Antonio Donato Nobre

Carbon dioxide transfer over a Central Amazonian rain forest

Tropical rain forests are among the most important and least monitored of terrestrial ecosystems. In recent years, their influence on atmospheric concentrations of carbon dioxide and water vapor has become the subject of much speculation. Here we present results from a yearlong study of CO2 fluxes at a tropical forest in central Amazonia, using the micrometeorological technique of eddy covariance. The diurnal cycle of CO2 flux was consistent with previous short-term studies in tropical rain forests, implying that the Amazonian rain forest shows a fair degree of spatial uniformity in bulk ecophysiological characteristics. Typical peak daytime photosynthesis rates were 24–28 μmol CO2 m−2 s−1, and respiration rates were 6–8 μmol CO2 m−2 s−1. There was significant seasonality in peak photosynthesis over the year, which appeared strongly correlated with soil moisture content. On the other hand, there was no evidence of strong seasonality in soil respiration. Central Amazonia has only a short, 3-month dry season, not atypical of tropical rain forest, and it is therefore likely that large areas of Amazonia exhibit significant seasonality in photosynthetic capacity. The gross primary production was calculated to be 30 t C ha−1 yr−1. An analysis of data quality is included in the appendix.

Biogeochemical cycling of carbon, water, energy, trace gases, and aerosols in Amazonia: The LBA-EUSTACH experiments

The biogeochemical cycling of carbon, water, energy, aerosols, and trace gases in the Amazon Basin was investigated in the project European Studies on Trace Gases and Atmospheric Chemistry as a Contribution to the Large-Scale Biosphere-Atmosphere Experiment in Amazonia (LBA-EUSTACH). We present an overview of the design of the project, the measurement sites and methods, and the meteorological conditions during the experiment. The main results from LBA-EUSTACH are: Eddy correlation studies in three regions of the Amazon Basin consistently show a large net carbon sink in the undisturbed rain forest. Nitrogen emitted by forest soils is subject to chemical cycling within the canopy space, which results in re-uptake of a large fraction of soil-derived NOx by the vegetation. The forest vegetation is both a sink and a source of volatile organic compounds, with net deposition being particularly important for partially oxidized organics. Concentrations of aerosol and cloud condensation nuclei (CCN) are highly seasonal, with a pronounced maximum in the dry (burning) season. High CCN concentrations from biomass burning have a pronounced impact on cloud microphysics, rainfall production mechanisms, and probably on large-scale climate dynamics.

Respiration from a tropical forest ecosystem: partitioning of sources and low carbon use efficiency

Understanding how tropical forest carbon balance will respond to global change requires knowledge of individual heterotrophic and autotrophic respiratory sources, together with factors that control respiratory variability. We measured leaf, live wood, and soil respiration, along with additional environmental factors over a 1-yr period in a Central Amazon terra firme forest. Scaling these fluxes to the ecosystem, and combining our data with results from other studies, we estimated an average total ecosystem respiration (Reco) of 7.8 μmol·m−2·s−1. Average estimates (per unit ground area) for leaf, wood, soil, total heterotrophic, and total autotrophic respiration were 2.6, 1.1, 3.2, 5.6, and 2.2 μmol·m−2·s−1, respectively. Comparing autotrophic respiration with net primary production (NPP) estimates indicated that only ∼30% of carbon assimilated in photosynthesis was used to construct new tissues, with the remaining 70% being respired back to the atmosphere as autotrophic respiration. This low ecosystem carbon use efficiency (CUE) differs considerably from the relatively constant CUE of ∼0.5 found for temperate forests. Our Reco estimate was comparable to the above-canopy flux (Fac) from eddy covariance during defined sustained high turbulence conditions (when presumably Fac = Reco) of 8.4 (95% ci = 7.5– 9.4). Multiple regression analysis demonstrated that ∼50% of the nighttime variability in Fac was accounted for by friction velocity (u*, a measure of turbulence) variables. After accounting for u* variability, mean Fac varied significantly with seasonal and daily changes in precipitation. A seasonal increase in precipitation resulted in a decrease in Fac, similar to our soil respiration response to moisture. The effect of daily changes in precipitation was complex: precipitation after a dry period resulted in a large increase in Fac, whereas additional precipitation after a rainy period had little effect. This response was similar to that of surface litter (coarse and fine), where respiration is greatly reduced when moisture is limiting, but increases markedly and quickly saturates with an increase in moisture.

