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FIRE AS A FUNDAMENTAL ECOLOGICAL PROCESS: RESEARCH ADVANCES AND FRONTIERS

The Science
The Future of Fire Consortium (FFC), composed of ecologists from around the globe with expertise ranging from paleoecology to atmospheric science, identified critical research frontiers in six areas of fire ecology and three emergent themes for future fire ecology research including: (1) the need to study fire across temporal and spatial scales, (2) the need to assess the mechanisms underlying a variety of feedbacks in the fire system, and (3) the need to improve representation of fire in a range of modeling contexts.

The Impact
As fire regimes and our relationships with fire continue to change, prioritizing these research areas and emergent themes will facilitate understanding of the ecological causes and consequences of future fires and fire management. 

Summary
In this review, critical research frontiers in six areas of fire ecology were identified: (1) expanding concepts of fire regimes, (2) understanding changing fire regimes, (3, 4) examining fire effects on aboveground and belowground ecology, (5) increasing fuels characterization in determining fire behavior, and (6) improving representation of fire processes in a variety of modeling contexts. Within these areas, three emergent themes for future fire ecology research including: (1) the need to study fire across temporal and spatial scales, (2) the need to assess the mechanisms underlying a variety of feedbacks in the fire system, and (3) the need to improve representation of fire in a range of modeling contexts. This review offers guidance to further our effort to understand both the fundamental role of fire in ecological systems and the human role in shaping fire activity. As fire regimes and our relationships with fire continue to change, prioritizing these research areas and emergent themes will facilitate understanding of the ecological causes and consequences of future fires and fire management.

Figure. Examples of the diversity of fire activity on Earth. Although these represent single fire events, the cumulative properties of fire events over time characterize a fire regime. (a) boreal Alaska, USA (b) prairie Kans., USA (c) oak savanna Minn., USA (d) Mediterranean biome Catalonia, Spain (e) Tanguro, Brazil (f) conifers Mont., USA (g) pine savanna Fla., USA (h) tundra Alaska, USA.

 

 

 

 

 

Contacts (BER PM): Daniel Stover, SC-23.1, Daniel.Stover@science.doe.gov (301-903-0289)

PI Contact: Kendra McLauchlan, Kansas State University, mclauch@ksu.edu

Funding
This manuscript is a product of discussions at the Future of Fire workshop held in November 2017 in Boulder, Colorado, USA. Support for this workshop was provided by NSF‐DEB‐1743681 to K.K.McLauchlan and A.J.Tepley. J.K. Shuman was supported by Next-Generation Ecosystem Experiments (NGEE Tropics), a project supported by the Office of Biological and Environmental Research in the Department of Energy, Office of Science.

Publications
McLauchlan, K. K., P. E. Higuera, J. Miesel, B. M. Rogers, J. Schweitzer, J. K. Shuman, A. Tepley, J. M. Varner, T. T. Veblen, et al., 2020, “Fire as a fundamental ecological process: research advances and frontiers.” Journal of Ecology 00:1-23 doi: 10.1111/1365-2745.13403

Related Links
Article URL: https://besjournals.onlinelibrary.wiley.com/doi/full/10.1111/1365-2745.13403

ROLE OF TREE MORTALITY IN FOREST RESPONSE TO RISING CO2

The Science
Researchers used simulations to explore how size- and age-dependent mortality of trees will affect changes in forest carbon storage in response to rising CO2. They found that faster growth as a result of increased CO2 caused increases in forest biomass that were twice as large when mortality was age-dependent compared with size-dependent.

The Impact
Understanding how forests will respond to rising CO2 is critical for predicting changes in the Earth’s climate. The results of this study highlight in particular the importance of understanding large tree mortality.

Summary
Little is known about how the probability of death changes as trees get older and larger. However, as rising CO2 is expected to cause trees to grow faster, it is important that we understand whether this will lead to trees growing larger, or whether they will continue to die at the same size, but in less time. This has important implications for the amount of carbon that is stored in forest ecosystems, and how long it is stored. Researchers used simulations to explore how different mechanisms of tree mortality could affect forest carbon storage. They found that increased growth from simulated increases in CO2 caused increases in biomass that were twice as large when mortality was age-dependent compared with size-dependent. Further, they found a much larger decrease in carbon storage time when mortality was size-dependent, as trees move through their life cycles more rapidly.

