J. Patrick Megonigal

The carbon balance of North American wetlands

We examine the carbon balance of North American wetlands by reviewing and synthesizing the published literature and soil databases. North American wetlands contain about 220 Pg C, most of which is in peat. They are a small to moderate carbon sink of about 49 Tg C yr−1, although the uncertainty around this estimate is greater than 100%, with the largest unknown being the role of carbon sequestration by sedimentation in freshwater mineral-soil wetlands. We estimate that North American wetlands emit 9 Tg methane (CH4) yr−1; however, the uncertainty of this estimate is also greater than 100%. With the exception of estuarine wetlands, CH4 emissions from wetlands may largely offset any positive benefits of carbon sequestration in soils and plants in terms of climate forcing. Historically, the destruction of wetlands through land-use changes has had the largest effects on the carbon fluxes and consequent radiative forcing of North American wetlands. The primary effects have been a reduction in their ability to sequester carbon (a small to moderate increase in radiative forcing), oxidation of their soil carbon reserves upon drainage (a small increase in radiative forcing), and reduction in CH4 emissions (a small to large decrease in radiative forcing). It is uncertain how global changes will affect the carbon pools and fluxes of North American wetlands. We will not be able to predict accurately the role of wetlands as potential positive or negative feedbacks to anthropogenic global change without knowing the integrative effects of changes in temperature, precipitation, atmospheric carbon dioxide concentrations, and atmospheric deposition of nitrogen and sulfur on the carbon balance of North American wetlands.

Tidal wetland stability in the face of human impacts and sea-level rise

Coastal populations and wetlands have been intertwined for centuries, whereby humans both influence and depend on the extensive ecosystem services that wetlands provide. Although coastal wetlands have long been considered vulnerable to sea-level rise, recent work has identified fascinating feedbacks between plant growth and geomorphology that allow wetlands to actively resist the deleterious effects of sea-level rise. Humans alter the strength of these feedbacks by changing the climate, nutrient inputs, sediment delivery and subsidence rates. Whether wetlands continue to survive sea-level rise depends largely on how human impacts interact with rapid sea-level rise, and socio-economic factors that influence transgression into adjacent uplands.

Estimating Global “Blue Carbon” Emissions from Conversion and Degradation of Vegetated Coastal Ecosystems

Recent attention has focused on the high rates of annual carbon sequestration in vegetated coastal ecosystems—marshes, mangroves, and seagrasses—that may be lost with habitat destruction (‘conversion’). Relatively unappreciated, however, is that conversion of these coastal ecosystems also impacts very large pools of previously-sequestered carbon. Residing mostly in sediments, this ‘blue carbon’ can be released to the atmosphere when these ecosystems are converted or degraded. Here we provide the first global estimates of this impact and evaluate its economic implications. Combining the best available data on global area, land-use conversion rates, and near-surface carbon stocks in each of the three ecosystems, using an uncertainty-propagation approach, we estimate that 0.15–1.02 Pg (billion tons) of carbon dioxide are being released annually, several times higher than previous estimates that account only for lost sequestration. These emissions are equivalent to 3–19% of those from deforestation globally, and result in economic damages of

Altered soil microbial community at elevated CO2 leads to loss of soil carbon

US 6–42 billion annually. The largest sources of uncertainty in these estimates stems from limited certitude in global area and rates of land-use conversion, but research is also needed on the fates of ecosystem carbon upon conversion. Currently, carbon emissions from the conversion of vegetated coastal ecosystems are not included in emissions accounting or carbon market protocols, but this analysis suggests they may be disproportionally important to both. Although the relevant science supporting these initial estimates will need to be refined in coming years, it is clear that policies encouraging the sustainable management of coastal ecosystems could significantly reduce carbon emissions from the land-use sector, in addition to sustaining the well-recognized ecosystem services of coastal habitats.

Elevated CO2 stimulates marsh elevation gain, counterbalancing sea-level rise

Increased carbon storage in ecosystems due to elevated CO2 may help stabilize atmospheric CO2 concentrations and slow global warming. Many field studies have found that elevated CO2 leads to higher carbon assimilation by plants, and others suggest that this can lead to higher carbon storage in soils, the largest and most stable terrestrial carbon pool. Here we show that 6 years of experimental CO2 doubling reduced soil carbon in a scrub-oak ecosystem despite higher plant growth, offsetting ≈52% of the additional carbon that had accumulated at elevated CO2 in aboveground and coarse root biomass. The decline in soil carbon was driven by changes in soil microbial composition and activity. Soils exposed to elevated CO2 had higher relative abundances of fungi and higher activities of a soil carbon-degrading enzyme, which led to more rapid rates of soil organic matter degradation than soils exposed to ambient CO2. The isotopic composition of microbial fatty acids confirmed that elevated CO2 increased microbial utilization of soil organic matter. These results show how elevated CO2, by altering soil microbial communities, can cause a potential carbon sink to become a carbon source.

