Rapid recovery of carbon cycle processes after the cessation of chronic nutrient enrichment.

Salt marshes provide critical ecosystem services including some of the highest rates of carbon storage on Earth. However, many salt marshes receive very high nutrient loads and there is a growing body of evidence indicating that this nutrient enrichment alters carbon cycle processes. While many restoration plans prioritize nutrient management in their efforts to conserve salt marsh ecosystems, there has been little empirical investigation of the capacity for carbon cycle processes to recover once nutrient loading is reduced. To address this, we compared rates of greenhouse gas fluxes (i.e., CO2 and methane) measured using static chambers, and soil organic matter decomposition, using both litter bags and the Tea Bag Index (TBI), during the last two years of a long-term, ecosystem-scale nutrient enrichment experiment (2015-2016) as well as in the first two years of recovery post-enrichment (2017-2018). We found that both ecosystem respiration (Reco) and decomposition processes (i.e., rhizome decomposition and soil organic matter stabilization) were enhanced by nutrient enrichment, but returned to reference ecosystem levels within the first year following the cessation of nutrient enrichment and remained at reference levels in the second year. These results suggest that management practices intended to reduce nutrient loads in coastal systems may, in fact, allow for rapid recovery of carbon cycle processes, potentially restoring the high carbon sequestration rates of these blue carbon ecosystems.

Not All Nitrogen Is Created Equal: Differential Effects of Nitrate and Ammonium Enrichment in Coastal Wetlands.

Excess reactive nitrogen (N) flows from agricultural, suburban, and urban systems to coasts, where it causes eutrophication. Coastal wetlands take up some of this N, thereby ameliorating the impacts on nearshore waters. Although the consequences of N on coastal wetlands have been extensively studied, the effect of the specific form of N is not often considered. Both oxidized N forms (nitrate, NO3-) and reduced forms (ammonium, NH4+) can relieve nutrient limitation and increase primary production. However, unlike NH4+, NO3- can also be used as an electron acceptor for microbial respiration. We present results demonstrating that, in salt marshes, microbes use NO3- to support organic matter decomposition and primary production is less stimulated than when enriched with reduced N. Understanding how different forms of N mediate the balance between primary production and decomposition is essential for managing coastal wetlands as N enrichment and sea level rise continue to assail our coasts.

Linking permafrost thaw to shifting biogeochemistry and food web resources in an arctic river.

Rapidly, increasing air temperatures across the Arctic are thawing permafrost and exposing vast quantities of organic carbon, nitrogen, and phosphorus to microbial processing. Shifts in the absolute and relative supplies of these elements will likely alter patterns of ecosystem productivity and change the way carbon and nutrients are delivered from upland areas to surface waters such as rivers and lakes. The ultra-oligotrophic nature of surface waters across the Arctic renders these ecosystems particularly susceptible to changes in productivity and food web dynamics as permafrost thaw alters terrestrial-aquatic linkages. The objectives of this study were to evaluate decadal-scale patterns in surface water chemistry and assess potential implications of changing water chemistry to benthic organic matter and aquatic food webs. Data were collected from the upper Kuparuk River on the North Slope of Alaska by the U.S. National Science Foundation's Long-Term Ecological Research program during 1978-2014. Analyses of these data show increases in stream water alkalinity and cation concentrations consistent with signatures of permafrost thaw. Changes are also documented for discharge-corrected nitrate concentrations (+), discharge-corrected dissolved organic carbon concentrations (-), total phosphorus concentrations (-), and δ13 C isotope values of aquatic invertebrate consumers (-). These changes show that warming temperatures and thawing permafrost in the upland environment are leading to shifts in the supply of carbon and nutrients available to surface waters and consequently changing resources that support aquatic food webs. This demonstrates that physical, geochemical, and biological changes associated with warming permafrost are fundamentally altering linkages between upland and aquatic ecosystems in rapidly changing arctic environments.

