Amazon forest biogeography predicts resilience and vulnerability to drought.

Amazonia contains the most extensive tropical forests on Earth, but Amazon carbon sinks of atmospheric CO2 are declining, as deforestation and climate-change-associated droughts1-4 threaten to push these forests past a tipping point towards collapse5-8. Forests exhibit complex drought responses, indicating both resilience (photosynthetic greening) and vulnerability (browning and tree mortality), that are difficult to explain by climate variation alone9-17. Here we combine remotely sensed photosynthetic indices with ground-measured tree demography to identify mechanisms underlying drought resilience/vulnerability in different intact forest ecotopes18,19 (defined by water-table depth, soil fertility and texture, and vegetation characteristics). In higher-fertility southern Amazonia, drought response was structured by water-table depth, with resilient greening in shallow-water-table forests (where greater water availability heightened response to excess sunlight), contrasting with vulnerability (browning and excess tree mortality) over deeper water tables. Notably, the resilience of shallow-water-table forest weakened as drought lengthened. By contrast, lower-fertility northern Amazonia, with slower-growing but hardier trees (or, alternatively, tall forests, with deep-rooted water access), supported more-drought-resilient forests independent of water-table depth. This functional biogeography of drought response provides a framework for conservation decisions and improved predictions of heterogeneous forest responses to future climate changes, warning that Amazonia's most productive forests are also at greatest risk, and that longer/more frequent droughts are undermining multiple ecohydrological strategies and capacities for Amazon forest resilience.

How deregulation, drought and increasing fire impact Amazonian biodiversity.

Biodiversity contributes to the ecological and climatic stability of the Amazon Basin1,2, but is increasingly threatened by deforestation and fire3,4. Here we quantify these impacts over the past two decades using remote-sensing estimates of fire and deforestation and comprehensive range estimates of 11,514 plant species and 3,079 vertebrate species in the Amazon. Deforestation has led to large amounts of habitat loss, and fires further exacerbate this already substantial impact on Amazonian biodiversity. Since 2001, 103,079-189,755 km2 of Amazon rainforest has been impacted by fires, potentially impacting the ranges of 77.3-85.2% of species that are listed as threatened in this region5. The impacts of fire on the ranges of species in Amazonia could be as high as 64%, and greater impacts are typically associated with species that have restricted ranges. We find close associations between forest policy, fire-impacted forest area and their potential impacts on biodiversity. In Brazil, forest policies that were initiated in the mid-2000s corresponded to reduced rates of burning. However, relaxed enforcement of these policies in 2019 has seemingly begun to reverse this trend: approximately 4,253-10,343 km2 of forest has been impacted by fire, leading to some of the most severe potential impacts on biodiversity since 2009. These results highlight the critical role of policy enforcement in the preservation of biodiversity in the Amazon.

Genome-centric view of carbon processing in thawing permafrost.

As global temperatures rise, large amounts of carbon sequestered in permafrost are becoming available for microbial degradation. Accurate prediction of carbon gas emissions from thawing permafrost is limited by our understanding of these microbial communities. Here we use metagenomic sequencing of 214 samples from a permafrost thaw gradient to recover 1,529 metagenome-assembled genomes, including many from phyla with poor genomic representation. These genomes reflect the diversity of this complex ecosystem, with genus-level representatives for more than sixty per cent of the community. Meta-omic analysis revealed key populations involved in the degradation of organic matter, including bacteria whose genomes encode a previously undescribed fungal pathway for xylose degradation. Microbial and geochemical data highlight lineages that correlate with the production of greenhouse gases and indicate novel syntrophic relationships. Our findings link changing biogeochemistry to specific microbial lineages involved in carbon processing, and provide key information for predicting the effects of climate change on permafrost systems.

The role of ecosystem transpiration in creating alternate moisture regimes by influencing atmospheric moisture convergence.