Ecosystem response to elevated CO2 levels limited by nitrogen-induced plant species shift.

Tidal wetlands experiencing increased rates of sea-level rise (SLR) must increase rates of soil elevation gain to avoid permanent conversion to open water. The maximal rate of SLR that these ecosystems can tolerate depends partly on mineral sediment deposition, but the accumulation of organic matter is equally important for many wetlands. Plant productivity drives organic matter dynamics and is sensitive to global change factors, such as rising atmospheric CO2 concentration. It remains unknown how global change will influence organic mechanisms that determine future tidal wetland viability. Here, we present experimental evidence that plant response to elevated atmospheric [CO2] stimulates biogenic mechanisms of elevation gain in a brackish marsh. Elevated CO2 (ambient + 340 ppm) accelerated soil elevation gain by 3.9 mm yr−1 in this 2-year field study, an effect mediated by stimulation of below-ground plant productivity. Further, a companion greenhouse experiment revealed that the CO2 effect was enhanced under salinity and flooding conditions likely to accompany future SLR. Our results indicate that by stimulating biogenic contributions to marsh elevation, increases in the greenhouse gas, CO2, may paradoxically aid some coastal wetlands in counterbalancing rising seas.

Life at the Energetic Edge: Kinetics of Circumneutral Iron Oxidation by Lithotrophic Iron-Oxidizing Bacteria Isolated from the Wetland-Plant Rhizosphere

Terrestrial ecosystems gain carbon through photosynthesis and lose it mostly in the form of carbon dioxide (CO2). The extent to which the biosphere can act as a buffer against rising atmospheric CO2 concentration in global climate change projections remains uncertain at the present stage. Biogeochemical theory predicts that soil nitrogen (N) scarcity may limit natural ecosystem response to elevated CO2 concentration, diminishing the CO2-fertilization effect on terrestrial plant productivity in unmanaged ecosystems. Recent models have incorporated such carbon–nitrogen interactions and suggest that anthropogenic N sources could help sustain the future CO2-fertilization effect. However, conclusive demonstration that added N enhances plant productivity in response to CO2-fertilization in natural ecosystems remains elusive. Here we manipulated atmospheric CO2 concentration and soil N availability in a herbaceous brackish wetland where plant community composition is dominated by a C3 sedge and C4 grasses, and is capable of responding rapidly to environmental change. We found that N addition enhanced the CO2-stimulation of plant productivity in the first year of a multi-year experiment, indicating N-limitation of the CO2 response. But we also found that N addition strongly promotes the encroachment of C4 plant species that respond less strongly to elevated CO2 concentrations. Overall, we found that the observed shift in the plant community composition ultimately suppresses the CO2-stimulation of plant productivity by the third and fourth years. Although extensive research has shown that global change factors such as elevated CO2 concentrations and N pollution affect plant species differently and that they may drive plant community changes, we demonstrate that plant community shifts can act as a feedback effect that alters the whole ecosystem response to elevated CO2 concentrations. Moreover, we suggest that trade-offs between the abilities of plant taxa to respond positively to different perturbations may constrain natural ecosystem response to global change.

SEASONAL PATTERNS AND PLANT-MEDIATED CONTROLS OF SUBSURFACE WETLAND BIOGEOCHEMISTRY

ABSTRACT Batch cultures of a lithotrophic Fe(II)-oxidizing bacterium, strain BrT, isolated from the rhizosphere of a wetland plant, were grown in bioreactors and used to determine the significance of microbial Fe(II) oxidation at circumneutral pH and to identify abiotic variables that affect the partitioning between microbial oxidation and chemical oxidation. Strain BrT grew only in the presence of an Fe(II) source, with an average doubling time of 25 h. In one set of experiments, Fe(II) oxidation rates were measured before and after the cells were poisoned with sodium azide. These experiments indicated that strain BrT accounted for 18 to 53% of the total iron oxidation, and the average cellular growth yield was 0.70 g of CH2O per mol of Fe(II) oxidized. In a second set of experiments, Fe(II) was constantly added to bioreactors inoculated with live cells, killed cells, or no cells. A statistical model fitted to the experimental data demonstrated that metabolic Fe(II) oxidation accounted for up to 62% of the total oxidation. The total Fe(II) oxidation rates in these experiments were strongly limited by the rate of Fe(II) delivery to the system and were also influenced by O2 and total iron concentrations. Additionally, the model suggested that the microbes inhibited rates of abiotic Fe(II) oxidation, perhaps by binding Fe(II) to bacterial exopolymers. The net effect of strain BrT was to accelerate total oxidation rates by up to 18% compared to rates obtained with cell-free treatments. The results suggest that neutrophilic Fe(II)-oxidizing bacteria may compete for limited O2 in the rhizosphere and therefore influence other wetland biogeochemical cycles.

