Skip to main content

Advertisement

SpringerLink
Log in

Nitrogen cycling in a freshwater estuary

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Freshwater estuaries may be important control points but have received limited research attention, emblematic of a general under-appreciation of these ecosystems and the services they provide. These ecotone environments exist at the interface of rivers flowing into large lakes, where seiches cause mixing of lotic and lentic waters within flooded river deltas. We assessed the dissolved inorganic nitrogen (DIN) retention and processing controls in the Saint Louis River Estuary (SLRE), which receives inputs from rivers, urban sources, and Lake Superior. Nitrate (NO3–N) was the dominant form of DIN and was consistently highest in the lower estuary due to seiche-delivered Lake Superior water and nitrification of ammonium from urban sources. The estuary transitioned from a net NO3–N source during high flows to a net sink during summer baseflow conditions. NO3–N availability controlled site-specific denitrification rates while sediment organic matter explained the spatial pattern in denitrification potential. As the estuary shifted from a riverine state to one with more lake influence, seiches delivered Lake Superior NO3–N to the lower portion of the estuary, alleviating the final denitrification control and activating the estuary’s ‘denitrification pump’. This amplified removal condition is maintained by critically delivered NO3–N during periods of warm temperatures and long residence times. Often these controls are unsynchronized in streams where NO3–N is typically lowest during summer baseflow. Similar ephemeral biogeochemical processes are likely found within other seiche-prone lakes where organic-rich sediments accumulate at river mouths and are supplied with chemically distinct lake water during low flow periods.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Barnes RT, Raymond PA (2010) Land-use controls on sources and processing of nitrate in small watersheds: insights from dual isotopic analysis. Ecol Appl 20:1961–1978

    Article  Google Scholar 

  • Baron JS, Hall EK, Nolan BT, Finlay JC, Bernhardt ES, Harrison JA, Chan F, Boyer EW (2012) The interactive effects of excess reactive nitrogen and climate change on aquatic ecosystems and water resources of the United States. Biogeochemistry 114:71–92

    Article  Google Scholar 

  • Beletsky D, Saylor JH, Schwab DJ (1999) Mean circulation in the Great Lakes. J Great Lakes Res 25:78–93

    Article  Google Scholar 

  • Bellinger BJ, Jicha TM, Lehto LP, Seifert-Monson LR, Bolgrien DW, Starry MA, Angradi TR, Pearson MS, Elonen C, Hill BH (2014) Sediment nitrification and denitrification in a Lake Superior estuary. J Great Lakes Res 40:392–403

    Article  Google Scholar 

  • Bonaglia S, Deutsch B, Bartoli M, Marchant HK, Brüchert V (2014) Seasonal oxygen, nitrogen and phosphorus in benthic cycling along an impacted Baltic Sea estuary: regulation and spatial patterns. Biogeochemistry 119:139–160

    Article  Google Scholar 

  • Bouchard V (2007) Export of organic matter from a coastal freshwater wetland to Lake Erie: an extension of the outwelling hypothesis. Aquat Ecol 41:1–17

    Article  Google Scholar 

  • Burgin AJ, Hamilton SK (2007) Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front Ecol Environ 5:89–96

    Article  Google Scholar 

  • Carpenter SR (2008) Phosphorus control is critical to mitigating eutrophication. Proc Natl Acad Sci 105:11039–11040

    Article  Google Scholar 

  • Czuba CR, Fallon JD, Kessler EW (2012) Floods of June 2012 in northeastern Minnesota: U.S. Geological Survey Scientific Investigations Report 2012–5283

  • Einarsson E, Lowe B (1968) Seiches and set-up on Lake Winnipeg. Limnol Oceanogr 13:257–271

    Article  Google Scholar 

  • Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Let 10:1135–1142

    Article  Google Scholar 

  • Enoksson V (1993) Nutrient recycling by coastal sediments: effects of added algal material. Mar Ecol Prog Ser 92:245–254

    Article  Google Scholar 

  • Erisman JW, Galloway JN, Seitzinger S, Bleeker A, Dise NB, Petrescu AMR, Leach AM, de Vries W (2013) Consequences of human modification of the global nitrogen cycle. Phil Trans R Soc B 368:20130116

    Article  Google Scholar 

  • Finlay JC, Sterner RW, Kumar S (2007) Isotopic evidence for in-lake production of accumulating nitrate in Lake Superior. Ecol Appl 17:2323–2332

    Article  Google Scholar 

  • Finlay JC, Small GE, Sterner RW (2013) Human influences on nitrogen removal in lakes. Science 342:247–250

    Article  Google Scholar 

  • Fitzpatrick ML, Long DT, Pijanowski BC (2007) Exploring the effects of urban and agricultural land use on surface water chemistry, across a regional watershed, using multivariate statistics. Appl Geochem 22:1825–1840

    Article  Google Scholar 

  • Forshay KJ, Stanley EH (2005) Rapid nitrate loss and denitrification in a temperate river floodplain. Biogeochemistry 75:43–64

    Article  Google Scholar 

  • Foster SQ, Fulweiler RW (2014) Spatial and historic variability of benthic nitrogen cycling in an anthropogenically impacted estuary. Front Mar Sci 1:1–16

    Article  Google Scholar 

  • Fulweiler RW, Heiss EM (2014) A decade of directly measured sediment N2 fluxes: what can Narragansett Bay tell us about the global ocean nitrogen budget? Oceanography 27:184–195

    Article  Google Scholar 

  • Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vorosmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226

    Article  Google Scholar 

  • Gardner JT, English M, Prowse TD (2006) Wind-forced seiche events on Great Slave Lake: hydrologic implications for the Slave River Delta, NWT, Canada. Hydrol Process 20:4051–4072