Figure. We used a reduced complexity form of FATES in which woody net primary productivity (NPP) increased through time and mortality was either constant, size- or age-dependent. We calculated changes in aboveground biomass and carbon turnover times relative to controls with constant woody NPP.

 

 

 

Contacts (BER PM): Daniel Stover, SC-23.1,  Daniel.Stover@science.doe.gov (301-903-0289)

PI Contact: Charles Koven, Lawrence Berkeley National Laboratory, cdkoven@lbl.gov

Funding
This research was supported as part of the Next Generation Ecosystem Experiments-Tropics, funded by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research. CK also acknowledges support from the DOE Early Career Research Program. LBNL is managed and operated by the Regents of the University of California under prime contract number DE-AC02-05CH11231. RF acknowledges the support of the National Center for Atmospheric Research, which is funded by the National Science Foundation.

Publications
Needham, J. F., Chambers, J., Fisher, R., Knox, R., Koven, C. D., “Forest response to simulated elevated CO2 under alternate hypotheses of size- and age-dependent mortality.” Global Change Biology, 2020.

STIMULATION OF ISOPRENE EMISSIONS AND ELECTRON TRANSPORT RATES ARE A KEY MECHANISM OF THERMAL TOLERANCE IN THE TROPICAL SPECIES VISMIA GUIANENSIS

The Science
The increase in global temperature directly affects the net primary productivity of the forest. High temperatures can influence the rates of chemical reactions in cells, such as photosynthesis, electron transport and isoprene emissions. In this study, we asked the following research questions:
1) Are reductions in photosynthesis at high leaf temperatures in tropical forests linked to a reduction in stomatal conductance (gs) rather than direct negative temperature effects on photosynthesis?
2) Do current isoprene emission models that link photosynthetic electron transport rates to isoprene emissions rates as a function of temperature hold true in tropical species?
3) What is the role of isoprene on thermal tolerance of photosynthesis at high temperatures?
We discovered that in a “thermophile” early successional species in the Amazon, photosynthetic electron transport rates increased linearly with temperature in concert with isoprene emissions, even as stomatal conductance and net photosynthetic carbon fixation declined. We observed the highest temperatures of continually increasing isoprene emissions yet reported and that blocking isoprene production induced a temperature-dependent loss of photosynthetic capacity.  

The Impact
Tropical forests absorb large amounts of atmospheric CO2, but substantial decreases in tropical forest gross primary productivity have been repeatedly demonstrated in the Amazon basin during periodic widespread drought associated with high temperature. Therefore, the physiological mechanisms through which tropical forests respond to high temperature are critically important to understand. While extreme warming will decrease stomatal conductance and net photosynthesis in tropical species, our observations support a thermal tolerance mechanism where the maintenance of high photosynthetic capacity under extreme warming is assisted by the simultaneous stimulation of photosynthetic electron transport (ETR) and metabolic pathways that consume the direct products of ETR including photorespiration and the biosynthesis of thermoprotective isoprenoids. Our results demonstrate that models which link isoprene emissions to the rate of ETR are ideal for tropical species and provide necessary “ground-truthing” for simulations of the large predicted increases in tropical isoprene emissions with climate warming.

Summary
Tropical forests absorb large amounts of atmospheric CO2 through photosynthesis, but high surface temperatures suppress this absorption while promoting isoprene emissions. While mechanistic isoprene emission models predict a tight coupling to ETR as a function of temperature, direct field observations of these phenomena are lacking in the tropics and are necessary to assess the impact of a warming climate on global isoprene emissions. Here, we demonstrate that in the early successional species Vismia guianensis in the central Amazon, ETR rates increased with temperature in concert with isoprene emissions, even as gs and net photosynthetic carbon fixation (Pn) declined. We observed the highest temperatures of continually increasing isoprene emissions yet reported (50°C). While Pn showed an optimum value of 32.6 ± 0.4°C, isoprene emissions, ETR, and the oxidation state of PSII reaction centers (qL) increased with leaf temperature with strong linear correlations for ETR (ƿ = 0.98) and qL (ƿ = 0.99) with leaf isoprene emissions. In contrast, other photoprotective mechanisms, such as non-photochemical quenching (NPQ), were not activated at elevated temperatures. Inhibition of isoprenoid biosynthesis repressed Pn at high temperatures through a mechanism that was independent of stomatal closure. While extreme warming will decrease gs and Pn in tropical species, our observations support a thermal tolerance mechanism where the maintenance of high photosynthetic capacity under extreme warming is assisted by the simultaneous stimulation of ETR and metabolic pathways that consume the direct products of ETR including photorespiration and the biosynthesis of thermoprotective isoprenoids. Our results confirm that models which link isoprene emissions to the rate of ETR hold true in tropical species and provide necessary “ground-truthing” for simulations of the large predicted increases in tropical isoprene emissions with climate warming.

