While traditionally considered important mainly in hypoxic roots during flooding, upregulation of fermentation pathways in plants is highlighted to be an evolutionarily conserved strategy under aerobic conditions.

The Science
Upregulation of fermentation in plants has mainly been considered important in hypoxic roots during flooding. However, plant fermentation rates remain poorly characterized across diverse plant functional types in managed and natural ecosystems globally. Here, new studies are summarized that demonstrate the upregulation of fermentation pathways in plants during 1) Growth and development, 2) Root hypoxia associated with flooding, and 3) Defense processes during abiotic stress. While maintenance and growth respiration are often modeled separately in terrestrial models, here we propose the concept of “Defense Respiration” fueled by acetate fermentation where upregulation of acetate fermentation contributes acetate substrate for alternative energy production via aerobic respiration, biosynthesis of primary and secondary metabolites, and the acetylation of proteins involved in defense gene regulation.

The Impact
Fermentation processes, are now recognized to be tightly integrated into plant growth and development as well as responses to abiotic stress. While traditionally considered important mainly in roots during flooding, fermentation in roots, stems, and leaves is now recognized as a critical drought survival strategy. Acetate produced by fermentation may be used as an energy source through “Defense Respiration” and as a stress signaling molecule critical to drought survival. We highlight new frontiers in leaf-atmosphere emission measurements as a potential way to study plant fermentation responses of individual leaves, branches, ecosystems and regions. We conclude that new field studies are urgently needed to resolve the physiological and ecological roles of plant fermentation metabolism under a changing climate.

Summary
Plant fermentation is an ancient metabolic pathway that may be critical in surviving hypoxic conditions experienced by roots during flooding. However, emerging evidence suggests that rather than a strict dependence on oxygen availability in tissues, fermentation can also be active under aerobic conditions linked to a drop in cellular energy status. Key adaptations to root hypoxia in flood tolerant species, including enhanced uptake of atmospheric oxygen in aerial tissues and delivery to roots, is lacking in flood intolerant species. This likely explains why much higher foliar emissions of ethanol and acetaldehyde have been observed from some flood intolerant species during flooding compared with flood tolerant species, in contrast to early predictions. Moreover, high tissue concentrations and atmospheric emissions of fermentation volatiles have been observed under aerobic conditions in well drained soils associated with temperature-linked growth processes as well as drought stress. Further, genomic and transcriptomic studies have revealed that a metabolic shift towards acetate fermentation occurs in roots and leaves which coordinates drought tolerance in plants via protein acetylation and the activation of the jasmonate signaling pathway. Additional studies revealed that acetate fermentation under aerobic conditions improves plant growth and that co-occurrence of acetate fermentation, aerobic respiration, and the utilization of acetate in biosynthetic pathways helps plants meet the high energetic and carbon demands of fast growth rates. This recent research appears to resolve the paradox from earlier work of why fermentation enzymes are so abundant in leaves when they are the least likely tissue to experience hypoxia. While destructive methods are mainly used to study fermentation patterns in plants, the emerging frontier of quantifying biosphere-atmosphere fluxes of fermentation volatiles and atmospheric vertical concentration gradients may provide a means to study dynamic fermentation responses in plants during growth and environmental stress from leaves, branches, ecosystems, landscapes and whole regions. This may enable studies aimed at improving the quantitative understanding of the plant physiological and ecological roles of fermentation under hypoxic and aerobic conditions. This includes potential critical roles in supporting productivity during favorable conditions for net carbon assimilation and growth, as well as defense processes linked to survival during abiotic stress in a changing climate.