Patterns of water and heat flux across a biome gradient from tropical forest to savanna in Brazil

[1] We investigated the seasonal patterns of water vapor and sensible heat flux along a tropical biome gradient from forest to savanna. We analyzed data from a network of flux towers in Brazil that were operated within the Large-Scale Biosphere-Atmosphere Experiment in Amazonia (LBA). These tower sites included tropical humid and semideciduous forest, transitional forest, floodplain (with physiognomies of cerrado), and cerrado sensu stricto. The mean annual sensible heat flux at all sites ranged from 20 to 38 Wm 2 , and was generally reduced in the wet season and increased in the late dry season, coincident with seasonal variations of net radiation and soil moisture. The sites were easily divisible into two functional groups based on the seasonality of evaporation: tropical forest and savanna. At sites with an annual precipitation above 1900 mm and a dry season length less than 4 months (Manaus, Santarem and Rondonia), evaporation rates increased in the dry season, coincident with increased radiation. Evaporation rates were as high as 4.0 mm d 1 in these evergreen or semidecidous forests. In contrast, ecosystems with precipitation less than 1700 mm and a longer dry season (Mato Grosso, Tocantins

Respiration from coarse wood litter in central Amazon forests

Respiration from coarse litter (trunks and large branches >10 cm diameter) was studied in central Amazon forests. Respiration ratesvaried over almost two orders of magnitude (1.003–0.014 µg Cg−1 C min−1, n = 61), and weresignificantly correlated with wood density (r2adj= 0.42), and moisture content (r2adj= 0.39). Additional samples taken from a nearby pasture indicatedthat wood moisture content was the most important factor controllingrespiration rates across sites (r2adj =0.65). Based on average coarse litter wood density and moisture content,the mean long-term carbon loss rate due to respiration was estimated tobe 0.13 yr−1 (range of 95% prediction interval(PI) = 0.11–0.15 yr−1). Comparing meanrespiration rate with mean mass loss (decomposition) rate from aprevious study, respiratory emissions to the atmosphere from coarselitter were predicted to be 76% (95% PI =65–88%) of total carbon loss, or about 1.9 (95% PI= 1.6–2.2) Mg C ha−1yr−1. Optimum respiration activity corresponded toabout 2.5 g H2O g−1 dry wood, and severelyrestricted respiration to < 0.5 g H2O g−1dry wood. Respiration from coarse litter in central Amazon forests iscomparable in magnitude to decomposing fine surface litter (e.g. leaves,twigs) and is an important carbon cycling component when characterizingheterotrophic respiration budgets and net ecosystem exchange(NEE).

ECOLOGICAL RESEARCH IN THE LARGE-SCALE BIOSPHERE– ATMOSPHERE EXPERIMENT IN AMAZONIA: EARLY RESULTS

The Large-scale Biosphere-Atmosphere Experiment in Amazonia (LBA) is a multinational, interdisciplinary research program led by Brazil. Ecological studies in LBA focus on how tropical forest conversion, regrowth, and selective logging influence carbon storage, nutrient dynamics, trace gas fluxes, and the prospect for sustainable land use in the Amazon region. Early results from ecological studies within LBA emphasize the var- iability within the vast Amazon region and the profound effects that land-use and land- cover changes are having on that landscape. The predominant land cover of the Amazon region is evergreen forest; nonetheless, LBA studies have observed strong seasonal patterns in gross primary production, ecosystem respiration, and net ecosystem exchange, as well as phenology and tree growth. The seasonal patterns vary spatially and interannually and evidence suggests that these patterns are driven not only by variations in weather but also by innate biological rhythms of the forest species. Rapid rates of deforestation have marked the forests of the Amazon region over the past three decades. Evidence from ground-based surveys and remote sensing show that substantial areas of forest are being degraded by logging activities and through the collapse of forest edges. Because forest edges and logged forests are susceptible to fire, positive feedback cycles of forest degradation may be initiated by land-use-change events. LBA studies indicate that cleared lands in the Amazon, once released from cultivation or pasture usage, regenerate biomass rapidly. However, the pace of biomass accumulation is dependent upon past land use and the depletion of nutrients by unsustainable land-management practices. The challenge for ongoing research within LBA is to integrate the recognition of diverse patterns and processes into general models for prediction of regional ecosystem function.