Figure 1. Proposed biochemical model of the acclimation to high temperature stress through the consumption of photosynthetic energy (ATP) and reducing equivalents (NADPH) through the activation of the isoprenoid pathway together in parallel with other coupled biochemical pathways (adapted from Voss et al., 2013 and Morfopoulos et al., 2014).  O2: oxygen; CO2: carbon dioxide; H2O: water; ATP: adenosine triphosphate; NADPH: Nicotinamide-Adenine-Dinucleotide-Phosphate; AOX: alternative oxidases of mitochondria.

Figure 2. Graphical representation the influence of proposed surface temperature impacts on plant physiological processes influencing terrestrial ecosystem carbon cycling from leaf to global scales. NPP: Net Primary Productivity, Gs: Stomatal Conductance, ETR: Electron Transport Rate, qL: Fraction of PSII centers that are oxidized, CO2: carbon dioxide.

 

PI Contact: Kolby Jardine, Earth and Environmental Sciences Area, Lawrence Berkeley National Laboratory, One Cyclotron Road, 84-155 Berkeley, CA, USA 94720, kjjardine@lbl.gov

Contacts (BER PM): Daniel Stover, SC-23.1, Daniel.Stover@science.doe.gov (301-903-0289) 

Funding
This material is based upon work supported as part of the Next Generation Ecosystem Experiments-Tropics (NGEE-Tropics) funded by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research`s Terrestrial Ecosystem Science Program through contract No. DE-AC02-05CH11231 to Lawrence Berkeley National Laboratory, DE-AC05-00OR22725 to Oak Ridge National Laboratory, and DE-SC0012704 to Brookhaven National Laboratory. Additional funding for this research was provided by the Brazilian Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). Logistical and scientific support is acknowledged by the Forest Management laboratory (LMF), Climate and Environment (CLIAMB), and Large Scale Biosphere-Atmosphere (LBA) programs at the National Institute for Amazon Research (INPA).

Publications
Rodrigues T, Baker C, Walker A, McDowell N, Rogers A, Higuchi N, Chambers J, Jardine K (2020) Stimulation of isoprene emissions and electron transport rates as a key mechanism of thermal tolerance in the tropical species Vismia guianensis, Global Change Biology. https://doi.org/10.1111/gcb.15213

Related Links
Data DOIs: Jardine K; Rodrigues T (2019): Isoprene, Chlorophyll fluorescence, and leaf temperature data from Manaus, Brazil, 2017 – 2018. 1.0. NGEE Tropics Data Collection. (dataset). http://dx.doi.org/10.15486/ngt/1570407

WIDESPREAD SHIFTS IN TROPICAL WATER AVAILABILITY FOR PLANTS IDENTIFIED DURING EL NIÑO

The Science
El Niño is a complex part of the climate system with extreme events occurring every 15 to 20 years that have major impacts on global water supplies. This study combined data derived from on-the-ground measurements and a suite of global datasets to determine where impacts on soil moisture from such events were most severe in the tropics and to explore possible links of these changes to other large-scale weather patterns.

The Impact
The study will provide a better understanding of where changes in moisture availability for plants are most severe in the tropics during El Niño to enable better predictions of impacts on the food supply and feedbacks of water from land back to the atmosphere through evapotranspiration. This can be used to guide decisions on where changes need to be made to water management systems during El Niño to offset expected decreases in moisture availability for crops and to improve global Earth system model predictions.

Summary
El Niño is an important part of the climate system that has widespread impacts on global water resource availability. This study employed a combination of modeled soil moisture datasets and on-the-ground measurements to determine what changes to expect for soil moisture during severe El Niño events. Supplemental datasets of evapotranspiration and precipitation were used to explore the possible link of these changes to non-El Niño related weather events. The analysis was focused on the humid tropics, which is important not only because of the higher severity of impacts due to its closer proximity to the El Niño source region, but also because historical observations in this region are generally sparse, which limits the ability to predict what will happen during an El Niño. Results indicate that the northern Amazon basin, as well as maritime regions of southeastern Asia, Indonesia and New Guinea will experience the largest reductions in soil moisture during the next severe El Niño. Information gleaned from the study can be used to develop better predictions of potential impacts on plants or the food supply so mitigation measures can be implemented, or to improve the understanding of tropical moisture feedbacks and how this might impact regional water supplies or the climate system.


