Abstract
Although sediments of the German Wadden Sea are suspected to eliminate a considerable share of nitrate delivered to the SE North Sea, their denitrification rates have not been systematically assessed. We determined N2 production rates over seasonal cycles (February 2009–April 2010) at two locations with two sediments types each, the first site (Meldorf Bight) receiving nitrate during all seasons from the Elbe river plume, and a second site on the island of Sylt, where nitrate is depleted during summer months. In sediments from the Sylt site, N2 production ranged from 15 to 32 μmol N2 m−2 h−1 in the fine sand station and from 7 to 13 μmol N2 m−2 h−1 in the coarse sand station; N2 production was not detected when nitrate was depleted in May and July of 2009. N2 production in the Meldorf Bight sediments were consistently detected at higher rates (58–130 μmol N2 m−2 h−1 in the very fine sand station and between 14 and 30 μmol N2 m−2 h−1 in the medium sand station). Analysis of ancillary parameters suggests that major factors controlling N2 production in coastal sediments of the German Wadden Sea are the nitrate concentrations in the overlying water, the ambient temperature, and the organic matter content of the sediment. Extrapolating our spot measurements to the zone of nitrate availability and sediment types, we estimate an annual nitrogen removal rate around 16 kt N year−1 for the entire northern sector of the German Wadden Sea area. This corresponds to 14% of the annual Elbe river nitrogen load.
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References
An S, Gardner WS (2002) Dissimilatory nitrate reduction to ammonium (DNRA) as a nitrogen link versus denitrification as a sink in a shallow estuary (Laguna Madre/Baffin Bay, TX). Mar Ecol-Prog Ser 237:41–50
An S, Gardner WS, Kana T (2001) Simultaneous measurement of denitrification and nitrogen fixation using isotope pairing with membrane inlet mass spectrometry analysis. Appl Environ Microbiol 67:1171–1178
Armstrong FAJ, Sterns CR, Strickland JDH (1967) The measurement of upwelling and subsequent biological processes by means of the Technicon AutoAnalyzer and associated equipment. Deep-Sea Res 14:381–389
Brewer PG, Riley JP (1966) The automatic determination of silicate-silicon in natural waters with special reference to sea water. Anal Chim Acta 35:514–519
Brion N, Baeyens W, De Galan S, Elskens M, Laane RW (2004) The North Sea: source or sink for nitrogen and phosphorus to the Atlantic Ocean? Biogeochemistry 68:277–296
Burgin AJ, Hamilton SK (2007) Have we overemphasized denitrification in aquatic ecosystems: a review of nitrate removal pathways. Front Ecol Environ 5:89–96
Christensen PB, Nielsen LP, Sörensen J, Revsbech NP (1990) Denitrification in nitrate rich streams: diurnal and seasonal variation related to benthic oxygen metabolism. Limnol Oceanogr 35:640–651
Christensen PB, Rysgaard S, Sloth NP, Dalsgaard T, Schwaerter S (2000) Sediment mineralization, nutrient fluxes, denitrification and dissimilatory nitrate reduction to ammonium in an estuarine fjord with sea cage trout farms. Aq Micro Ecol 21:73–84
Cook PLM, Wenzhöfer F, Rysgaard S, Galaktionov OS, Meysman FJR, Eyre BD, Cornwell J, Huettel M, Glud RN (2006) Quantification of denitrification in permeable sediments: insights from a two-dimensional simulation analysis and experimental data. Limnol Oceanogr Method 4:294–307
Cornwell JC, Kemp WM, Kana TM (1999) Denitrification in coastal ecosystems. Aquat Ecol 33:41–54
de Beer D, Wenzhöfer F, Ferdelman TG, Boehme SE, Huettel M, van Beusekom JEE, Böttcher ME, Musat N, Dubilier N (2005) Transport and mineralization rates in North Sea sandy intertidal sediments, Sylt-Rømø Basin, Waddensea. Limnol Oceanogr 50:113–127
