Nitrogen regulation by natural systems in “unnatural” landscapes: denitrification in ultra-urban coastal ecosystems

Figures & data

Figure 1. Examples of habitat found in temperate coastal ecosystems (a) Salt marsh islands, (b) Perimeter marsh downstream of a Combined Sewer Outfall, and (c) perimeter tidal creek and marsh platform. Images from Jamaica Bay, New York in 2011. Source: Bernice Rosenzweig.

Table 1. Environmental controls on denitrification and anammox.

Environmental Control	Effects on denitrification and anammox
Labile organic carbon	● Denitrification is heterotrophic and dependent on the availability of organic carbon (Velinsky et al. 2017; Marchant et al. 2016; Gardner and McCarthy 2009; Smyth et al. 2013; Piehler and Smyth 2011; Deek et al. 2013). ● When/where labile organic carbon is abundant, denitrifying microorganisms usually outcompete anammox microorganisms for NO2^−, since denitrifying microorganisms vastly outnumber anammox microorganisms and, under most conditions, denitrification will be thermodynamically favored. (Thamdrup and Dalsgaard 2002; Lam and Kuypers 2011; Engström et al. 2005) ● Under some conditions, anammox has been observed to be positively correlated with sediment organic carbon since sediments with abundant organic carbon can support high rates of NO2^− production, which can support increased rates of anammox even though denitrification is thermodynamically favored and remains relatively more important. (Trimmer, Nicholls, and Deflandre 2003)
Nitrate (NO3^−)/Nitrite (NO2^−) concentrations	● Denitrification rates are dependent on the availability of NO3^− and NO2^− ● Trimmer et al. (2005) observed a biphasic relationship between anammox rates and NO3^−concentrations, which they attributed to competition for NO2^− when its supply through denitrification is limited and enhancement of anammox when NO2^− is generated in abundance by denitrification.
Ammonium (NH4^+)/Ammonia (NH3) concentration	In systems with high NH4^+ concentrations (such as those that receive effluent from WWTPs): ● Anammox can actually be thermodynamically favored over denitrification (Babbin and Ward 2013). ● The occurrence of anammox under high NH4^+ loading would also be highly dependent on pH, since anammox bacteria have been found to be inhibited by the build-up NH3 (Jin et al. (2012)
Turbidity/light penetration	Sea grass stands are hotspots of denitrification (Velinsky et al. 2017; Marchant et al. 2016; Gardner and McCarthy 2009; Smyth et al. 2013; Piehler and Smyth 2011; Deek et al. 2013). ● Reduced light penetration can degrade sea grass productivity and areal coverage (Valiela 2015; Burkholder, Tomasko, and Touchette 2007).
Anoxic water column	Although denitrification and anammox require localized anoxia to be thermodynamically favorable, anoxic water column conditions can: ● Directly inhibit coupled nitrification-denitrification ● Result in the accumulation of sulfide in surficial sediments, which inhibits both coupled nitrification-denitrification and anammox (Joye and Hollibaugh 1995; Jensen et al. 2008; Sears et al. 2004; Thamdrup and Dalsgaard 2002) ● Indirectly reduce the system-level rate of denitrification and anammox by changing the composition of benthic faunal communities, favoring species that are less effective for bioturbation.
Trace pharmaceuticals	Broad spectrum antibiotics: ● Are known to inhibit the synthesis of the enzymes needed to facilitate denitrification by microorganisms (Tiedje, Simkins and Groffman 1989) ● May also inhibit existing denitrification enzyme activity in microbes (Pell et al. 1996; Brooks, Smith and Macalady 1992) ● In laboratory studies designed to replicate the coastal environment, residual antibiotics and other pharmaceuticals may decrease overall rates of denitrification while also resulting in increased emissions of N2O (Hou et al. 2015a; Yin et al. 2017, Yin et al. 2016).
Other urban pollutants	● Heavy metal contamination can actually enhance denitrification in some settings by selecting for contaminant-tolerant species with increased burrowing activity, which can facilitate the transport of NO3^− into sediment zones where denitrification is favorable (Banks et al. 2013). ● Some organic contaminants and microplastics reduce burrowing activity in marine macroinvertebrates, with potential implications for nutrient transport, redox zonation and the occurrence of denitrification and anammox (Green et al. 2016).

Figure 2. Natural (dendritic) tidal creeks and ditched (perpendicular) channels shown in a digital elevation model of two salt marsh islands of Jamaica Bay. Ditching was commonly used for mosquito control in urban wetlands during the twentieth century, but may unintentionally impact nitrogen regulation by enhancing tidal flushing and/or modifying macroinvertebrate community structure. Land elevation data are from the USA Geological Survey (USGS) 1m National Elevation Dataset https://lta.cr.usgs.gov/NED.