The terrestrial water cycle links the soil and atmosphere moisture reservoirs through four fluxes: precipitation, evaporation, runoff, and atmospheric moisture convergence (net import of water vapor to balance runoff). Each of these processes is essential for sustaining human and ecosystem well-being. Predicting how the water cycle responds to changes in vegetation cover remains a challenge. Recently, changes in plant transpiration across the Amazon basin were shown to be associated disproportionately with changes in rainfall, suggesting that even small declines in transpiration (e.g., from deforestation) would lead to much larger declines in rainfall. Here, constraining these findings by the law of mass conservation, we show that in a sufficiently wet atmosphere, forest transpiration can control atmospheric moisture convergence such that increased transpiration enhances atmospheric moisture import and results in water yield. Conversely, in a sufficiently dry atmosphere increased transpiration reduces atmospheric moisture convergence and water yield. This previously unrecognized dichotomy can explain the otherwise mixed observations of how water yield responds to re-greening, as we illustrate with examples from China's Loess Plateau. Our analysis indicates that any additional precipitation recycling due to additional vegetation increases precipitation but decreases local water yield and steady-state runoff. Therefore, in the drier regions/periods and early stages of ecological restoration, the role of vegetation can be confined to precipitation recycling, while once a wetter stage is achieved, additional vegetation enhances atmospheric moisture convergence and water yield. Recent analyses indicate that the latter regime dominates the global response of the terrestrial water cycle to re-greening. Evaluating the transition between regimes, and recognizing the potential of vegetation for enhancing moisture convergence, are crucial for characterizing the consequences of deforestation as well as for motivating and guiding ecological restoration.

Asymmetric response of Amazon forest water and energy fluxes to wet and dry hydrological extremes reveals onset of a local drought-induced tipping point.

Understanding the effects of intensification of Amazon basin hydrological cycling-manifest as increasingly frequent floods and droughts-on water and energy cycles of tropical forests is essential to meeting the challenge of predicting ecosystem responses to climate change, including forest "tipping points". Here, we investigated the impacts of hydrological extremes on forest function using 12+ years of observations (between 2001-2020) of water and energy fluxes from eddy covariance, along with associated ecological dynamics from biometry, at the Tapajós National Forest. Measurements encompass the strong 2015-2016 El Niño drought and La Niña 2008-2009 wet events. We found that the forest responded strongly to El Niño-Southern Oscillation (ENSO): Drought reduced water availability for evapotranspiration (ET) leading to large increases in sensible heat fluxes (H). Partitioning ET by an approach that assumes transpiration (T) is proportional to photosynthesis, we found that water stress-induced reductions in canopy conductance (Gs ) drove T declines partly compensated by higher evaporation (E). By contrast, the abnormally wet La Niña period gave higher T and lower E, with little change in seasonal ET. Both El Niño-Southern Oscillation (ENSO) events resulted in changes in forest structure, manifested as lower wet-season leaf area index. However, only during El Niño 2015-2016, we observed a breakdown in the strong meteorological control of transpiration fluxes (via energy availability and atmospheric demand) because of slowing vegetation functions (via shutdown of Gs and significant leaf shedding). Drought-reduced T and Gs , higher H and E, amplified by feedbacks with higher temperatures and vapor pressure deficits, signaled that forest function had crossed a threshold, from which it recovered slowly, with delay, post-drought. Identifying such tipping point onsets (beyond which future irreversible processes may occur) at local scale is crucial for predicting basin-scale threshold-crossing changes in forest energy and water cycling, leading to slow-down in forest function, potentially resulting in Amazon forests shifting into alternate degraded states.

Territorial Differential Meta-Evolution: An Algorithm for Seeking All the Desirable Optima of a Multivariable Function.

Territorial Differential Meta-Evolution (TDME) is an efficient, versatile, and reliable algorithm for seeking all the global or desirable local optima of a multivariable function. It employs a progressive niching mechanism to optimize even challenging, highdimensional functions with multiple global optima and misleading local optima. This article introduces TDME and uses standard and novel benchmark problems to quantify its advantages over HillVallEA, which is the best-performing algorithm on the standard benchmark suite that has been used by all major multimodal optimization competitions since 2013. TDME matches HillVallEA on that benchmark suite and categorically outperforms it on a more comprehensive suite that better reflects the potential diversity of optimization problems. TDME achieves that performance without any problem-specific parameter tuning.

