Robinson W. Fulweiler

Reversal of the net dinitrogen gas flux in coastal marine sediments

The flux of nitrogen from land and atmosphere to estuaries and the coastal ocean has increased substantially in recent decades. The observed increase in nitrogen loading is caused by population growth, urbanization, expanding water and sewer infrastructure, fossil fuel combustion and synthetic fertilizer consumption. Most of the nitrogen is removed by denitrification in the sediments of estuaries and the continental shelf, leading to a reduction in both cultural eutrophication and nitrogen pollution of the open ocean. Nitrogen fixation, however, is thought to be a negligible process in sub-tidal heterotrophic marine systems. Here we report sediment core data from Narragansett Bay, USA, which demonstrate that heterotrophic marine sediments can switch from being a net sink to being a net source of nitrogen. Mesocosm and core incubation experiments, together with a historic data set of mean annual chlorophyll production, support the idea that a climate-induced decrease in primary production has led to a decrease in organic matter deposition to the benthos and the observed reversal of the net sediment nitrogen flux. Our results suggest that some estuaries may no longer remove nitrogen from the water column. Instead, nitrogen could be exported to the continental shelf and the open ocean and could shift the effect of anthropogenic nitrogen loading beyond the immediate coastal zone.

The Terrestrial Silica Pump

Silicon (Si) cycling controls atmospheric CO2 concentrations and thus, the global climate, through three well-recognized means: chemical weathering of mineral silicates, occlusion of carbon (C) to soil phytoliths, and the oceanic biological Si pump. In the latter, oceanic diatoms directly sequester 25.8 Gton C yr−1, accounting for 43% of the total oceanic net primary production (NPP). However, another important link between C and Si cycling remains largely ignored, specifically the role of Si in terrestrial NPP. Here we show that 55% of terrestrial NPP (33 Gton C yr−1) is due to active Si-accumulating vegetation, on par with the amount of C sequestered annually via marine diatoms. Our results suggest that similar to oceanic diatoms, the biological Si cycle of land plants also controls atmospheric CO2 levels. In addition, we provide the first estimates of Si fixed in terrestrial vegetation by major global biome type, highlighting the ecosystems of most dynamic Si fixation. Projected global land use change will convert forests to agricultural lands, increasing the fixation of Si by land plants, and the magnitude of the terrestrial Si pump.

Ecological footprints and shadows in an urban estuary, Narragansett Bay, RI (USA)

Because the rise of cities in North America was much later than in many other parts of the world, their connections to the hinterland were influenced early in their development by railroads and steam-powered water transport. These fossil fuel-based links made it possible to widely separate the “upstream” autotrophic supporting systems from the heterotrophic cities. Here, we take a different look at the connection between a city (Providence, RI, USA) and its supporting natural systems by focusing on the export of industrial and metabolic wastes from the city to the “downstream” coastal ecosystem in Narragansett Bay. In this way, we can track the history of a city by examining the concentrations of nutrients, metals, and hydrocarbons in the water and sediments of the estuary. In the greater Providence metropolitan area at the head of Narragansett Bay, there was rapid population and industrial expansion during the 1800s without the proper infrastructure to deal with water supply for public safety and health. On the other hand, the absence of a public water supply kept industrial and metabolic wastes largely on land. However, from the fall of 1871, on with the construction of a public water supply and sewer system, human wastes began flowing into the estuary. By reconstructing the historical record of metals and other pollutants, we illustrate clear temporal and spatial gradients of urban impact on the bay. Unfortunately, while numerous studies during the 1970s and 1980s focused on documenting metal and hydrocarbon pollution in the bay, there has been little effort to quantify the impact of mitigation efforts that have greatly reduced the input of metals and hydrocarbons to the system. Nutrient reductions are more recent and ongoing.

Examining the impact of acetylene on N-fixation and the active sediment microbial community

Here we examined the impact of a commonly employed method used to measure nitrogen fixation, the acetylene reduction assay (ARA), on a marine sediment community. Historically, the ARA technique has been broadly employed for its ease of use, in spite of numerous known artifacts. To gauge the severity of these effects in a natural environment, we employed high-throughput 16S rRNA gene sequencing to detect differences in acetylene-treated sediments vs. non-treated control sediments after a 7 h incubation. Within this short time period, significant differences were seen across all activity of microbes identified in the sediment, implying that the changes induced by acetylene occur quickly. The results have important implications for our understanding of marine nitrogen budgets. Moreover, because the ARA technique has been widely used in terrestrial and freshwater habitats, these results may be applicable to other ecosystems.