Deutsch B, Forster S, Wilhelm M, Dippner JW, Voss M (2010) Denitrification in sediments as a major nitrogen sink in the Baltic Sea: an extrapolation using sediment characteristics. Biogeoscie Disc 7:2487–2521
Duff JH, Triska FJ, Oremland RS (1984) Denitrification associated with stream Periphyton: chamber estimates from undisrupted communities. J Environ Qual 13:514–518
DWD (2010) Deutscher Wetterdienst, Presse- und Öffentlichkeitsarbeit. Deutschlandwetter im Winter 2009/2010. http://www.dwd.de/bvbw/generator/DWDWWW/Content/Presse/Pressemitteilungen/2010/20100226__Deutschlandwetter__Winter__2009__2010,templateId=raw,property=publicationFile.pdf/20100226_Deutschlandwetter_Winter_2009_2010.pdf. Accessed 7 June 2010
Eyre BD, Rysgaard S, Dalsgard T, Christensen PB (2002) Comparison of Isotope Pairing and N2:Ar methods for measuring sediment denitrification: assumptions, modifications, and implications. Estuaries 25:1077–1087
Gao H, Schreiber F, Collins G, Jensen MM, Kostka JE, Lavik G, de Beer D, Zhou H, Kuypers MMM (2010) Aerobic denitrification in permeable Wadden Sea sediments. ISME J 4(3):417–426
Gardner WS, McCarthy MJ (2009) Nitrogen dynamics at the sediment-interface in shallow, sub-tropical Florida Bay: why denitrification efficiency may decrease with increased eutrophication. Biogeochemistry 95:185–198
Gardner WS, Seitzinger SP, Malczyk JM (1991) The effects of sea salts on the forms of nitrogen released from estuarine and freshwater sediments: does ion pairing affect ammonium flux? Estuaries 14:157–166
Giblin AE, Weston NB, Banta GT, Tucker J, Hopkinson CS (2010) The effects of salinity on nitrogen losses from an oligohaline estuarine sediment. Estuar Coast 33:1054–1068
Gihring TM, Canion A, Riggs A, Huettel M, Kostka JE (2010) Denitrification in shallow, sublittoral Gulf of Mexico permeable sediments. Limnol Oceanogr 55:43–54
Golterman HL (2004) The chemistry of phosphate and nitrogen compounds in sediments. Kluwer Academic Publishers, Dordrecht
Grasshoff K, Ehrhardt M, Kremling K (1983) Methods of seawater analysis. Verlag Chemie, Weinheim
Huettel M, Roy H, Precht E, Ehrenhauss S (2003) Hydrodynamical impact on biogeochemical processes in aquatic sediments. Hydrobiol 494:231–236
Hydes DJ, Kelly-Gerreyn BA, Le Gall AC, Proctor R (1999) The balance of supply of nutrients and demands of biological production and denitrification in a temperate latitude shelf sea–a treatment of the southern North Sea as an extended estuary. Mar Chem 68:117–131
Jensen KM, Jensen MH, Kristensen E (1996) Nitrification and denitrification in Wadden Sea sediments (Königshafen, Island of Sylt, Germany) as measured by nitrogen isotope pairing and isotope dilution. Aquat Microb Ecol 11:181–191
Kana TM, Darkangelo C, Hunt MD, Oldham JB, Bennett GE, Cornwell JC (1994) Membrane inlet mass spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples. Anal Chem 66:4166–4170
Kieskamp WM, Lohse L, Epping E, Helder W (1991) Seasonal variation of denitrification rates and nitrous oxide fluxes in intertidal sediments of the western Wadden Sea. Mar Ecol-Prog Ser 72:145–151
Koch MS, Maltby E, Oliver GA, Bakker SA (1992) Factors controlling denitrification rates of tidal mudflats and fringing salt marshes in south-west England. Estuar Coast Shelf S 34:471–485
Köster R (1998) Wattsedimente. In: Umweltatlas Wattenmeer, Bd I: Nordfriesisches und Dithmarscher Wattenmeer. Ulmer-Verlag, Stuttgart, pp 40–41
Lavrentyev PJ, Gardner WS, Yang L (2000) Effects of the zebra mussel on nitrogen dynamics and the microbial community at the sediment–water interface. Aquat Microb Ecol 21:187–194
Law CS, Owens NJP (1992) Denitrification and nitrous oxide in the North Sea. Neth J Sea Res 25:65–74