Coupling plant litter quantity to a novel metric for litter quality explains C storage changes in a thawing permafrost peatland.

Permafrost thaw is a major potential feedback source to climate change as it can drive the increased release of greenhouse gases carbon dioxide (CO2 ) and methane (CH4 ). This carbon release from the decomposition of thawing soil organic material can be mitigated by increased net primary productivity (NPP) caused by warming, increasing atmospheric CO2 , and plant community transition. However, the net effect on C storage also depends on how these plant community changes alter plant litter quantity, quality, and decomposition rates. Predicting decomposition rates based on litter quality remains challenging, but a promising new way forward is to incorporate measures of the energetic favorability to soil microbes of plant biomass decomposition. We asked how the variation in one such measure, the nominal oxidation state of carbon (NOSC), interacts with changing quantities of plant material inputs to influence the net C balance of a thawing permafrost peatland. We found: (1) Plant productivity (NPP) increased post-thaw, but instead of contributing to increased standing biomass, it increased plant biomass turnover via increased litter inputs to soil; (2) Plant litter thermodynamic favorability (NOSC) and decomposition rate both increased post-thaw, despite limited changes in bulk C:N ratios; (3) these increases caused the higher NPP to cycle more rapidly through both plants and soil, contributing to higher CO2 and CH4  fluxes from decomposition. Thus, the increased C-storage expected from higher productivity was limited and the high global warming potential of CH4 contributed a net positive warming effect. Although post-thaw peatlands are currently C sinks due to high NPP offsetting high CO2 release, this status is very sensitive to the plant community's litter input rate and quality. Integration of novel bioavailability metrics based on litter chemistry, including NOSC, into studies of ecosystem dynamics, is needed to improve the understanding of controls on arctic C stocks under continued ecosystem transition.

Understanding water and energy fluxes in the Amazonia: Lessons from an observation-model intercomparison.

Tropical forests are an important part of global water and energy cycles, but the mechanisms that drive seasonality of their land-atmosphere exchanges have proven challenging to capture in models. Here, we (1) report the seasonality of fluxes of latent heat (LE), sensible heat (H), and outgoing short and longwave radiation at four diverse tropical forest sites across Amazonia-along the equator from the Caxiuanã and Tapajós National Forests in the eastern Amazon to a forest near Manaus, and from the equatorial zone to the southern forest in Reserva Jaru; (2) investigate how vegetation and climate influence these fluxes; and (3) evaluate land surface model performance by comparing simulations to observations. We found that previously identified failure of models to capture observed dry-season increases in evapotranspiration (ET) was associated with model overestimations of (1) magnitude and seasonality of Bowen ratios (relative to aseasonal observations in which sensible was only 20%-30% of the latent heat flux) indicating model exaggerated water limitation, (2) canopy emissivity and reflectance (albedo was only 10%-15% of incoming solar radiation, compared to 0.15%-0.22% simulated), and (3) vegetation temperatures (due to underestimation of dry-season ET and associated cooling). These partially compensating model-observation discrepancies (e.g., higher temperatures expected from excess Bowen ratios were partially ameliorated by brighter leaves and more interception/evaporation) significantly biased seasonal model estimates of net radiation (Rn ), the key driver of water and energy fluxes (LE ~ 0.6 Rn and H ~ 0.15 Rn ), though these biases varied among sites and models. A better representation of energy-related parameters associated with dynamic phenology (e.g., leaf optical properties, canopy interception, and skin temperature) could improve simulations and benchmarking of current vegetation-atmosphere exchange and reduce uncertainty of regional and global biogeochemical models.

Methane dynamics regulated by microbial community response to permafrost thaw.

