas the spatial model slightly underpredicted necromass. When parameterized from the same field data, the spatial regression model with differential mortality estimated only 7.5% more dead trees across the entire blowdown than the random mortality model, yet it estimated 51% greater necromass. We suggest that predictions of forest carbon loss from wind disturbance are sensitive to not only the underlying spatial dependence of observations, but also the biological differences between individuals that promote differential levels of mortality.

The steady-state mosaic of disturbance and succession across an old-growth Central Amazon forest landscape.

Old-growth forest ecosystems comprise a mosaic of patches in different successional stages, with the fraction of the landscape in any particular state relatively constant over large temporal and spatial scales. The size distribution and return frequency of disturbance events, and subsequent recovery processes, determine to a large extent the spatial scale over which this old-growth steady state develops. Here, we characterize this mosaic for a Central Amazon forest by integrating field plot data, remote sensing disturbance probability distribution functions, and individual-based simulation modeling. Results demonstrate that a steady state of patches of varying successional age occurs over a relatively large spatial scale, with important implications for detecting temporal trends on plots that sample a small fraction of the landscape. Long highly significant stochastic runs averaging 1.0 Mg biomass⋅ha(-1)⋅y(-1) were often punctuated by episodic disturbance events, resulting in a sawtooth time series of hectare-scale tree biomass. To maximize the detection of temporal trends for this Central Amazon site (e.g., driven by CO2 fertilization), plots larger than 10 ha would provide the greatest sensitivity. A model-based analysis of fractional mortality across all gap sizes demonstrated that 9.1-16.9% of tree mortality was missing from plot-based approaches, underscoring the need to combine plot and remote-sensing methods for estimating net landscape carbon balance. Old-growth tropical forests can exhibit complex large-scale structure driven by disturbance and recovery cycles, with ecosystem and community attributes of hectare-scale plots exhibiting continuous dynamic departures from a steady-state condition.

Amazon windthrow disturbances are likely to increase with storm frequency under global warming.

Forest mortality caused by convective storms (windthrow) is a major disturbance in the Amazon. However, the linkage between windthrows at the surface and convective storms in the atmosphere remains unclear. In addition, the current Earth system models (ESMs) lack mechanistic links between convective wind events and tree mortality. Here we find an empirical relationship that maps convective available potential energy, which is well simulated by ESMs, to the spatial pattern of large windthrow events. This relationship builds connections between strong convective storms and forest dynamics in the Amazon. Based on the relationship, our model projects a 51 ± 20% increase in the area favorable to extreme storms, and a 43 ± 17% increase in windthrow density within the Amazon by the end of this century under the high-emission scenario (SSP 585). These results indicate significant changes in tropical forest composition and carbon cycle dynamics under climate change.

Impacts of tropical cyclones on U.S. forest tree mortality and carbon flux from 1851 to 2000.

Tropical cyclones cause extensive tree mortality and damage to forested ecosystems. A number of patterns in tropical cyclone frequency and intensity have been identified. There exist, however, few studies on the dynamic impacts of historical tropical cyclones at a continental scale. Here, we synthesized field measurements, satellite image analyses, and empirical models to evaluate forest and carbon cycle impacts for historical tropical cyclones from 1851 to 2000 over the continental U.S. Results demonstrated an average of 97 million trees affected each year over the entire United States, with a 53-Tg annual biomass loss, and an average carbon release of 25 Tg y(-1). Over the period 1980-1990, released CO(2) potentially offset the carbon sink in forest trees by 9-18% over the entire United States. U.S. forests also experienced twice the impact before 1900 than after 1900 because of more active tropical cyclones and a larger extent of forested areas. Forest impacts were primarily located in Gulf Coast areas, particularly southern Texas and Louisiana and south Florida, while significant impacts also occurred in eastern North Carolina. Results serve as an important baseline for evaluating how potential future changes in hurricane frequency and intensity will impact forest tree mortality and carbon balance.

Dry Season Transpiration and Soil Water Dynamics in the Central Amazon.