Saltmarsh plant responses to eutrophication.

In saltmarsh plant communities, bottom-up pressure from nutrient enrichment is predicted to increase productivity, alter community structure, decrease biodiversity, and alter ecosystem functioning. Previous work supporting these predictions has been based largely on short-term, plot-level (e.g., 1-300 m2 ) studies, which may miss landscape-level phenomena that drive ecosystem-level responses. We implemented an ecosystem-scale, nine-year nutrient experiment to examine how saltmarsh plants respond to simulated conditions of coastal eutrophication. Our study differed from previous saltmarsh enrichment studies in that we applied realistic concentrations of nitrate (70-100 µM NO3- ), the most common form of coastal nutrient enrichment, via tidal water at the ecosystem scale (~60,000 m2 creeksheds). Our enrichments added a total of 1,700 kg N·creek-1 ·yr-1 , which increased N loading 10-fold vs. reference creeks (low-marsh, 171 g N·m-2 ·yr-1 ; high-marsh, 19 g N·m-2 ·yr-1 ). Nutrients increased the shoot mass and height of low marsh, tall Spartina alterniflora; however, declines in stem density resulted in no consistent increase in aboveground biomass. High-marsh plants S. patens and stunted S. alterniflora did not respond consistently to enrichment. Nutrient enrichment did not shift community structure, contrary to the prediction of nutrient-driven dominance of S. alterniflora and Distichlis spicata over S. patens. Our mild responses may differ from the results of previous studies for a number of reasons. First, the limited response of the high marsh may be explained by loading rates orders of magnitude lower than previous work. Low loading rates in the high marsh reflect infrequent inundation, arguing that inundation patterns must be considered when predicting responses to estuarine eutrophication. Additionally, we applied nitrate instead of the typically used ammonium, which is energetically favored over nitrate for plant uptake. Thus, the form of nitrogen enrichment used, not just N-load, may be important in predicting plant responses. Overall, our results suggest that when coastal eutrophication is dominated by nitrate and delivered via flooding tidal water, aboveground saltmarsh plant responses may be limited despite moderate-to-high water-column N concentrations. Furthermore, we argue that the methodological limitations of nutrient studies must be considered when using results to inform management decisions about wetlands.

Nutrient enrichment induces dormancy and decreases diversity of active bacteria in salt marsh sediments.

Microorganisms control key biogeochemical pathways, thus changes in microbial diversity, community structure and activity can affect ecosystem response to environmental drivers. Understanding factors that control the proportion of active microbes in the environment and how they vary when perturbed is critical to anticipating ecosystem response to global change. Increasing supplies of anthropogenic nitrogen to ecosystems globally makes it imperative that we understand how nutrient supply alters active microbial communities. Here we show that nitrogen additions to salt marshes cause a shift in the active microbial community despite no change in the total community. The active community shift causes the proportion of dormant microbial taxa to double, from 45 to 90%, and induces diversity loss in the active portion of the community. Our results suggest that perturbations to salt marshes can drastically alter active microbial communities, however these communities may remain resilient by protecting total diversity through increased dormancy.

Flowering and biomass allocation in U.S. Atlantic coast Spartina alterniflora.

PREMISE OF THE STUDY: Salt marshes are highly productive and valuable ecosystems, providing many services on which people depend. Spartina alterniflora Loisel (Poaceae) is a foundation species that builds and maintains salt marshes. Despite this species' importance, much of its basic reproductive biology is not well understood, including flowering phenology, seed production, and the effects of flowering on growth and biomass allocation. We sought to better understand these life history traits and use that knowledge to consider how this species may be affected by climate change. METHODS: We examined temporal and spatial patterns in flowering and seed production in S. alterniflora at a latitudinal scale (along the U.S. Atlantic coast), regional scale (within New England), and local scale (among subhabitats within marshes) and determined the impact of flowering on growth allocation using field and greenhouse studies. KEY RESULTS: Flowering stem density did not vary along a latitudinal gradient, while at the local scale plants in the less submerged panne subhabitats produced fewer flowers and seeds than those in more frequently submerged subhabitats. We also found that a shift in biomass allocation from above to belowground was temporally related to flowering phenology. CONCLUSIONS: We expect that environmental change will affect seed production and that the phenological relationship with flowering will result in limitations to belowground production and thus affect marsh elevation gain. Salt marshes provide an excellent model system for exploring the interactions between plant ecology and ecosystem functioning, enabling better predictions of climate change impacts.