Although field observations to quantify plant fermentative metabolism patterns across diverse plant functional types are in general lacking, ecosystems regularly exposed to root flooding like mangroves and low-lying tropical forests may be considered to have high rates of fermentative metabolism. For example, in Amazonian floodplain forests, more than 1000 tree species are exposed to extended annual submergence lasting up to 9 months each year, with full submergence of young trees. Despite hypoxia, restricted photosynthesis rates, and extremely low light levels during the submergence, leafed seedlings survival rates are high. Aerobic fermentation metabolism coupled to respiration in fast growing tropical pioneer tree species like Vismia guianensis, may also be important in the re-growth of tropical forests following a disturbance. In addition, high temperature and drought stress characteristic of desert ecosystems may also stimulate high rates of fermentative metabolism as a key survival trait. For example, creosotebush (Larrea tridentata), which grows in well drained sandy soils, is vastly distributed in North American deserts, and was reported to have large temperature-stimulated leaf emissions of the fermentation volatiles acetaldehyde, acetic acid, acetone, ethanol, and methyl acetate during the summer monsoon in the Sonoran desert. Thus, plant fermentation studies across diverse plant functional traits like photosynthetic types (C3, C4, and crassulacean acid metabolism), growth rates, wood density, specific leaf area, etc. may lead to improvements in our predictive understanding of the roles of plant fermentative metabolism in the establishment and resilience of ecosystem structure and function.

Figure. Graphical representation of acetate fermentation metabolism in plant cells and whole trees during root flooding and drought. Also shown are emerging methods of biosphere-atmosphere studies of fermentation volatile emissions from leaf to global scales, and an ecosystem pizza showing globally important ecosystems and the main processes anticipated to dominate fermentation processes in plants. Image credit: Kolby Jardine.

Contact: Kolby Jardine, Research Scientist (LBNL: Earth and Environmental Sciences Area, Ecology Department), kjjardine@lbl.gov

Funding
This material is based upon work supported by the US Department of Energy (DOE), Office of Science, Office of Biological and Environmental Research (BER), Biological System Science Division (BSSD), Early Career Research Program under Award no. FP00007421 to KJJ and at the Lawrence Berkeley National Laboratory (LBNL). Additional DOE support was provided by the Coastal Observations, Mechanisms, and Predictions Across Scales (COMPASS) project and the Next Generation Ecosystem Experiments-Tropics (NGEE-Tropics) through contract no. DE-AC02-05CH11231 as part of DOE’s Terrestrial Ecosystem Science Program.

Publications
Jardine K and McDowell N. (2023) Fermentation-mediated Growth, Signaling, and Defense in Plants. New Phytologist, Tansley Review. https://nph.onlinelibrary.wiley.com/doi/full/10.1111/nph.19015.

Changing wetland soils in the Peruvian Amazon threaten global climate with more greenhouse gas emissions

The Science
Amazonian wetlands, including wet peatlands, are a major carbon and nitrogen sink but also sources of methane (CH₄). Additionally, Peruvian rainforests are home to an impressive diversity of species, including 5% of globally known amphibians and 16% of butterflies. However, these ecological capacities are increasingly vulnerable to the impacts of global warming, droughts, and land use changes. The changes are turning the Amazonian peatlands to sources of dangerous greenhouse gases – carbon dioxide (CO₂) and nitrous oxide (laughing gas; N₂O). To better understand the environmental drivers of CO₂, methane (CH₄) and N₂O fluxes in Peruvian peatlands across a wide range of land uses, an international team lead by Dr. Jaan Pärn and Prof. Ülo Mander from the University of Tartu, in collaboration wihh Dr. Robinson I. Negron-Juarez of Lawrence Berkeley lab, conducted a measurement campaign in Iquitos, the Peruvian Amazon. The campaign took place from the end of dry season in September 2019 to late rainy season in March 2020. The team investigated three sites:

1. A pristine swamp forest in the Quistococha lake floodplain.
2. A young secondary swamp forest grown on fallow pasture and banana plantation on an alluvial toe slope.
3. A slash-and-burn manioc (Manihot esculenta) field.

The team measured CO₂, CH₄, N₂O fluxes, denitrification (N₂O and N₂) potential from intact peat cores, and auxiliary environmental characteristics (soil temperature, water table, O₂ and other chemistry) from the soil. In the pristine swamp forest, CO₂, CH₄, N₂O fluxes were also measured from palm and Symphonia hardwood trunks.

The Impact
The peat swamp forests under slight water table drawdown emitted large amounts of both CO₂ and CH₄. Much of the CH₄ was released through palm trunks, which is a novel addition to current knowledge. A heavy post-drought shower created a hot moment of N₂O in the pristine swamp forest. The analysis revealed nitrifiers – a group of soil microbes – as responsible for the N₂O production. Several indirect signs of temporary oxygen intrusion in the swamp forest soil were noticed, facilitating the aerobic microbes. The manioc field, in no surprise, emitted relatively high amounts of CO₂ and N₂O.