With current observations and future projections of more intense and frequent droughts in the tropics, understanding the impact that extensive dry periods may have on tree and ecosystem-level transpiration and concurrent carbon uptake has become increasingly important. Here, we investigate paired soil and tree water extraction dynamics in an old-growth upland forest in central Amazonia during the 2018 dry season. Tree water use was assessed via radial patterns of sap flow in eight dominant canopy trees, each a different species with a range in diameter, height, and wood density. Paired multi-sensor soil moisture probes used to quantify volumetric water content dynamics and soil water extraction within the upper 100 cm were installed adjacent to six of those trees. To link depth-specific water extraction patterns to root distribution, fine root biomass was assessed through the soil profile to 235 cm. To scale tree water use to the plot level (stand transpiration), basal area was measured for all trees within a 5 m radius around each soil moisture probe. The sensitivity of tree transpiration to reduced precipitation varied by tree, with some increasing and some decreasing in water use during the dry period. Tree-level water use scaled with sapwood area, from 11 to 190 L per day. Stand level water use, based on multiple plots encompassing sap flow and adjacent trees, varied from ∼1.7 to 3.3 mm per day, increasing linearly with plot basal area. Soil water extraction was dependent on root biomass, which was dense at the surface (i.e., 45% in the upper 5 cm) and declined dramatically with depth. As the dry season progressed and the upper soil dried, soil water extraction shifted to deeper levels and model projections suggest that much of the water used during the month-long dry-down could be extracted from the upper 2-3 m. Results indicate variation in rates of soil water extraction across the research area and, temporally, through the soil profile. These results provide key information on whole-tree contributions to transpiration by canopy trees as water availability changes. In addition, information on simultaneous stand level dynamics of soil water extraction that can inform mechanistic models that project tropical forest response to drought.

Species-Specific Shifts in Diurnal Sap Velocity Dynamics and Hysteretic Behavior of Ecophysiological Variables During the 2015-2016 El Niño Event in the Amazon Forest.

Current climate change scenarios indicate warmer temperatures and the potential for more extreme droughts in the tropics, such that a mechanistic understanding of the water cycle from individual trees to landscapes is needed to adequately predict future changes in forest structure and function. In this study, we contrasted physiological responses of tropical trees during a normal dry season with the extreme dry season due to the 2015-2016 El Niño-Southern Oscillation (ENSO) event. We quantified high resolution temporal dynamics of sap velocity (Vs), stomatal conductance (gs) and leaf water potential (ΨL) of multiple canopy trees, and their correlations with leaf temperature (Tleaf) and environmental conditions [direct solar radiation, air temperature (Tair) and vapor pressure deficit (VPD)]. The experiment leveraged canopy access towers to measure adjacent trees at the ZF2 and Tapajós tropical forest research (near the cities of Manaus and Santarém). The temporal difference between the peak of gs (late morning) and the peak of VPD (early afternoon) is one of the major regulators of sap velocity hysteresis patterns. Sap velocity displayed species-specific diurnal hysteresis patterns reflected by changes in Tleaf. In the morning, Tleaf and sap velocity displayed a sigmoidal relationship. In the afternoon, stomatal conductance declined as Tleaf approached a daily peak, allowing ΨL to begin recovery, while sap velocity declined with an exponential relationship with Tleaf. In Manaus, hysteresis indices of the variables Tleaf-Tair and ΨL-Tleaf were calculated for different species and a significant difference (p < 0.01, α = 0.05) was observed when the 2015 dry season (ENSO period) was compared with the 2017 dry season ("control scenario"). In some days during the 2015 ENSO event, Tleaf approached 40°C for all studied species and the differences between Tleaf and Tair reached as high at 8°C (average difference: 1.65 ± 1.07°C). Generally, Tleaf was higher than Tair during the middle morning to early afternoon, and lower than Tair during the early morning, late afternoon and night. Our results support the hypothesis that partial stomatal closure allows for a recovery in ΨL during the afternoon period giving an observed counterclockwise hysteresis pattern between ΨL and Tleaf.

Dry and hot: the hydraulic consequences of a climate change-type drought for Amazonian trees.

How plants respond physiologically to leaf warming and low water availability may determine how they will perform under future climate change. In 2015-2016, an unprecedented drought occurred across Amazonia with record-breaking high temperatures and low soil moisture, offering a unique opportunity to evaluate the performances of Amazonian trees to a severe climatic event. We quantified the responses of leaf water potential, sap velocity, whole-tree hydraulic conductance (Kwt), turgor loss and xylem embolism, during and after the 2015-2016 El Niño for five canopy-tree species. Leaf/xylem safety margins (SMs), sap velocity and Kwt showed a sharp drop during warm periods. SMs were negatively correlated with vapour pressure deficit, but had no significant relationship with soil water storage. Based on our calculations of canopy stomatal and xylem resistances, the decrease in sap velocity and Kwt was due to a combination of xylem cavitation and stomatal closure. Our results suggest that warm droughts greatly amplify the degree of trees' physiological stress and can lead to mortality. Given the extreme nature of the 2015-2016 El Niño and that temperatures are predicted to increase, this work can serve as a case study of the possible impact climate warming can have on tropical trees.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'.

Global satellite monitoring of climate-induced vegetation disturbances.