Permafrost contains about 50% of the global soil carbon. It is thought that the thawing of permafrost can lead to a loss of soil carbon in the form of methane and carbon dioxide emissions. The magnitude of the resulting positive climate feedback of such greenhouse gas emissions is still unknown and may to a large extent depend on the poorly understood role of microbial community composition in regulating the metabolic processes that drive such ecosystem-scale greenhouse gas fluxes. Here we show that changes in vegetation and increasing methane emissions with permafrost thaw are associated with a switch from hydrogenotrophic to partly acetoclastic methanogenesis, resulting in a large shift in the δ(13)C signature (10-15‰) of emitted methane. We used a natural landscape gradient of permafrost thaw in northern Sweden as a model to investigate the role of microbial communities in regulating methane cycling, and to test whether a knowledge of community dynamics could improve predictions of carbon emissions under loss of permafrost. Abundance of the methanogen Candidatus 'Methanoflorens stordalenmirensis' is a key predictor of the shifts in methane isotopes, which in turn predicts the proportions of carbon emitted as methane and as carbon dioxide, an important factor for simulating the climate feedback associated with permafrost thaw in global models. By showing that the abundance of key microbial lineages can be used to predict atmospherically relevant patterns in methane isotopes and the proportion of carbon metabolized to methane during permafrost thaw, we establish a basis for scaling changing microbial communities to ecosystem isotope dynamics. Our findings indicate that microbial ecology may be important in ecosystem-scale responses to global change.

Leaf reflectance spectroscopy captures variation in carboxylation capacity across species, canopy environment and leaf age in lowland moist tropical forests.

Understanding the pronounced seasonal and spatial variation in leaf carboxylation capacity (Vc,max ) is critical for determining terrestrial carbon cycling in tropical forests. However, an efficient and scalable approach for predicting Vc,max is still lacking. Here the ability of leaf spectroscopy for rapid estimation of Vc,max was tested. Vc,max was estimated using traditional gas exchange methods, and measured reflectance spectra and leaf age in leaves sampled from tropical forests in Panama and Brazil. These data were used to build a model to predict Vc,max from leaf spectra. The results demonstrated that leaf spectroscopy accurately predicts Vc,max of mature leaves in Panamanian tropical forests (R2  = 0.90). However, this single-age model required recalibration when applied to broader leaf demographic classes (i.e. immature leaves). Combined use of spectroscopy models for Vc,max and leaf age enabled construction of the Vc,max -age relationship solely from leaf spectra, which agreed with field observations. This suggests that the spectroscopy technique can capture the seasonal variability in Vc,max , assuming sufficient sampling across diverse species, leaf ages and canopy environments. This finding will aid development of remote sensing approaches that can be used to characterize Vc,max in moist tropical forests and enable an efficient means to parameterize and evaluate terrestrial biosphere models.

Seasonal and drought-related changes in leaf area profiles depend on height and light environment in an Amazon forest.

Seasonal dynamics in the vertical distribution of leaf area index (LAI) may impact the seasonality of forest productivity in Amazonian forests. However, until recently, fine-scale observations critical to revealing ecological mechanisms underlying these changes have been lacking. To investigate fine-scale variation in leaf area with seasonality and drought we conducted monthly ground-based LiDAR surveys over 4 yr at an Amazon forest site. We analysed temporal changes in vertically structured LAI along axes of both canopy height and light environments. Upper canopy LAI increased during the dry season, whereas lower canopy LAI decreased. The low canopy decrease was driven by highly illuminated leaves of smaller trees in gaps. By contrast, understory LAI increased concurrently with the upper canopy. Hence, tree phenological strategies were stratified by height and light environments. Trends were amplified during a 2015-2016 severe El Niño drought. Leaf area low in the canopy exhibited behaviour consistent with water limitation. Leaf loss from short trees in high light during drought may be associated with strategies to tolerate limited access to deep soil water and stressful leaf environments. Vertically and environmentally structured phenological processes suggest a critical role of canopy structural heterogeneity in seasonal changes in Amazon ecosystem function.

Hydraulic traits explain differential responses of Amazonian forests to the 2015 El Niño-induced drought.