Figure. Cluster analysis of mean October to December soil moisture changes during “Super El Niño” events. Red cell colors indicate regions where decrease was most severe.

Contacts (BER PM): Daniel Stover, SC-23.1, Daniel.Stover@science.doe.gov (301-903-0289) 

PI Contact: Jeffrey Chambers, Lawrence Berkeley National Laboratory, jchambers@lbl.org (510-495-2932)

Funding
This project was supported as part of the Next-Generation Ecosystem Experiments – Tropics, funded by the United States Department of Energy Office of Science Office of Biological and Environmental Research through the Terrestrial Ecosystem Science program.

Publications
Solander, B.D. Newman and C. Xu, et al., “The pantropical response of soil moisture to El Niño.” Hydrology and Earth System Sciences 24, 2303-2322 (2020). https://doi.org/10.5194/hess-24-2303-2020.

Related Links
Associated data that was used for this research was uploaded to the Next-Generation Ecosystem Experiments – Tropics online data archive (NGT0132-NGT0146 & NGT0148: https://ngt-data.lbl.gov/)

LEAF ISOPRENE AND MONOTERPENE EMISSION DISTRIBUTION IN THE 5 MOST ABUNDANT TREE GENERA IN THE AMAZON BASIN

The Science
1. Tropical forests are acknowledged to be the largest global source of isoprene (C5H8) and monoterpenes (C10H16) emissions, with current synthesis studies suggesting few tropical species emit isoprenoids (20-38%) and do so with highly variable emission capacities, including within the same genera.
2. This apparent lack of a clear phylogenetic thread has created difficulties both in linking isoprenoid function with evolution and for the development of accurate biosphere-atmosphere models.
3. Here, a field-portable system was developed for the identification and quantification of isoprene and monoterpene emissions from leaves in parallel with leaf physiological measurements including photosynthesis and transpiration.
4. The system will enable the characterization of carbon and energy allocation to the biosynthesis and emission of isoprenoids linked with photosynthesis and their biological and environmental sensitivities (e.g. light, temperature, CO2).
5. Using this system, a systematic isoprenoid emission study was conducted across the five most abundant tree genera in the Amazon.

The Impact
1. The hyperdominant species (69) across the top five most abundant genera, which make up about 50% of all individuals in the Basin, showed high abundance of isoprenoid emitters (isoprene: 63.8%; monoterpenes: 17.4%; both 11.6%). Among the abundant genera, only Pouteria had a low frequency of isoprene emitting species (15.8% of 19 species). In contrast, Protium, Licania, Inga, and Eschweilera were rich in isoprene emitting species (83.3% of 12 species, 61.1% of 18 species, 100% of 8 species, and 100% of 12 species, respectively).
2. In every genus, species with light-dependent isoprene emissions together with β-ocimene emissions were observed.
3. These observations demonstrate that isoprene biological function and phylogenetic relationship studies cannot be conducted without including monoterpenes. The findings support the emerging view of the evolution of isoprene synthases from ocimene synthases.
4. The finding (i.e. 64% of species observed vs 20% suggested in the literature) improves understanding of isoprenoid function-evolution relationships and represents a base for the development of more accurate Earth System Models.