Summary
Peruvian Amazonia is a global sink of carbon but a hotspot of CH₄ and N₂O emissions. With an objective to identify environmental drivers of CO₂, CH₄ and N₂O fluxes of Peruvian wetland soils under a broad range of land use, an international team lead by Dr. Jaan Pärn and Prof. Ülo Mander from the University of Tartu and involving Dr. Robinson I. Negron-Juarez of Lawrence Berkeley lab held a measurement campaign in Iquitos, the Peruvian Amazon. The investigation showed that even small changes in soil moisture can create ‘hot moments’ of GHG emissions from microbes in Amazonian wetland soils, and should therefore be carefully monitored.

Figure. The left figure shows the site location and experimental design. The right figure shows carbon dioxide (CO₂), methane (CH₄) and nitrous oxide (N₂O) fluxes in from the Peruvian wetland soils, and their box plots. Significant differences according to Wilcoxon test are shown with asterisks as follows: * – p<0.05; ** – p<0.01; *** –p<0.001. Asterisks directly above box without brackets denote significant difference from all other sites in the plot. Images: courtesy of Jaan Pärn. Peat core image: Anna Macphie, Uni. St. Andrews

 Contact: Jaan Pärn (University of Tartu), jaan.parn@ut.ee 

Funding
The study was supported by the Estonian Research Council (PRG352 and MOBERC-20 grants) and the EU through the European Research Executive Agency (HORIZON-WIDERA Living Labs for Wetland Forest Research Twinning project No 101079192), European Regional Development Fund (ENVIRON and EcolChange Centres of Excellence, Estonia and the MOBTP101 returning researcher grant by the Mobilitas Pluss programme), the European Social Fund (Doctoral School of Earth Sciences and Ecology), LIFE programme project “Demonstration of climate change mitigation potential of nutrients rich organic soils in Baltic States and Finland” (LIFE OrgBalt, LIFE18 CCM/LV/001158), Czech Science Foundation (17-18112Y), and project SustES – Adaptation strategies for sustainable ecosystem services and food security under adverse environmental conditions (CZ.02.1.01/0.0/0 .0/16_019/0000797).

Dr. Negron-Juarez was supported by the Next Generation Ecosystem Experiments – Tropics funded by the U.S Department of Energy, Office of Biological and Environmental Research

 Publication: Parn et al. “Effects of Water Table Fluctuation on Greenhouse Gas Emissions from Wetland Soils in the Peruvian Amazon”, Wetlands, 43:62 (2023). https://doi.org/10.1007/s13157-023-01709-z.

Interplay of Turbulence Regimes, Deep Convection, and Tree Mortality in the Amazon Rainforest

The Science
With focus in the Central Amazon (Fig A), at the Tropical Silviculture Experimental Station -EEST (located about 60 km northwest of Manaus, 2°36′S, 60°12′W, 130 m ...) also known as ZF2, we investigated the influence of seasonality and proximity to the forest canopy on nocturnal turbulence regimes in the roughness sublayer (Fig B). Since convective systems of different scales are common in this region (Fig C), we also analyzed the effect of extreme wind gusts (propagated from convective downdrafts) (Fig D) on the organization of the turbulence regimes, and their potential to cause the mortality of canopy trees.

The Impact
Two different turbulence regimes were identified at three heights above the canopy: a weakly stable (WS) and a very stable regime (VS). The threshold wind speeds that mark the transition between turbulence regimes were larger during the dry season and increased as a function of the height above the canopy. Downdrafts occurred only in the WS and favored a fully coupled state of wind flow along the canopy profile.

Summary
Our study data include high-frequency winds, temperature and ozone concentration at different heights during the dry and wet seasons of 2014. In addition, we used critical wind-speed data derived from a tree-winching experiment and a modeling study conducted in the same study site. This study provides three novel contributions. The first was the identification of different turbulence regimes and their patterns in terms of seasonality and proximity to the forest canopy in the nocturnal roughness sublayer. The second was the assessment of the effects of near surface wind gusts (propagated from downdrafts) on the organization of turbulence regimes. Finally, it provides evidence on the occurrence of extreme wind gusts associated with convective downdrafts, with potential to promote damage and mortality of canopy trees. These aspects highlight the strong interactions between atmospheric and biospheric processes and mechanisms regulating forest structure and dynamics.