Reducing uncertainties in the response of tropical forests to global change requires understanding how intra- and interannual climatic variability selects for different species, community functional composition and ecosystem functioning, so that the response to climatic events of differing frequency and severity can be predicted. Here we present an extensive dataset of hydraulic traits of dominant species in two tropical Amazon forests with contrasting precipitation regimes - low seasonality forest (LSF) and high seasonality forest (HSF) - and relate them to community and ecosystem response to the El Niño-Southern Oscillation (ENSO) of 2015. Hydraulic traits indicated higher drought tolerance in the HSF than in the LSF. Despite more intense drought and lower plant water potentials in HSF during the 2015-ENSO, greater xylem embolism resistance maintained similar hydraulic safety margin as in LSF. This likely explains how ecosystem-scale whole-forest canopy conductance at HSF maintained a similar response to atmospheric drought as at LSF, despite their water transport systems operating at different water potentials. Our results indicate that contrasting precipitation regimes (at seasonal and interannual time scales) select for assemblies of hydraulic traits and taxa at the community level, which may have a significant role in modulating forest drought response at ecosystem scales.

Cryptic phenology in plants: Case studies, implications, and recommendations.

Plant phenology-the timing of cyclic or recurrent biological events in plants-offers insight into the ecology, evolution, and seasonality of plant-mediated ecosystem processes. Traditionally studied phenologies are readily apparent, such as flowering events, germination timing, and season-initiating budbreak. However, a broad range of phenologies that are fundamental to the ecology and evolution of plants, and to global biogeochemical cycles and climate change predictions, have been neglected because they are "cryptic"-that is, hidden from view (e.g., root production) or difficult to distinguish and interpret based on common measurements at typical scales of examination (e.g., leaf turnover in evergreen forests). We illustrate how capturing cryptic phenology can advance scientific understanding with two case studies: wood phenology in a deciduous forest of the northeastern USA and leaf phenology in tropical evergreen forests of Amazonia. Drawing on these case studies and other literature, we argue that conceptualizing and characterizing cryptic plant phenology is needed for understanding and accurate prediction at many scales from organisms to ecosystems. We recommend avenues of empirical and modeling research to accelerate discovery of cryptic phenological patterns, to understand their causes and consequences, and to represent these processes in terrestrial biosphere models.

Biological processes dominate seasonality of remotely sensed canopy greenness in an Amazon evergreen forest.

Satellite observations of Amazon forests show seasonal and interannual variations, but the underlying biological processes remain debated. Here we combined radiative transfer models (RTMs) with field observations of Amazon forest leaf and canopy characteristics to test three hypotheses for satellite-observed canopy reflectance seasonality: seasonal changes in leaf area index, in canopy-surface leafless crown fraction and/or in leaf demography. Canopy RTMs (PROSAIL and FLiES), driven by these three factors combined, simulated satellite-observed seasonal patterns well, explaining c. 70% of the variability in a key reflectance-based vegetation index (MAIAC EVI, which removes artifacts that would otherwise arise from clouds/aerosols and sun-sensor geometry). Leaf area index, leafless crown fraction and leaf demography independently accounted for 1, 33 and 66% of FLiES-simulated EVI seasonality, respectively. These factors also strongly influenced modeled near-infrared (NIR) reflectance, explaining why both modeled and observed EVI, which is especially sensitive to NIR, captures canopy seasonal dynamics well. Our improved analysis of canopy-scale biophysics rules out satellite artifacts as significant causes of satellite-observed seasonal patterns at this site, implying that aggregated phenology explains the larger scale remotely observed patterns. This work significantly reconciles current controversies about satellite-detected Amazon phenology, and improves our use of satellite observations to study climate-phenology relationships in the tropics.

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.

Age-dependent leaf physiology and consequences for crown-scale carbon uptake during the dry season in an Amazon evergreen forest.