Summary
Tropical forests are acknowledged to be the largest global source of isoprene (C5H8) and monoterpenes (C10H16) emissions, with current synthesis studies suggesting few tropical species emit isoprenoids (20-38%) and do so with highly variable emission capacities, including within the same genera. This apparent lack of a clear phylogenetic thread has created difficulties both in linking isoprenoid function with evolution and for the development of accurate biosphere-atmosphere models. Here, we present a systematic emission study of “hyperdominant” tree species in the Amazon Basin. Across 162 individuals, distributed among 25 botanical families and 113 species, isoprenoid emissions were widespread among both early and late successional species (isoprene: 61.9% of the species; monoterpenes: 15.0%; both isoprene and monoterpenes: 9.7%). The hyperdominant species (69) across the top five most abundant genera, which make up about 50% of all individuals in the Basin, had a similar abundance of isoprenoid emitters (isoprene: 63.8%; monoterpenes: 17.4%; both 11.6%). Among the abundant genera, only Pouteria had a low frequency of isoprene emitting species (15.8% of 19 species). In contrast, Protium, Licania, Inga, and Eschweilera were rich in isoprene emitting species (83.3% of 12 species, 61.1% of 18 species, 100% of 8 species, and 100% of 12 species, respectively). Light response curves of individuals in each of the five genera showed light-dependent, photosynthesis-linked emission rates of isoprene and monoterpenes. Importantly, in every genus, we observed species with light-dependent isoprene emissions together with monoterpenes including β-ocimene. These observations support the emerging view of the evolution of isoprene synthases from β-ocimene synthases. Our results have important implications for understanding isoprenoid function-evolution relationships and the development of more accurate Earth System Models. 

Figure 1. Images of the coupled leaf portable photosynthesis (Li6400XT) and volatile emission autosampler (Less-P) system developed in this study for the combined analysis of net photosynthesis and volatile isoprenoid emissions at remote field site locations in the Amazon forest.

Figure 2. Graphical illustration of the biochemical, ecological, and atmospheric roles of volatile isoprenoids (isoprene and monoterpenes) within plants, ecosystems, and the atmosphere. Volatile isoprenoids protect photosynthesis during abiotic stress, are involved in multi-trophic interactions within ecosystems, and following atmospheric oxidation, impact climate through influences over secondary organic aerosol (SOA) and cloud condensation nuclei (CCN) lifecycles in the troposphere.

Figure 3. Schematic showing biosphere-atmosphere interactions and climate feedbacks mediated by exchange of CO2 and biogenic volatile organic compounds (BVOCs).

 

PI Contact: Kolby Jardine, Earth and Environmental Sciences Area, Lawrence Berkeley National Laboratory, One Cyclotron Road, 84-155, Berkeley, CA, USA 94720, kjjardine@lbl.gov

Contact (BER PM): Daniel Stover, SC-23.1, Daniel.Stover@science.doe.gov (301-903-0289) 

Funding
This material is based upon work supported as part of the Next Generation Ecosystem Experiments-Tropics (NGEE-Tropics) funded by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research through contract No. DE-AC02-05CH11231 to LBNL, as part of DOE’s Terrestrial Ecosystem Science Program. Funding for the data analysis and manuscript preparation was provided by the DOE Office of Science Early Career Research Program (FY18 DOE National Laboratory Announcement Number: LAB 17-1761), Topic: Plant Systems for the Production of Biofuels and Bioproducts. Graduate student support was supported by the National Council for Scientific and Technological Development (CNPq) in Brazil. Logistical and scientific support is acknowledged by the Forest Management (MF), Climate and Environment (CLIAMB), and Large-Scale Biosphere-Atmosphere (LBA) programs at the National Institute for Amazon Research (INPA).

Publications
1. Jardine K, Zorzanelli R, Gimenez B, Piva L, Teixeira A, Fontes C, Robles E, Chambers J, Higuchi N, Martin S (2020) Leaf isoprene and monoterpene emission distribution in the 5 most abundant tree genera in the Amazon Basin, Phytochemistry, Vol. 175, 112366. https://doi.org/10.1016/j.phytochem.2020.112366
2. Jardine K, Zorzanelli R, Gimenez B, Robles E, Piva L (2020) Development of a portable leaf photosynthesis and volatile organic compounds emission system, MethodsX, Vol. 7, 100880 https://doi.org/10.1016/j.mex.2020.100880
3. Jardine, K., Zorzanelli R., Gimenez B., Robles E., Piva L.(2020) Leaf gas exchange and volatile isoprenoid emission dataset of hyperdominant tree genera in the Amazon forest, Phytochemistry Data in Brief.