Watershed responses to Amazon soya bean cropland expansion and intensification.

The expansion and intensification of soya bean agriculture in southeastern Amazonia can alter watershed hydrology and biogeochemistry by changing the land cover, water balance and nutrient inputs. Several new insights on the responses of watershed hydrology and biogeochemistry to deforestation in Mato Grosso have emerged from recent intensive field campaigns in this region. Because of reduced evapotranspiration, total water export increases threefold to fourfold in soya bean watersheds compared with forest. However, the deep and highly permeable soils on the broad plateaus on which much of the soya bean cultivation has expanded buffer small soya bean watersheds against increased stormflows. Concentrations of nitrate and phosphate do not differ between forest or soya bean watersheds because fixation of phosphorus fertilizer by iron and aluminium oxides and anion exchange of nitrate in deep soils restrict nutrient movement. Despite resistance to biogeochemical change, streams in soya bean watersheds have higher temperatures caused by impoundments and reduction of bordering riparian forest. In larger rivers, increased water flow, current velocities and sediment flux following deforestation can reshape stream morphology, suggesting that cumulative impacts of deforestation in small watersheds will occur at larger scales.

Coastal eutrophication as a driver of salt marsh loss.

Salt marshes are highly productive coastal wetlands that provide important ecosystem services such as storm protection for coastal cities, nutrient removal and carbon sequestration. Despite protective measures, however, worldwide losses of these ecosystems have accelerated in recent decades. Here we present data from a nine-year whole-ecosystem nutrient-enrichment experiment. Our study demonstrates that nutrient enrichment, a global problem for coastal ecosystems, can be a driver of salt marsh loss. We show that nutrient levels commonly associated with coastal eutrophication increased above-ground leaf biomass, decreased the dense, below-ground biomass of bank-stabilizing roots, and increased microbial decomposition of organic matter. Alterations in these key ecosystem properties reduced geomorphic stability, resulting in creek-bank collapse with significant areas of creek-bank marsh converted to unvegetated mud. This pattern of marsh loss parallels observations for anthropogenically nutrient-enriched marshes worldwide, with creek-edge and bay-edge marsh evolving into mudflats and wider creeks. Our work suggests that current nutrient loading rates to many coastal ecosystems have overwhelmed the capacity of marshes to remove nitrogen without deleterious effects. Projected increases in nitrogen flux to the coast, related to increased fertilizer use required to feed an expanding human population, may rapidly result in a coastal landscape with less marsh, which would reduce the capacity of coastal regions to provide important ecological and economic services.

Microbial community composition in sediments resists perturbation by nutrient enrichment.

Functional redundancy in bacterial communities is expected to allow microbial assemblages to survive perturbation by allowing continuity in function despite compositional changes in communities. Recent evidence suggests, however, that microbial communities change both composition and function as a result of disturbance. We present evidence for a third response: resistance. We examined microbial community response to perturbation caused by nutrient enrichment in salt marsh sediments using deep pyrosequencing of 16S rRNA and functional gene microarrays targeting the nirS gene. Composition of the microbial community, as demonstrated by both genes, was unaffected by significant variations in external nutrient supply in our sampling locations, despite demonstrable and diverse nutrient-induced changes in many aspects of marsh ecology. The lack of response to external forcing demonstrates a remarkable uncoupling between microbial composition and ecosystem-level biogeochemical processes and suggests that sediment microbial communities are able to resist some forms of perturbation.