Figure. (A) Study area – Central Amazon, and high frequency sensor. (B) Relationship between turbulence velocity scale () and mean wind speed ( ) at different heights in the dry and wet season during the nighttime. Triangles indicate the threshold wind speed () at which the very stable changed to weakly stable regime. (C) GOES 13 image during 13 April 2014 at 0300 UTC when downdrafts reached the micrometeorology tower at the study area (red dot). (D) horizontal wind speed () over the sensor during 13 April.

Contact: Daniel Magnabosco Marra (Max Planck, Biogeochemistry), dmarra@bgc-jena.mpg.de

Funding
R Negron-Juarez was supported by the Next Generation Ecosystem Experiments-Tropics (NGEE-Tropics), funded by the U.S. Department of Energy, Office of Science. This study is part of the Wind–Tree Interaction Project (INVENTA) and the Amazon Tall Tower Observatory (ATTO), funded by the German Federal Ministry of Education and Research (BMBF, contracts 01LB1001A and 01LK1602A), the Brazilian Ministry of Science, Technology and Innovation (MCTI/FINEP, contract 01.11.01248.00) and the Max Planck Society (MPG), Germany.

Publication: Mendoca A, Dias-Junior C, Acevedo O, Santana R, Costa F, Negron-Juarez R, Manzi A, Trumbore S, Magnabosco Marra D. Agricultural and Forest Meteorology, 339, 109526 (2023), DOI: https://doi.org/10.1016/j.agrformet.2023.109526

This study identifies 38 cases of windthrows in the Amazonia to explore the relationship between windthrows and the characteristics (storm passing time, cloud top temperature, and maximum precipitation) of mesoscale convective systems (MCSs) that produced them.

The Science
Fan-shaped dead forest patches were found over the entire Amazonia. These patches, over 37 hectares, affect the role the Amazon forests played in the world’s carbon cycle. Scientists found that frequent storms result in these dead forest patches, but how does the process happen? In this study, we explored the three characteristics of storms, including their passing over time, cloud top temperature, and associated precipitation, to identify their relationship with the size of the dead forests. We found that long-lived storms with thicker and tall clouds, result in bigger sizes of dead forest patches. Moreover, forests in the western Amazonia are more vulnerable to storms than forests on the other parts of the Amazonia.

The Impact
My research explores how extreme storms impact tree loss in tropical forests, especially in the Amazon. These storms, responsible for 50-90% of annual rainfall in the tropics, often result in toppling trees, which disrupts the forest’s ability to store carbon, a crucial ability to fight climate change. Previously, these phenomena were studied separately, but my work connects them. By analyzing satellite data, I’ve started uncovering relationships between the characteristics of extreme storms and tree loss sizes. This understanding can improve climate models, providing more accurate predictions about our changing environment.

Summary
Our research delved into the relationship between large-scale storm systems known as mesoscale convective systems (MCSs) and the phenomenon of ‘windthrow’ – when storms uproot trees – in the Amazon rainforest. We examined 38 pairs of windthrow and their associated MCS events to identify the specific storm characteristics influencing the extent of windthrow. We found that MCSs with a longer storm duration tended to result in more extensive windthrow. We found a positive correlation between the storm’s duration and the area of forest affected. The depth of convection clouds within the storm also played a role. Deep convection caused larger windthrow across the entire Amazon. In contrast, shallow convection led to medium-sized windthrows in western Amazonia and smaller ones in central Amazonia. Interestingly, we observed that rainfall wasn’t uniformly distributed among forest disturbances of the same size, suggesting the need for more precise precipitation data to establish a clearer relationship with windthrow sizes. This study offers detailed case studies on windthrows and corresponding MCS features. It helps reduce the uncertainty of previous research due to data mismatches between MCSs and windthrows, offering fresh insights into how land and atmosphere interact. These findings are important for refining our climate models and, ultimately, our understanding of climate change impacts on the ecosystem.