Related Links
Data DOIs:
1. Jardine K; Zorzanelli R; Gimenez B; Robles E; Rosa L (2020): Leaf isoprene and monoterpene emission data-set across hyperdominant tree genera in the Amazon basin. 1.0. NGEE Tropics Data Collection. (dataset). http://dx.doi.org/10.15486/ngt/1602142
2. Jardine K, Zorzanelli R, Gimenez B, Robles E, Rosa L (2020): Raw leaf gas exchange data in the Amazon basin, 2014-2016. 1.0. NGEE Tropics Data Collection. (dataset). http://dx.doi.org/10.15486/ngt/1602143
3. Jardine K, Zorzanelli R, Gimenez B, Robles E, Rosa L (2020): Raw leaf isoprene and monoterpene emission GC-MS chromatograms/calibrations for MassHunter software, Brazil, 2014-2016. 1.0. NGEE Tropics Data Collection. (dataset). http://dx.doi.org/10.15486/ngt/1602144

FINE-ROOT DYNAMICS VARY WITH SOIL DEPTH AND PRECIPITATION IN A LOW-NUTRIENT TROPICAL FOREST IN THE CENTRAL AMAZONIA

The Science
A common assumption in tropical ecology is that root systems respond rapidly to climatic cues but that most of that response is limited to the uppermost layer of the soil, with relatively limited changes in deeper layers. However, this assumption has not been tested directly, preventing models from accurately predicting the response of tropical forests to environmental change.

The Impact
This study presents new direct estimates of fine‐root productivity and turnover in a Central Amazonian plateau tropical forest, as well as the factors controlling their dynamics, which are crucial to the understanding of above‐ versus below ground trade‐offs and linkages determining forest function. The findings demonstrate a relationship between fine‐root dynamics and precipitation regimes and emphasize the importance of deeper roots for accurate estimates of primary productivity and the interaction between roots and carbon, water, and nutrients.

Summary
Our objective was to quantify the patterns and controls of fine-root productivity, standing stock, and mortality and fine-root population turnover across the vertical soil profile in an Amazonian plateau tropical forest. We measured seasonal dynamics of fine roots with high spatial and temporal resolution using minirhizotrons to see below the surface in a mature forest in Central Amazonia. Minirhizotron measurements were calibrated with fine roots extracted from soil cores. Our direct observations of fine‐root dynamics to a depth of 90 cm enabled us to reach three important advances in our understanding of fine‐root dynamics in this site: (a) Although the largest fraction of fine‐root biomass and productivity is in the top 10 cm of the soil profile, a substantial fraction is deeper than 30 cm (46.1% and 40.6%, respectively); (b) As is often assumed but rarely observed, fine‐root turnover declined with depth; (c) Seasonal variation in precipitation drives root dynamics, but the direction and strength of the influence of precipitation varies with depth. Fine‐root productivity and mortality in surface layers were positively related to precipitation. Fine‐root stock was greater in dry periods in the deepest layer where water is likely more available at that time. Our data extend the quantification of root dynamics to deeper in the soil profile than previous studies in tropical forests, contributing to our understanding of ecosystem net primary production, carbon cycling, and environmental controls on fine‐root dynamics.

Figure. Fine roots at the soil surface are important for nutrient cycling in wet tropical forests, but a substantial fraction of fine-root productivity occurs deeper in the soil. 

 

 

 

 

 

Contacts (BER PM): Daniel Stover, SC-23.1, Daniel.Stover@science.doe.gov (301-903-0289) 

PI Contact: Richard J. Norby, Department of Ecology & Evolutionary Biology, University of Tennessee-Knoxville,  rnorby@utk.edu, 865-603-0752

Funding
This work was supported in part by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research Program, Climate and Environmental Sciences Division through the NGEE-Tropics program at Oak Ridge National Laboratory (ORNL). ORNL is managed by University of Tennessee (UT)-Battelle, LLC, for the U.S. Department of Energy under contract DE-AC05-00OR22725.

Publications
1. Cordeiro AL, Norby RJ, Andersen KM, Valverde-Barrantes O, Fuchslueger L, Oblitas E, Hartley IP, Iversen CM, Gonçalves NB, Takeshi B, Lapola DM, Quesada CA. 2020. Fine-root dynamics vary with soil depth and precipitation in a low nutrient tropical forest in the Central Amazonia. Plant-Environment Interactions, DOI:10.1002/pei3.10010.
2. Cordeiro AL, Valverde‐Barrantes O, Oblitas E, Gonçalves NB, Andersen KM, Quesada CA, Norby RJ. 2019. Fine‐root production, mortality, and standing stock from minirhizotron measurements, AmazonFACE site, Brazil. 1.0. NGEE Tropics Data Collection (dataset). http://dx.doi.org/10.15486/ngt/1523508.

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