THE ROBUSTNESS OF EDDY CORRELATION FLUXES FOR AMAZON RAIN FOREST CONDITIONS

We analyzed errors and uncertainties in time-integrated eddy correlation data for sites in the Amazon. A well-known source of potential error in eddy correlation is through possible advective losses of CO2 emissions during calm nights. There are also questions related to the treatment of low frequencies, non-horizontal flow, and uncertainties in, e.g., corrections for tube delay and frequency loss, as well as the effect of missing data. In this study, we systematically explore these issues for the specific situation of flux mea- surements at two Amazon forest sites. Results indicate that, for this specific environment with tall forest and tall towers, errors and uncertainties caused by data spikes, delay cor- rections, and high-frequency loss are small (,3% on an annual basis). However, sensitivities to the treatment of low frequencies and non-horizontal flow can be large, especially if the landscape is not homogeneous. Given that there is no consensus on methodology here, this represents an uncertainty of 10-25% on annual total carbon uptake. The other large un- certainty is clearly in the nighttime fluxes. Two different ways to evaluate the validity of these fluxes resulted in at least a 100% difference of annual totals. Finally, we show that uncertainty (standard errors) associated with data gaps can be reduced to ,0.5 Mg·ha 21 ·yr 21 if data are covering at least half of the time, with random spread. Overall uncertainty, on annual CO2 fluxes, excluding the nighttime dilemma, is estimated at 612% (central Amazon site) to 632% (southwest Amazon site). Additionally, the nighttime uncertainty is of similar magnitude as the time-integrated fluxes themselves.

TURBULENCE STATISTICS ABOVE AND WITHIN TWO AMAZON RAIN FOREST CANOPIES

The turbulence structure in two Amazon rain forestswas characterised for a range of above-canopystability conditions, and the results compared withprevious studies in other forest canopies and recenttheory for the generation of turbulent eddies justabove forest canopies. Three-dimensional wind speedand temperature fluctuation data were collectedsimultaneously at up to five levels inside and abovetwo canopies of 30–40 m tall forests, during threeseparate periods. We analysed hourly statistics, jointprobability distributions, length scales, spatialcorrelations and coherence, as well as power spectraof vertical and horizontal wind speed.The daytime results show a sharp attenuation ofturbulence in the top third of the canopies, resultingin very little movement, and almost Gaussianprobability distributions of wind speeds, in the lowercanopy. This contrasts with strongly skewed andkurtotic distributions in the upper canopy. At night,attenuation was even stronger and skewness vanishedeven in the upper canopy. Power spectral peaks in thelower canopy are shifted to lower frequencies relativeto the upper canopy, and spatial correlations andcoherences were low throughout the canopy. Integrallength scales of vertical wind speed at the top of thecanopy were small, about 0.15 h compared to avalue of 0.28 h expected from the shear lengthscale at the canopy top, based on the hypothesis that theupper canopy air behaves as a plane mixing layer. Allthis suggests that, although exchange is not totallyinhibited, tropical rain forest canopies differ from other forests in that rapid, coherentdownward sweeps do not penetrate into the lowercanopy, and that length scales are suppressed. This isassociated with a persistent inversion of stability inthat region compared to above-canopy conditions. Theinversion is likely to be maintained by strong heatabsorption in the leaves concentrated near thecanopy top, with the generally weak turbulence beingunable to destroy the temperature gradients over thelarge canopy depth.

NOCTURNAL ACCUMULATION OF CO2 UNDERNEATH A TROPICAL FOREST CANOPY ALONG A TOPOGRAPHICAL GRADIENT

Flux measurements of carbon dioxide and water vapor above tropical rain forests are often difficult to interpret because the terrain is usually complex. This complexity induces heterogeneity in the surface but also affects lateral movement of carbon dioxide (CO2) not readily detected by the eddy covariance systems. This study describes such variability using measurements of CO2 along vertical profiles and along a toposequence in a tropical rain forest near Manaus, Brazil. Seasonal and diurnal variation was recorded, with atmospheric CO2 concentration maxima around dawn, generally higher CO2 build-up in the dry season and stronger daytime CO2 drawdown in the wet season. This variation was reflected all along the toposequence, but the slope and valley bottom accumulated clearly more CO2 than the plateaus, depending on atmospheric stability. Particularly during stable nights, accumulation was along lines of equal altitude, suggesting that large amounts of CO2 are stored in the valleys of the landscape. Flushing of this store only occurs during mid-morning, when stored CO2 may well be partly transported back to the plateaus. It is clear that, for proper interpretation of tower fluxes in such complex and actively respiring terrain, the horizontal variability of storage needs to be taken into account not only during the night but also during the mornings.