Figure. The workflow of correlating a windthrow event on the land surface to its associated convective storm in the atmosphere using remote sensing images from both land and meteorological satellites. Image courtesy of Yanlei Feng.

Contact: Yanlei Feng (UC Berkeley PhD graduates, currently at Carnegie Institute for Science), ylfeng@berkeley.edu

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 under contract number DE-AC02-05CH11231. We acknowledge the World Climate Research Programme, which, through its Working Group on Coupled Modelling, coordinated and promoted CMIP6. We thank the climate modeling groups for producing and making available their model output, the Earth System Grid Federation (ESGF) for archiving the data and providing access, and the multiple funding agencies who support CMIP6 and ESGF.

Publication: Feng, Y., Negrón‐Juárez, R.I., Chiang, J.C. and Chambers, J.Q., 2023. Case studies of forest windthrows and mesoscale convective systems in Amazonia. Geophysical Research Letters, 50(12), p.e2023GL104395. https://doi.org/10.1029/2023GL104395

ForestGEO scientists quantified the proportion of total biomass losses from damaged but surviving trees across seven tropical forests.

The Science
Damage (i.e., branchfall, trunk breakage, wood decay) is a ubiquitous feature in forest ecosystems. Yet, traditional forest inventories assume tree mortality as the only source of biomass losses. While previous studies have shown that damage is an important condition preceding tree death, the contribution of non-lethal damage (i.e., from surviving trees) to total forest biomass (and therefore carbon) losses remained unclear. ForestGEO scientists combined field-based measurements of tree completeness with vertical volume profile models obtained from terrestrial laser scanning to show that 42% (range 12%–76% across forests) of total aboveground biomass loss is due to damage to living trees across seven tropical forests.

The Impact
Ground-based biomass stocks and fluxes are widely used to estimate carbon budgets, to quantify forest carbon offsets, and to calibrate and validate remote sensing products employed to obtain biomass estimates at regional and global scales. This study shows that biomass loss from damage to living trees constitutes an important and overlooked component of biomass loss. These results contrast with the typically low forest biomass losses estimated only from tree mortality and suggest that forest carbon turnover may be higher than previously thought. Since forest disturbance rates are expected to increase under climate change the biomass loss to damage is likely to become more important.

Summary
Forest carbon losses constitute a significant source of uncertainty in vegetation models. These estimates are typically calculated based on the biomass of dead trees, without accounting for losses via damage to living trees: branchfall, trunk breakage, wood decay. In this study, forest ecologists employ multiple annual records of tree survival and structural completeness to compare aboveground biomass (AGB) loss via damage to living trees to total AGB loss (mortality + damage) in seven tropical forests widely distributed across environmental conditions. Researchers find that 42% (3.62 Mg ha-1 yr-1; 95% CI 2.36–5.25) of total AGB loss (8.72 Mg ha-1 yr-1; CI 5.57–12.86) is due to damage to living trees. They also find that conventional forest inventories overestimate stand-level AGB stocks by 4% (1-17% range across forests) because assume structurally complete trees, underestimate total AGB loss by 29% (6-57%) due to overlooked damage-related AGB losses, and overestimate AGB loss via mortality by 22% (7-80%) because of the assumption that trees are undamaged before dying. These results indicate that forest carbon fluxes are higher than previously thought. Damage on living trees is an underappreciated component of the forest carbon cycle that is likely to become even more important as the frequency of forest disturbances increases.

Figure. Damaged but surviving trees are highly frequent across forest ecosystems. Photo credits: C.Y. Chia-Hao (left), D. Zuleta (center, right).

Contact: Daniel Zuleta, Ph.D., Ecologist (Postdoctoral fellow) at Forest Global Earth Observatory, Smithsonian Tropical Research Institute in Washington, DC (dfzuleta@gmail.com)

Funding
This project was supported as part of the Next Generation Ecosystem Experiments–Tropics and was funded by the Office of Biological and Environmental Research (BER) within the U.S. Department of Energy’s (DOE) Office of Science. Data collection was supported by the Forest Global Earth Observatory (ForestGEO) of the Smithsonian Institution.

Publication: Zuleta, D., et al. “Damage to living trees contributes to almost half of the biomass losses in tropical forests” Global Change Biology in press (2023). https://doi.org/10.1111/gcb.16687.