Satellite and tower-based metrics of forest-scale photosynthesis generally increase with dry season progression across central Amazônia, but the underlying mechanisms lack consensus. We conducted demographic surveys of leaf age composition, and measured the age dependence of leaf physiology in broadleaf canopy trees of abundant species at a central eastern Amazon site. Using a novel leaf-to-branch scaling approach, we used these data to independently test the much-debated hypothesis - arising from satellite and tower-based observations - that leaf phenology could explain the forest-scale pattern of dry season photosynthesis. Stomatal conductance and biochemical parameters of photosynthesis were higher for recently mature leaves than for old leaves. Most branches had multiple leaf age categories simultaneously present, and the number of recently mature leaves increased as the dry season progressed because old leaves were exchanged for new leaves. These findings provide the first direct field evidence that branch-scale photosynthetic capacity increases during the dry season, with a magnitude consistent with increases in ecosystem-scale photosynthetic capacity derived from flux towers. Interactions between leaf age-dependent physiology and shifting leaf age-demographic composition are sufficient to explain the dry season photosynthetic capacity pattern at this site, and should be considered in vegetation models of tropical evergreen forests.

Ecosystem heterogeneity and diversity mitigate Amazon forest resilience to frequent extreme droughts.

The impact of increases in drought frequency on the Amazon forest's composition, structure and functioning remain uncertain. We used a process- and individual-based ecosystem model (ED2) to quantify the forest's vulnerability to increased drought recurrence. We generated meteorologically realistic, drier-than-observed rainfall scenarios for two Amazon forest sites, Paracou (wetter) and Tapajós (drier), to evaluate the impacts of more frequent droughts on forest biomass, structure and composition. The wet site was insensitive to the tested scenarios, whereas at the dry site biomass declined when average rainfall reduction exceeded 15%, due to high mortality of large-sized evergreen trees. Biomass losses persisted when year-long drought recurrence was shorter than 2-7 yr, depending upon soil texture and leaf phenology. From the site-level scenario results, we developed regionally applicable metrics to quantify the Amazon forest's climatological proximity to rainfall regimes likely to cause biomass loss > 20% in 50 yr according to ED2 predictions. Nearly 25% (1.8 million km2 ) of the Amazon forests could experience frequent droughts and biomass loss if mean annual rainfall or interannual variability changed by 2σ. At least 10% of the high-emission climate projections (CMIP5/RCP8.5 models) predict critically dry regimes over 25% of the Amazon forest area by 2100.

Hydraulic redistribution affects modeled carbon cycling via soil microbial activity and suppressed fire.

Hydraulic redistribution (HR) of water from moist to drier soils, through plant roots, occurs world-wide in seasonally dry ecosystems. Although the influence of HR on landscape hydrology and plant water use has been amply demonstrated, HR's effects on microbe-controlled processes sensitive to soil moisture, including carbon and nutrient cycling at ecosystem scales, remain difficult to observe in the field and have not been integrated into a predictive framework. We incorporated a representation of HR into the Community Land Model (CLM4.5) and found the new model improved predictions of water, energy, and system-scale carbon fluxes observed by eddy covariance at four seasonally dry yet ecologically diverse temperate and tropical AmeriFlux sites. Modeled plant productivity and microbial activities were differentially stimulated by upward HR, resulting at times in increased plant demand outstripping increased nutrient supply. Modeled plant productivity and microbial activities were diminished by downward HR. Overall, inclusion of HR tended to increase modeled annual ecosystem uptake of CO2 (or reduce annual CO2 release to the atmosphere). Moreover, engagement of CLM4.5's ground-truthed fire module indicated that though HR increased modeled fuel load at all four sites, upward HR also moistened surface soil and hydrated vegetation sufficiently to limit the modeled spread of dry season fire and concomitant very large CO2 emissions to the atmosphere. Historically, fire has been a dominant ecological force in many seasonally dry ecosystems, and intensification of soil drought and altered precipitation regimes are expected for seasonally dry ecosystems in the future. HR may play an increasingly important role mitigating development of extreme soil water potential gradients and associated limitations on plant and soil microbial activities, and may inhibit the spread of fire in seasonally dry ecosystems.