Figure 3. Simplified representation of nitrogen cycling processes in coastal ecosystems.

Figure 4. Hypothetical cross-section of a coastal salt marsh showing potential transport pathways of water column N and sites where denitrification may occur.

Figure 5. Map of the Jamaica Bay Watershed, which includes locations of Waste Water Treatment Plant (WWTP) Facilities and CSOs. Vegetation coverage is modified from the Ecological Covertype Map, Version 2, developed by the Natural Areas Conservancy (O'Neill-Dunne et al. 2014). The vegetation layer is only available for New York City. Impervious cover data is from the 2011 National Land Cover Database (Homer et al. 2012).

Table 2. Jamaica Bay sources of N_r.

Jamaica Bay Nr Source	Estimated Annual Load (kg N yr ^−1)	% of Total Annual Load	Estimation Source/Approach
Wastewater Treatment Plants (WWTPs)	4.5x10^6	76.3	NYC DEP, Unpublished, December 2016
Atmospheric Deposition	9.8 x10^5	16.5	Du et al. 2014 (Using highest value observed for Northeast United States)
Groundwater Discharge	2.5 x10^5	4.3	Benotti, Abbene, and Terracciano 2007
Combined Sewer Overflows (CSOs)	8.9 x10^4	1.5	Benotti, Abbene, and Terracciano 2007
Subway Dewatering (pumped water bypasses WWTPs)	8.4 x10^4	1.4	Benotti, Abbene, and Terracciano 2007
Landfill Leaching	~ 0	~ 0	Assumed to be negligible following landfill capping and remediation over the past decade.
Total Nr input to Jamaica Bay:	5.9x10^6

Figure 6. N loading from the 4 Waste Water Treatment Plants (WWTPs) in the Jamaica Bay Watershed. Data from the EPA ECHO Monthly Discharge Monitoring Report (https://cfpub.epa.gov/dmr/index.cfm).

Figure 7. Annual median (a) NO₃⁻ and (b) NH₄⁺ measured in Jamaica Bay surface waters in 2013. Data from the Jamaica Bay Water Quality Database (City University of New York (CUNY) Brooklyn College, Center for International Earth Science Information Network (CIESIN) Columbia University, New York City Department of Environmental Protection (NYCDEP), and National Park Service (NPS) 2017), see http://www.ciesin.columbia.edu/jbwq/parameters.html for detailed sampling methods.

Table 3. Comparison of nitrogen removal efficiency in studies of urban coastal systems.

Site	Area of Coastal Habit Considered (km^−2)	N load per unit area of coastal habitat (kg N km^−2 yr^−1)	% of N removed as N2 (through denitrification and anammox)	Approach	Study
Colne River Estuary, United Kingdom	4.8	5.1x10^4 (studies conducted from 1995 – 1998)	18–27 (studies conducted from 1993–1995)	IPT	(N loads from (Dong, Nedwell, and Stott 2006))
Wadden Sea, The Netherlands/Germany	14.7x10^4	5.1 x10^4 to 5.6 x10^4	~ 30	IPT	(Gao et al. 2012)
Elbe Estuary	Not provided	4.7x10^7 kg N yr^−1 (areal rates not provided)	~ 11 (assuming the March-September average rate is also applicable from October-February)	IPT	(Deek et al. 2013)
Jinpu Bay, China	2,000	3.5 x10^3	~ 20	IPT	(Yin et al. 2015)
Barnegat Bay, NJ	280 (including 110km^2 of wetlands)	2.4 x10^3	~ 28 ± 7	MIMS	(Velinsky et al. 2017)
Jamaica Bay, NY	89 (including 22 km^2 of wetlands)	6.6 x10^4	~ 17	Rates obtained by Cornwell, Michael Kemp, and Kana 1999(MIMS) and Koop-Jakobsen and Giblin 2010 (IPT)	This review

IPT: Isotope Pairing Technique; MIMS: N₂:Ar ratio approach using Membrane Inlet Mass Spectrometry

Figure 8. Tidal wetlands with % of example year inundated. Vegetation coverage is modified from the Ecological Covertype Map, Version 2, developed by the Natural Areas Conservancy (Forgione et al. 2015). The vegetation layer is only available for New York City and a small area of tidal wetlands outside the city’s political boundary are excluded here. Water-level time series are from Year 2013 at USGS Tide Gage 01311850 (Jamaica Bay at Inwood). Vertical adjustments were made using vData version 3.3. Land elevation data is from the USGS 1m National Elevation Dataset.

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