Dry-season greening of Amazon forests

Evidence from ecological studies1,2, eddy flux towers3–5, and satellites3,6 shows that many tropical forests ‘green up’ during higher sunlight annual dry seasons, suggesting they are more limited by light than water. Morton et al.7 reported that satellite-observed dry-season green up in Amazon forests is an artefact of seasonal variations in sunsensor geometry. However, here we argue that even after artefact correction, data from Morton et al. show statistically significant increases in canopy greenness during the dry season. Integrating corrected satellite with ground observations indicates that dry-season forest greening is prevalent in Amazonia, probably reflecting large-scale seasonal upregulation of photosynthesis by canopy leaf dynamics. There is a reply to this Brief Communication Arising by Morton, D. C. et al. Nature 531, http://dx.doi.org/10.1038/nature16458 (2016). Variations in sun-sensor geometry induce artefacts in remotely sensed vegetated surfaces8. Satellite studies thus typically use models to correct artefacts (for example, Moderate Resolution Imaging Spectroradiometer (MODIS) leaf area index9, and multiangle implementation of atmospheric correction (MAIAC) enhanced vegetation index10 (EVI)) or compositing algorithms designed to minimize artefacts (standard MODIS EVI11). Morton et al.7 used a modelling approach to correct MODIS satellite data, which they state removed seasonal changes in surface reflectance, and redefined debates over how climate controls forest productivity in the Amazon. Setting aside arguments that the remote sensing analysis by Morton et al. is faulty12, we take their correction7 at face value, and ask two questions. First, we ask whether the corrected results support their core conclusion that dry-season green up, previously observed by MODIS EVI, is eliminated. The hypothesis that Amazon forests green up in the dry season3 can be rigorously evaluated by formal statistical tests. Morton et al.7 showed that their correction reduces estimated dry season green up, Δ EVI (the EVI change during the dry season, Δ EVI = October EVI − June EVI; figure 3 in ref. 7 and Fig. 1). As the corrected mean Δ EVI was smaller than an a priori estimate of error for individual EVI observations, they concluded that the corrected mean Δ EVI was indistinguishable from zero. We find that this comparison, however, is not appropriate for assessing whether corrected EVI can resolve a basin-wide green up. The correct comparison, of mean Δ EVI to the error of the mean of the whole population of observations, is accomplished with standard statistical tests that lever the probability theory ‘law of large numbers’13. For example, the 95% confidence interval13 for basin-wide mean of corrected Δ EVI significantly excludes zero (Fig. 1). Alternatively, the corrected Δ EVI distribution7 can be compared to the binomial distribution generated by the null hypothesis that pixels are equally likely to exhibit positive or negative Δ EVI (Fig. 1), which is analogous to treating ‘green up’ or ‘brown down’ as the outcome of the flip of a fair coin. These standard tests show that corrected Δ EVI7, though substantially smaller in magnitude than uncorrected, nonetheless shows a highly significant increase in forest greenness. Second, we ask whether the smaller, but statistically significant, green up seen in the data from Morton et al. (Fig. 1) is biologically meaningful in terms of consistency with mechanisms and magnitude of seasonal changes in canopy-scale biophysics observed on the ground. We find that at an intensively measured site, significant dry-season increases in leaf area index are driven by coordinated flushing of new leaves, which have higher near-infrared reflectance (Fig. 2a) (mechanisms that Morton et al.7 hypothesized could drive true increases in satelliteobserved EVI). Leaf flushing is followed, after 1 to 2 months, by increases in photosynthetic capacity derived from CO2 fluxes measured at eddy flux towers (Fig. 2a). This correlation—1-month-lagged photosynthetic capacity with leaf area index, r = + 0.90, and with MAIAC EVI, r = + 0.89, where r is Pearson’s correlation coefficient, and the time lag is for new leaves to develop their photosynthetic capacity14—establishes a link between eddy flux measurements and biophysical properties observable from satellites. On the basis of this link, we find that increases in dry-season greenness seen by corrected EVI products (whether those of ref. 7 or the MAIAC EVI of Lyapustin et al.10; Fig. 2b) are real and consistently correlated with photosynthetic capacity increases seen at towers within the region analysed by Morton et al. (including adjustment for possible sun-angle effects on canopy illumination). This suggests that even the smaller corrected Δ EVI7 reflects mechanisms of canopy changes actually observed on the ground, and is therefore biologically meaningful. The analysis in Morton et al.7 is, notably, stimulating a productive re-examination of the methodology, meaning and magnitude of remote sensing indices, their artefacts, and their relation to field studies on the ground6,12. However, we believe that the primary substantive finding of Morton et al. of consistent canopy structure and greenness is incorrect. Both satellite remote sensing and ground-based observations show dry-season increases in greenness and biophysical properties associated with canopy photosynthesis across scales, from individual leaves to ecosystems to regions, in support of the conclusion that Amazon forests green up with sunlight in the dry season3,14.