Terrestrial disturbances are accelerating globally, but their full impact is not quantified because we lack an adequate monitoring system. Remote sensing offers a means to quantify the frequency and extent of disturbances globally. Here, we review the current application of remote sensing to this problem and offer a framework for more systematic analysis in the future. We recommend that any proposed monitoring system should not only detect disturbances, but also be able to: identify the proximate cause(s); integrate a range of spatial scales; and, ideally, incorporate process models to explain the observed patterns and predicted trends in the future. Significant remaining challenges are tied to the ecology of disturbances. To meet these challenges, more effort is required to incorporate ecological principles and understanding into the assessments of disturbance worldwide.

Large-scale wind disturbances promote tree diversity in a Central Amazon forest.

Canopy gaps created by wind-throw events, or blowdowns, create a complex mosaic of forest patches varying in disturbance intensity and recovery in the Central Amazon. Using field and remote sensing data, we investigated the short-term (four-year) effects of large (>2000 m(2)) blowdown gaps created during a single storm event in January 2005 near Manaus, Brazil, to study (i) how forest structure and composition vary with disturbance gradients and (ii) whether tree diversity is promoted by niche differentiation related to wind-throw events at the landscape scale. In the forest area affected by the blowdown, tree mortality ranged from 0 to 70%, and was highest on plateaus and slopes. Less impacted areas in the region affected by the blowdown had overlapping characteristics with a nearby unaffected forest in tree density (583 ± 46 trees ha(-1)) (mean ± 99% Confidence Interval) and basal area (26.7 ± 2.4 m(2) ha(-1)). Highly impacted areas had tree density and basal area as low as 120 trees ha(-1) and 14.9 m(2) ha(-1), respectively. In general, these structural measures correlated negatively with an index of tree mortality intensity derived from satellite imagery. Four years after the blowdown event, differences in size-distribution, fraction of resprouters, floristic composition and species diversity still correlated with disturbance measures such as tree mortality and gap size. Our results suggest that the gradients of wind disturbance intensity encompassed in large blowdown gaps (>2000 m(2)) promote tree diversity. Specialists for particular disturbance intensities existed along the entire gradient. The existence of species or genera taking an intermediate position between undisturbed and gap specialists led to a peak of rarefied richness and diversity at intermediate disturbance levels. A diverse set of species differing widely in requirements and recruitment strategies forms the initial post-disturbance cohort, thus lending a high resilience towards wind disturbances at the community level.

Carbon dioxide emitted from live stems of tropical trees is several years old.

Storage carbon (C) pools are often assumed to contribute to respiration and growth when assimilation is insufficient to meet the current C demand. However, little is known of the age of stored C and the degree to which it supports respiration in general. We used bomb radiocarbon ((14)C) measurements to determine the mean age of carbon in CO2 emitted from and within stems of three tropical tree species in Peru. Carbon pools fixed >1 year previously contributed to stem CO2 efflux in all trees investigated, in both dry and wet seasons. The average age, i.e., the time elapsed since original fixation of CO2 from the atmosphere by the plant to its loss from the stem, ranged from 0 to 6 years. The average age of CO2 sampled 5-cm deep within the stems ranged from 2 to 6 years for two of the three species, while CO2 in the stem of the third tree species was fixed from 14 to >20 years previously. Given the consistency of (14)C values observed for individuals within each species, it is unlikely that decomposition is the source of the older CO2. Our results are in accordance with other studies that have demonstrated the contribution of storage reserves to the construction of stem wood and root respiration in temperate and boreal forests. We postulate the high (14)C values observed in stem CO2 efflux and stem-internal CO2 result from respiration of storage C pools within the tree. The observed age differences between emitted and stem-internal CO2 indicate an age gradient for sources of CO2 within the tree: CO2 produced in the outer region of the stem is younger, originating from more recent assimilates, whereas the CO2 found deeper within the stem is older, fueled by several-year-old C pools. The CO2 emitted at the stem-atmosphere interface represents a mixture of young and old CO2. These observations were independent of season, even during a time of severe regional drought. Therefore, we postulate that the use of storage C for respiration occurs on a regular basis challenging the assumption that storage pools serve as substrates for respiration only during times of limited assimilation.

Large seasonal swings in leaf area of Amazon rainforests.

Despite early speculation to the contrary, all tropical forests studied to date display seasonal variations in the presence of new leaves, flowers, and fruits. Past studies were focused on the timing of phenological events and their cues but not on the accompanying changes in leaf area that regulate vegetation-atmosphere exchanges of energy, momentum, and mass. Here we report, from analysis of 5 years of recent satellite data, seasonal swings in green leaf area of approximately 25% in a majority of the Amazon rainforests. This seasonal cycle is timed to the seasonality of solar radiation in a manner that is suggestive of anticipatory and opportunistic patterns of net leaf flushing during the early to mid part of the light-rich dry season and net leaf abscission during the cloudy wet season. These seasonal swings in leaf area may be critical to initiation of the transition from dry to wet season, seasonal carbon balance between photosynthetic gains and respiratory losses, and litterfall nutrient cycling in moist tropical forests.