Salt marsh ecosystem biogeochemical responses to nutrient enrichment: a paired 15N tracer study.

We compared processing and fate of dissolved NO3- in two New England salt marsh ecosystems, one receiving natural flood tide concentrations of approximately 1-4 micromol NO3-/ L and the other receiving experimentally fertilized flood tides containing approximately 70-100 micromol NO3-/ L. We conducted simultaneous 15NO3- (isotope) tracer additions from 23 to 28 July 2005 in the reference (8.4 ha) and fertilized (12.4 ha) systems to compare N dynamics and fate. Two full tidal cycles were intensively studied during the paired tracer additions. Resulting mass balances showed that essentially 100% (0.48-0.61 mol NO3-N.ha(-1).h(-1)) of incoming NO3- was assimilated, dissimilated, sorbed, or sedimented (processed) within a few hours in the reference system when NO3- concentrations were 1.3-1.8 micromol/L. In contrast, only 50-60% of incoming NO3- was processed in the fertilized system when NO3- concentrations were 84-96 micromol/L; the remainder was exported in ebb tidewater. Gross NO3- processing was approximately 40 times higher in the fertilized system at 19.34-24.67 mol NO3-N.ha(-1).h(-1). Dissimilatory nitrate reduction to ammonium was evident in both systems during the first 48 h of the tracer additions but <1% of incoming 15NO3- was exported as 15NH4+. Nitrification rates calculated by 15NO3- dilution were 6.05 and 4.46 mol.ha(-1).h(-1) in the fertilized system but could not be accurately calculated in the reference system due to rapid (<4 h) NO3- turnover. Over the five-day paired tracer addition, sediments sequestered a small fraction of incoming NO3-, although the efficiency of sequestration was 3.8% in the reference system and 0.7% in the fertilized system. Gross sediment N sequestration rates were similar at 13.5 and 12.6 mol.ha(-1).d(-1), respectively. Macrophyte NO3- uptake efficiency, based on tracer incorporation in aboveground tissues, was considerably higher in the reference system (16.8%) than the fertilized system (2.6%), although bulk uptake of NO3- by plants was lower in the reference system (1.75 mol NO3-.ha(-1).d(-1)) than the fertilized system (approximately 10 mol NO3-.ha(-1).d(-1)). Nitrogen processing efficiency decreased with NO3- load in all pools, suggesting that the nutrient processing capacity of the marsh ecosystem was exceeded in the fertilized marsh.

Salt marsh sediment bacteria: their distribution and response to external nutrient inputs.

A primary focus among microbial ecologists in recent years has been to understand controls on the distribution of microorganisms in various habitats. Much less attention has been paid to the way that environmental disturbance interacts with processes that regulate bacterial community composition. We determined how human disturbance affected the distribution and community structure of salt marsh sediment bacteria by using denaturing gradient gel electrophoresis of 16S rRNA in five different habitats in each of four salt marshes located in northeastern Massachusetts, USA. Two of the four marsh creeks were experimentally enriched 15 x above background by the addition of nitrogen and phosphorus fertilizers for two or more growing seasons. Our results indicate that extrinsic factors acting at broad scales do not influence the distribution of salt marsh sediment bacteria. Intrinsic factors, controlled by local-scale environmental heterogeneity, do play a role in structuring these sediment microbial communities, although nutrient enrichment did not have a consequential effect on the microbial community in most marsh habitats. Only in one habitat, a region of the marsh creek wall that is heavily colonized by filamentous algae, did we see any effect of fertilization on the microbial community structure. When similar habitats were compared among marshes, there was considerable convergence in the microbial community composition during the growing season. Environmental factors that correlated best with microbial community composition varied with habitat, suggesting that habitat-specific intrinsic forces are primarily responsible for maintaining microbial diversity in salt marsh sediments.