Sediment Nitrogen Fixation: a Call for Re-evaluating Coastal N Budgets

Coastal ocean primary productivity is often limited by nitrogen (N) availability, which is determined by the balance between N sources (e.g., N-fixation, groundwater, river inputs, etc.) and sinks (e.g., denitrification, sediment burial, etc.). Historically, heterotrophic N-fixation in sediments was excluded as a significant source of N in estuarine budgets, based on low, indirectly measured rates (e.g., acetylene reduction assay) and because it was unnecessary to achieve mass balance. Many recent studies using net N2 flux measurements have shown that sediment N-fixation can equal or exceed N2 loss. In an effort to quantify N2 production and consumption simultaneously, we measured N-fixation and denitrification directly in sediment cores from a temperate estuary (Waquoit Bay, MA). N-fixation, dissimilatory nitrate reduction to ammonium, and denitrification occurred simultaneously, and the net N2 flux shifted from uptake (N-fixation) to efflux (denitrification) over the 120-h incubation. Evidence for N-fixation included net 28N2 and 30N2 uptake, 15NH4+ production from 30N2 additions, 15Norganic matter production, and nifH expression. N-fixation from 30N2 was up to eight times higher than potential denitrification. However, N-fixation calculated from 15NO3− was one half of the measured fixation from 30N2, indicating that 15NO3-isotope labeling calculations may underestimate N-fixation. These results highlight the dynamic nature of sediment N cycling and suggest that quantifying individual processes allows a greater understanding of what net N2 fluxes signify and how that balance varies over time.

Silica uptake by Spartina—evidence of multiple modes of accumulation from salt marshes around the world

Silicon (Si) plays a critical role in plant functional ecology, protecting plants from multiple environmental stressors. While all terrestrial plants contain some Si, wetland grasses are frequently found to have the highest concentrations, although the mechanisms driving Si accumulation in wetland grasses remain in large part uncertain. For example, active Si accumulation is often assumed to be responsible for elevated Si concentrations found in wetland grasses. However, life stage and differences in Si availability in the surrounding environment also appear to be important variables controlling the Si concentrations of wetland grasses. Here we used original data from five North American salt marshes, as well as all known published literature values, to examine the primary drivers of Si accumulation in Spartina, a genus of prolific salt marsh grasses found worldwide. We found evidence of multiple modes of Si accumulation in Spartina, with passive accumulation observed in non-degraded marshes where Spartina was native, while rejective accumulation was found in regions where Spartina was invasive. Evidence of active accumulation was found in only one marsh where Spartina was native, but was also subjected to nutrient over-enrichment. We developed a conceptual model which hypothesizes that the mode of Si uptake by Spartina is dependent on local environmental factors and genetic origin, supporting the idea that plant species should be placed along a spectrum of Si accumulation. We hypothesize that Spartina exhibits previously unrecognized phenotypic plasticity with regard to Si accumulation, allowing these plants to respond to changes in marsh condition. These results provide new insight regarding how salt marsh ecosystems regulate Si exchange at the land-sea interface.

The eutrophication commandments

Typically, rising atmospheric carbon dioxide concentrations are used to illustrate how humans have impacted the earth. However, we have also dramatically altered the amount of nitrogen (N) and phosphorus (P) cycling through the biosphere. Eventually these nutrients are carried to coastal receiving waters where they cause severe, often negative consequences including increased phytoplankton and macroalgae blooms, loss of submerged aquatic vegetation, low oxygen events, and decreased biodiversity. In many systems mitigation efforts are now underway to return these ecosystems to a less impacted state. While many uncertainties about the best way to manage eutrophic systems remain it is clear that we must take action to lessen our human nutrient footprint. Based on our current understanding of eutrophic systems we present ten eutrophication commandments or guidelines as a tool for scientists, policy makers, managers, and the public.