Geochemical control of microbial Fe(III) reduction potential in wetlands: Comparison of the rhizosphere to non-rhizosphere soil

In tidal marshes, spatial and temporal variability in the importance of mi- crobial metabolic pathways influences ecosystem-level processes such as soil carbon stor- age, the regeneration of inorganic nutrients, and the production of atmospherically important trace gases. We measured seasonal changes in rates of microbial Fe(III) reduction, sulfate reduction, and methanogenesis in tidal freshwater and brackish marshes on the Patuxent River, Maryland, USA, and assessed the ability of plant roots to influence these processes by regenerating electron acceptors and supplying electron donors. In both marshes, the importance of microbial Fe(III) reduction was greatest early in the summer and decreased through the study period. Coincident with the seasonal decline in Fe(III) reduction, me- thanogenesis (freshwater marsh) or sulfate reduction (brackish site) increased in importance. At the brackish marsh, the partitioning of anaerobic carbon metabolism between Fe(III) reduction and sulfate reduction was similar within and below the root zone, suggesting that rhizosphere processes did not control anaerobic metabolism at this site. Instead, seasonal biogeochemical patterns at the brackish marsh were affected by factors such as water table depth and iron-sulfur interactions. At the tidal freshwater site, our results suggest that changes in rates of Fe(III) reduction and methanogenesis were directly affected by plant- mediated processes. In midsummer, Fe(III) reduction accounted for a greater fraction of total anaerobic metabolism in rhizosphere-influenced surface soils than in soils below the root zone. High rates of Fe(III) reduction occurred at the expense of methanogenesis. This study documented strong temporal variations in the outcome of microbial competition for electron donors that ultimately affected the balance between Fe(III) reduction and me- thanogenesis within tidal freshwater marsh soils. Our data suggested that variations in microbial metabolic pathways were regulated by physiochemical factors at the brackish site and plant activity at the freshwater site. Plant regulation of Fe(III) reduction is a largely unstudied mechanism by which plants influence wetland carbon cycling and greenhouse gas production.

Effects of flooding on root and shoot production of bald cypress in large experimental enclosures

We compared the reactivity and microbial reduction potential of Fe(III) minerals in the rhizosphere and non-rhizosphere soil to test the hypothesis that rapid Fe(III) reduction rates in wetland soils are explained by rhizosphere processes. The rhizosphere was defined as the area immediately adjacent to a root encrusted with Fe(III)-oxides or Fe plaque, and non-rhizosphere soil was >0.5 cm from the root surface. The rhizosphere had a significantly higher percentage of poorly crystalline Fe (66+/-7%) than non-rhizosphere soil (23+/-7%); conversely, non-rhizosphere soil had a significantly higher proportion of crystalline Fe (50+/-7%) than the rhizosphere (18+/-7%, P<0.05 in all cases). The percentage of poorly crystalline Fe(III) was significantly correlated with the percentage of FeRB (r=0.76), reflecting the fact that poorly crystalline Fe(III) minerals are labile with respect to microbial reduction. Abiotic reductive dissolution consumed about 75% of the rhizosphere Fe(III)-oxide pool in 4 h compared to 23% of the soil Fe(III)-oxide pool. Similarly, microbial reduction consumed 75-80% of the rhizosphere pool in 10 days compared to 30-40% of the non-rhizosphere soil pool. Differences between the two pools persisted when samples were amended with an electron-shuttling compound (AQDS), an Fe(III)-reducing bacterium (Geobacter metallireducens), and organic carbon. Thus, Fe(III)-oxide mineralogy contributed strongly to differences in the Fe(III) reduction potential of the two pools. Higher amounts of poorly crystalline Fe(III) and possibly humic substances, and a higher Fe(III) reduction potential in the rhizosphere compared to the non-rhizosphere soil, suggested the rhizosphere is a site of unusually active microbial Fe cycling. The results were consistent with previous speculation that rapid Fe cycling in wetlands is due to the activity of wetland plant roots.