Lohse L, Malschaert JFP, Slomp CP, Helder W, van Raaphorst W (1993) Nitrogen cycling in North Sea sediments: interaction of denitrification and nitrification in offshore and coastal areas. Mar Ecol-Prog Ser 101:283–296
Lohse L, Kloosterhuis R, van Raaphorst W, Helder W (1996) Denitrification rates in continental shelf sediments of the North Sea: acetylene block technique versus isotope pairing. Mar Ecol-Prog Ser 132:169–179
McCarthy MJ, Gardner WS (2003) An application of membrane inlet mass spectrometry to measure denitrification in a recirculating mariculture system. Aquaculture 218:341–355
Middelburg JJ, Soetaert K (2004) The role of sediments in shelf ecosystem dynamics. In: Robinson AR, McCarthy J, Rothschild, BJ (eds) The Sea,vol 13, pp 353–373
Middelburg JJ, Soetaert K, Herman PMJ, Heip C (1996) Denitrification in marine sediments: a model study. Global Biogeochem Cy 10:661–673
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36
Nedwell DB (1982) Exchange of nitrate, and the products of bacterial nitrate reduction, between seawater and sediment from a U.K. saltmarsh. Estuar Coast Shelf S 14:557–566
Nielsen LP (1992) Denitrification in sediment determined from nitrogen isotope pairing. FEMS Microbiol Lett 86:357–362
Nixon SW, Atkinson LP, Berounsky VM, Billén G, Boicourt WC, Boynton WR, Church TM, Ditoro DM, Elmgren R, Garber JH, Giblin AE, Jahnke RA, Owens NJP, Pilson MEQ, Seitzinger SP (1996) The fate of nitrogen and phosphorus at the land-sea margin of the North Atlantic Ocean. Biogeochemistry 35:141–180
Owens NJP, Woodward EMS, Aiken J, Bellan IE, Rees AP (1990) Primary production and nitrogen assimilation in the North Sea during July 1987. Neth J Sea Res 25:143–154
Pätsch J, Serna A, Dähnke K, Schlarbaum T, Johannsen A, Emeis K (2010) Nitrogen cycling in the German Bight (SE North Sea): clues from modelling stable nitrogen isotopes. Cont Shelf Res 30:203–213
Pettijohn FJ, Potter PE (1972) Sand and sandstone. Springer, New York
Piña-Ochoa E, Álvarez-Cobelas M (2006) Denitrification in aquatic environments: a cross-system analysis. Biogeochemistry 81:111–130
Radach G, Pätsch L (2007) Variability of continental riverine freshwater and nutrient inputs into the North Sea for the years 1977–2000 and its consequences for the assessment of eutrophication. Est and Coasts 30:66–81
Rao AMF, McCarthy MJ, Gardner WS, Jahnke A (2007) Respiration and denitrification in permeable continental shelf deposits on the South Atlantic bight: rates of carbon and nitrogen cycling from sediment column experiments. Cont Shelf Res 27:1801–1819
Rao AMF, McCarthy MJ, Gardner WS, Jahnke A (2008) Respiration and denitrification in permeable continental shelf deposits on the South Atlantic bight:N2:Ar and isotope pairing measurements in sediment column experiments. Cont Shelf Res 28:602–613
Risgaard Petersen NLP, Nielsen S, Rysgaard DT, Meyer RL (2003) Application of the isotope pairing technique in sediments where anammox and denitrification coexist. Limnol Oceanogr: Methods 1:63–73
Scott JT, McCarthy MJ, Gardner WS, Doyle RD (2008) Denitrification, dissimilatory nitrate reduction to ammonium, and nitrogen fixation along a nitrate concentration gradient in a created freshwater wetland. Biogeochemistry 87:11–99
Seitzinger SP (1988) Denitrification in freshwater and coastal marine ecosystems: Ecological and geochemical significance. Limnol Oceanogr 33:702–724
Seitzinger S, Nixon SW (1985) Eutrophication and the rate of denitrification and N2O production in coastal marine sediments. Limnol Oceanogr 30:1332–1339
Sørensen J (1978) Denitrification rates in a marine sediment as measured by the acetylene inhibition technique. Appl Environ Microbiol 36:139–143
Sørensen J, Jørgensen BB, Revsbech NP (1979) A comparison of oxygen, nitrate and sulfate respiration in coastal marine sediments. Mar Ecol 5:105–115