Directly Measured Denitrification Reveals Oyster Aquaculture and Restored Oyster Reefs Remove Nitrogen at Comparable High Rates

Coastal systems are increasingly impacted by over-enrichment of nutrients, which has cascading effects for ecosystem functioning. Oyster restoration and aquaculture are both hypothesized to mitigate excessive nitrogen (N) loads via benthic denitrification. The degree to which these management activities perform similar functions for removing N, however, has not been extensively examined in New England, a place where nutrient runoff is high and increasing oyster (Crassostrea virginica) restoration and aquaculture activity is taking place. Here, we use a novel in situ methodology to directly measure net N2 and O2 fluxes across the sediment-water interface in a shallow (~1 m) coastal pond in southern Rhode Island. We collected data seasonally during 2013 and 2014 at restored oyster reefs, oyster aquaculture, oyster cultch (shell), and bare sediment. Restored oyster reefs and aquaculture had the highest mean (± SE) denitrification rates, 581.9 (± 164.2) and 346 (± 168.6) μmol N2-N m-2 h-1, respectively, and are among the highest recorded for oyster-dominated environments. Denitrification rates at sites with oyster cultch were 60.9 (± 44.3) μmol N2-N m-2 h-1, which is substantially less than the sites with active oysters but still more than 50% higher than denitrification rates measured in bare sediment (24.4 ± 10.1 μmol N2-N m-2 h-1). The increase in denitrification rates at treatments, however, varied by season and the greatest rates for restored reefs were in the fall. Overall, the greatest aggregate denitrification rates occurred in the fall. Sediment oxygen demand (SOD) followed similar patterns but with greater overall rates in the summer, and displayed a strong linear relationship with denitrification (R2 = 0.9273). Our results demonstrate that habitats associated with live oysters have higher net denitrification rates and that oyster reef restoration and oyster aquaculture may provide similar benefits to the ecosystem in terms of N removal. However, gas fluxes may also be affected where three-dimensional structure is introduced via oyster shell cultch and this appears to be seasonally-dependent. These data will be important for managers as they incorporate oysters into nutrient reduction strategies and consider system-level trade-offs in services provided by oyster reef restoration and aquaculture activities.

Molecular evidence for sediment nitrogen fixation in a temperate New England estuary.

Primary production in coastal waters is generally nitrogen (N) limited with denitrification outpacing nitrogen fixation (N2-fixation). However, recent work suggests that we have potentially underestimated the importance of heterotrophic sediment N2-fixation in marine ecosystems. We used clone libraries to examine transcript diversity of nifH (a gene associated with N2-fixation) in sediments at three sites in a temperate New England estuary (Waquoit Bay, Massachusetts, USA) and compared our results to net sediment N2 fluxes previously measured at these sites. We observed nifH expression at all sites, including a site heavily impacted by anthropogenic N. At this N impacted site, we also observed mean net sediment N2-fixation, linking the geochemical rate measurement with nifH expression. This same site also had the lowest diversity (non-parametric Shannon = 2.75). At the two other sites, we also detected nifH transcripts, however, the mean N2 flux indicated net denitrification. These results suggest that N2-fixation and denitrification co-occur in these sediments. Of the unique sequences in this study, 67% were most closely related to uncultured bacteria from various marine environments, 17% to Cluster III, 15% to Cluster I, and only 1% to Cluster II. These data add to the growing body of literature that sediment heterotrophic N2-fixation, even under high inorganic nitrogen concentrations, may be an important yet overlooked source of N in coastal systems.

Does elevated CO2 alter silica uptake in trees

Human activities have greatly altered global carbon (C) and Nitrogen (N) cycling. In fact, atmospheric concentrations of carbon dioxide (CO2) have increased 40% over the last century and the amount of N cycling in the biosphere has more than doubled. In an effort to understand how plants will respond to continued global CO2 fertilization, long-term free-air CO2 enrichment experiments have been conducted at sites around the globe. Here we examine how atmospheric CO2 enrichment and N fertilization affects the uptake of silicon (Si) in the Duke Forest, North Carolina, a stand dominated by Pinus taeda (loblolly pine), and five hardwood species. Specifically, we measured foliar biogenic silica concentrations in five deciduous and one coniferous species across three treatments: CO2 enrichment, N enrichment, and N and CO2 enrichment. We found no consistent trends in foliar Si concentration under elevated CO2, N fertilization, or combined elevated CO2 and N fertilization. However, two-thirds of the tree species studied here have Si foliar concentrations greater than well-known Si accumulators, such as grasses. Based on net primary production values and aboveground Si concentrations in these trees, we calculated forest Si uptake rates under control and elevated CO2 concentrations. Due largely to increased primary production, elevated CO2 enhanced the magnitude of Si uptake between 20 and 26%, likely intensifying the terrestrial silica pump. This uptake of Si by forests has important implications for Si export from terrestrial systems, with the potential to impact C sequestration and higher trophic levels in downstream ecosystems.