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The excessive input of anthropogenic nutrients to coastal waters has impacted estuarine ecosystems worldwide, resulting in low oxygen conditions, increases in the severity and frequency of nuisance and harmful algal blooms, the loss of submerged aquatic vegetation, and changes to community diversity and structure. Salt marshes are ecologically important estuarine ecosystems that provide habitat for marine and terrestrial species, provide protection from storm surge, and transform nutrients at high rates. Because of these qualities there is much interest from scientific and management communities to understand the impacts of nutrient enrichment on salt marshes, as well as the potential for marshes to remove excess nutrients from estuarine systems. Nitrogen (N) is the limiting nutrient in most coastal ecosystems and therefore studies on nutrient enrichment in marshes have largely focused on N. While decades of research have characterized the exchange of nitrogen between marshes and adjacent tidal waters, the net impact of the microbial-mediated fluxes of nitrogen gas (N2) is less understood. Nitrogen fixation and denitrification serve as important pathways for sources and sinks of N within the ecosystem. Nitrogen fixation is the process by which N2 gas is fixed into a biologically-available form and can be important in enhancing marsh primary production. Denitrification transforms nitrate into N2 gas, effectively removing N from the marsh. Both processes are controlled by various factors, including dissolved inorganic nitrogen (DIN) levels. Prior research has demonstrated that N fixation can be suppressed by high levels of ammonium and nitrate while denitrification is often enhanced by an increased availability of nitrate. Many studies have examined the impact of N enrichment on denitrification and/or N fixation in salt marshes and have found varying results. While some have reported that higher DIN levels stimulated denitrification and suppressed N fixation, opposite or no relationships have also been observed. The variation in findings demonstrates that more investigation is needed, particularly because of the spatial heterogeneity of salt marshes and the methodological difficulties in measuring denitrification and N fixation. Even less is known regarding the impact of nutrient reductions on salt marsh biogeochemistry and N cycling. In many estuaries and coastal watersheds management actions to reduce nutrient inputs from wastewater treatment facilities and septic systems have been or will soon be implemented. Therefore it is increasingly important to better understand the response of salt marsh nutrient cycling to both nutrient enrichment and reduction. To examine the impact of changes in N regime on salt marsh N cycling, we measured denitrification and N fixation in two marshes with varying degrees of longterm N enrichment from tidal waters. We conducted our work in Narragansett Bay, Rhode Island, which has an established down-bay gradient in estuarine nutrient concentrations. Our highly N enriched marsh was located in the Providence River Estuary, where the majority of anthropogenic N enters the Bay, and our low N marsh was located near the mouth of the Bay. To compare N cycling activity between the two marshes and to understand how activity differs seasonally, we measured denitrification and N fixation in separate sediment incubations on a monthly basis over an annual cycle (excluding winter months) from June 2011 to June 2012. Our measurements were made in intact sediment cores collected from the tidally influenced low marsh zone dominated by short-form Spartina alterniflora. While this was meant to capture differences between the marshes with long-term exposure to high or low tidal N inputs, we also aimed to understand how N cycling activity would respond to changes in N regime. Therefore we additionally conducted an experiment in which sediment cores were extracted and transplanted between the marshes, along with cores that were re-planted within the same marsh (serving as experimental controls). After three months (July to October 2011) we collected the cores and in two separate incubations measured denitrification and N fixation rates. For all of our denitrification measurements, we employed the isotope pairing technique (IPT) in which a heavy isotope nitrate (N-NO3) tracer is added to the overlying water to track the production of N2 gas. The IPT method allowed us to measure ambient denitrification, including differentiating direct denitrification from coupled nitrification-denitrification. We were also able to measure the capacity for denitrification. By measuring and distinguishing the different types of denitrification using IPT, we could comprehensively characterize the role of marsh sediments in removing tidal N (via direct denitrification) and the total capacity to denitrify when nitrate was not limiting (i.e. very high nitrate concentrations). We found that ambient denitrification was greater at the high N marsh, due to enhanced direct denitrification stimulated by elevated levels of tidal nitrate. The difference in activity between marshes was greatest in the early fall and spring when nitrate levels seasonally peaked in the surface waters at the high N marsh. Coupled nitrification-denitrification and sediment oxygen demand were similar between sites, suggesting that sediment carbon availability was also similar. We also observed greater denitrification capacity at the high N marsh, suggesting that the denitrifiers were better adapted to efficiently process high N inputs. Results from the transplant experiment corroborated these findings. When sediments from the low N marsh were transplanted into the high N environment, ambient denitrification activity increased but never fully reached levels seen in sediments native to the high N marsh. Additionally, the capacity for denitrification was greatest in cores from the high N marsh that remained in their high N environment. In contrast, denitrification capacity and ambient activity decreased when cores from the high N marsh were transplanted into a low N environment. Our experiments demonstrated that N enrichment stimulated direct denitrification and suppressed N fixation, while N reductions had the opposite effects. The overall results suggest that external N inputs act as an important control on denitrification, driving short-term responses to changes in N regime, as well as shaping microbial activity on longer time scales. For the N fixation measurements we employed the commonly used acetylene reduction assay technique, a proxy measurement that tracks the reduction of acetylene gas to ethylene by nitrogenase, the enzyme responsible for N fixation in diazotrophs. Similar to denitrification, we measured N fixation on a monthly basis over an annual cycle in intact, whole cores. We also compared incubation techniques because few salt marsh N fixation studies have employed the use of whole cores and instead have used bottle-type incubations with small sediment plug samples. In four of these monthly incubations, measurements made in whole cores were compared to concurrent sediment plug bottle incubations. Though the sediment plug incubations yielded significantly higher rates than the whole cores, we observed greater N fixation at the low N marsh using both methods. Because carbon availability was similar between marshes, we attribute the differences between marshes to the suppression of N fixation by high tidal DIN levels at the high N marsh. The N fixation transplant experiment also demonstrated that activity was likely suppressed at the high N marsh. Nitrogen fixation declined when sediments were transplanted from the low N marsh into an N enriched environment, but never decreased to the low levels seen in sediments native to the high N marsh. The impacts of N reduction on sediments from the high N marsh were not clear due to high variability among cores. Similar to denitrification, we observed short-term responses to changes in N regime and a potential legacy effect from long-term N availability that influenced N fixation activity. Regarding the role of salt marshes in nitrogen removal, net N2 flux was dominated by denitrification, with direct denitrification driving differences between sites in tidal N removal. However, our observed rates of denitrification and N fixation were at the lower end of the range reported in the literature. Also, the estimated percent of N removed in tidal water per square meter of low marsh was small (5% annual average in the high N marsh and 12% in the low N marsh), owing to relatively low rates of denitrification paired with a limited amount of time that the low marsh was flooded with tidal waters. The overall trends we observed in all of our experiments, however, demonstrate that seasonal and historical N availability and changes in N regime have significant impacts on N fixation and denitrification in these marshes.

RESPONSES OF NITROGEN CYCLING TO NUTRIENT ENRICHMENT IN NEW ENGLAND SALT MARSHES OVER AN ANNUAL CYCLE