Steingruber SM, Friedrich J, Gächter R, Wehrli B (2001) Measurement of denitrification with the 15N isotope pairing technique. Appl Env Microbiol 9:3771–3778
Sundbäck K, Miles A, Göransson E (2000) Nitrogen fluxes, denitrification and the role of micro-phytobenthos in microtidal shallow-water sediments: an annual study. Mar Ecol-Prog Ser 200:59–76
Sweerts JP, Bär-Gilissen MJ, Cornelese AA, Cappenberg TE (1991) Oxygen-consuming processes at the profundal and littoral sediment-water interface of a small meso-eutrophic lake (Lake Vechten, The Netherlands). Limnol Oceanogr 36:1124–1133
Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microb 68:1312–1318
Tiedje JM (1987) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder AJB (ed) Biology of anaerobic microorganims. Wiley, New York, pp 179–244
Trimmer M, Nicholls JC (2009) Production of nitrogen gas via anammox and denitrification in intact sediment cores along a continental shelf to slope transect in the North Atlantic. Limnol Oceanogr 54:577–589
van Beusekom JEE, de Jonge VN (2002) Long-term changes in Wadden Sea nutrient cycles: importance of organic matter import from the North Sea. Hydrobiologia 475(476):185–194
van Beusekom JEE, van de Jonge VN (1998) Retention of phosphorus and nitrogen in the Ems Estuary. Estuaries 21:527–539
van Beusekom JEE, Brockmann UH, Hesse KJ, Hickel W, Poremba K, Tillmann U (1999) The importance of sediments in the transformation and turnover of nutrients and organic matter in the Wadden Sea and German Bight. Ger J Hydrography 51:245–266
van Beusekom JEE, Fock H, de Jong F, Diel-Christiansen S, Christiansen B (2001) Wadden Sea specific eutrophication criteria. Wadden Sea Ecosystem 14:1–115
van Beusekom JEE, Loebl M, Martens P (2009) Distant riverine nutrient supply and local temperature drive the long-term phytoplankton development in a temperate coastal basin. J Sea Res 61:26–33
van Luijn F, Boers CM, Lijklema L, Sweerts JPRA (1999) Nitrogen fluxes and processes in sandy and muddy sediments from a shallow eutrophic lake. Water Res 33:33–42
van Raaphorst W, Kloosterhuis HT, Cramer A, Bakker KJM (1990) Nutrient early diagenesis in the sediments of the Dogger Bank area, North Sea: pore water results. Neth J Sea Res 26:25–52
van Raaphorst W, Kloosterhuis HT, Berghuis EM, Gieles AJM, Malschaert JFP, van Noort GJ (1992) Nitrogen cycling in two types of sediments of the Southern North Sea (Frisian Front, Broadfourteens): field data and mesocosm results. Neth J Sea Res 28:293–316
Weiss RF (1970) The solubility of nitrogen, oxygen and argon in water and seawater. Deep Sea Res Oceanographic Abstracts 17:721–735
Wentworth CK (1922) A scale of grade and class terms for clastic sediments. J Geo 30(5):377–392
Acknowledgments
We thank the Helmholtz-Zentrum Geesthacht, Institute for Coastal Research and the DFG (Em 37/29) for financial support. In particular, we thank W.S. Gardner and M.J. McCarthy (Marine Science Institute, University of Texas at Austin) for their helpful introduction to sediment incubation. We acknowledge N. Lahajnar and F. Langenberg (IfBM, University of Hamburg) for supervising work on the data set of sediment characteristics. We thank the FTZ Westküste, Büsum and the AWI, List for providing laboratory space and our technician M. Ankele for assistance during field trips. A. Wieland is acknowledged for an introduction into oxygen profiling, corrections and helpful comments on an earlier draft.
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Deek, A., Emeis, K. & van Beusekom, J. Nitrogen removal in coastal sediments of the German Wadden Sea. Biogeochemistry 108, 467–483 (2012). https://doi.org/10.1007/s10533-011-9611-1
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DOI: https://doi.org/10.1007/s10533-011-9611-1