    Article  Google Scholar 

  • Garnier J, Cébron A, Tallec G, Billen G, Sebilo M, Martinez A (2006) Nitrogen behaviour and nitrous oxide emission in the tidal Seine river estuary (France) as influenced by human activities in the upstream watershed. Biogeochemistry 77:305–326

    Article  Google Scholar 

  • Giblin AE, Tobias CR, Song B, Weston N, Banta GT, Rivera-Monroy VH (2013) The importance of dissimilatory nitrate reduction to ammonium (DNRA) in the nitrogen cycle of coastal ecosystems. Oceanography 26:124–131

    Article  Google Scholar 

  • Groffman PM, Holland EA, Myrold DD, Robertson GP, Zou X (1999) Denitirification. In: Robertson GP, Bledsoe CS, Coleman DC, Sollins P (eds) Standand soil methods long-term ecological research. Oxford University, New York, pp 272–288

    Google Scholar 

  • Groffman PM, Altabet MA, Böhlke JK, Butterbach-Bahl K, David MB, Firestone MK, Giblin AE, Kana TM, Nielsen LP, Voytek MA (2006) Methods for measuring denitrification: diverse approaches to a difficult problem. Ecol Appl 16:2091–2122

    Article  Google Scholar 

  • Herdendorf CE (1990) Great Lakes estuaries. Estuaries 13:493–503

    Article  Google Scholar 

  • Hill AR (1993) Base cation chemistry of storm runoff in a forested headwater wetland. Water Resour Res 29:2663–2673

    Article  Google Scholar 

  • Hoellein TJ, Bruesewitz DA, Richardson DC (2013) Revisiting Odum (1956): a synthesis of aquatic ecosystem metabolism. Limnol Oceanogr 58:2089–2100

    Article  Google Scholar 

  • Hoffman JC, Peterson GS, Cotter AM, Kelly JR (2010) Using stable isotope mixing in a Great Lakes coastal tributary to determine food web linkages in young fishes. Estuar Coasts 33:1391–1405

    Article  Google Scholar 

  • Howarth R, Swaney D, Billen G, Garnier J, Hong B, Humborg C, Johnes P, Mörth C-M, Marino R (2012) Nitrogen fluxes from the landscape are controlled by net anthropogenic nitrogen inputs and by climate. Front Ecol Environ 10:37–43

    Article  Google Scholar 

  • Johnston CA, Bridgham SD, Schubauer-Berigan JP (2001) Nutrient dynamics in relation to geomorphology of riverine wetlands. Soil Sci Am J 65:557–577

    Article  Google Scholar 

  • Kabeya N, Kubota T, Shimizu A, Nobuhiro T, Tsuboyama Y, Chann S, Tith N (2008) Isotopic investigation of river water mixing around the confluence of the Tonle Sap and Mekong rivers. Hydrol Process 22:1351–1358

    Article  Google Scholar 

  • Knuth ML, Kelly JR (2011) Denitrification rates in a Lake Superior coastal wetland. Aquat Ecosyst Health Manag 14:414–421

    Article  Google Scholar 

  • Koop-Jakobsen K, Giblin AE (2010) The effect of increased nitrate loading on nitrate reduction via denitrification and DNRA in salt marsh sediments. Limnol Oceanogr 55:789–802

    Article  Google Scholar 

  • Kumar S, Sterner RW, Finlay JC, Brovold S (2007) Spatial and temporal variation of ammonium in Lake Superior. J Great Lakes Res 33:581–591

    Article  Google Scholar 

  • Larson JH, Trebitz AS, Steinman AD, Wiley MJ, Mazur MC, Pebbles V, Braun HA, Seelbach PW (2012) Great Lakes rivermouth ecosystems: scientific synthesis and management implications. J Great Lakes Res 39:513–524

    Article  Google Scholar 

  • Lewis WM, Wurtsbaugh WA, Paerl HW (2011) Rationale for control of anthropogenic nitrogen and phosphorus to reduce eutrophication of inland waters. Environ Sci Technol 45:10300–10305

    Article  Google Scholar 

  • Loken LC (2014) Hydrologic and biotic controls of nitrogen cycling in a Lake Superior freshwater estuary. MS Thesis, University of Wisconsin, Madison

  • McCarthy MJ, Gardner WS, Lavrentyev PJ, Moats KM, Frank J, Klarer DM (2007) Effects of hydrological flow regime on sediment-water interface and water column nitrogen dynamics in a Great Lakes coastal wetland (Old Woman Creek, Lake Erie). J Great Lakes Res 33:219–231

    Article  Google Scholar 

  • Meyers PA, Teranes JL (2001) Sediment organic matter. In: Last WM, Smol JP (eds) Tracking environmental change using lake sediments, vol 2., Physical and geochemical methods. Kluwer, Dordrecht, pp 239–269

    Chapter  Google Scholar 

  • Middelburg JJ, Nieuwenhuize J (2001) Nitrogen isotope tracing of dissolved inorganic nitrogen behaviour in tidal estuaries. Estuar Coast Shelf Sci 53:385–391

    Article  Google Scholar 

  • Morrice JA, Kelly JR, Trebitz AS, Cotter AM, Knuth ML (2004) Temporal dynamics of nutrients (N and P) and hydrology in a Lake Superior coastal wetland. J Great Lakes Res 30:82–96

    Article  Google Scholar 

  • Morrice JA, Trebitz AS, Kelly JR, Sierszen ME, Cotter AM, Hollenhorst T (2011) Determining sources of water to Great Lakes coastal wetlands: a classification approach. Wetlands 31:1199–1213

    Article  Google Scholar 

  • Mortimer CH, Fee EJ (1976) Free surface oscillations and tides of Lakes Michigan and Superior. Philos Trans R Soc Lond B 281:1–61

    Article  Google Scholar 

  • Mulholland PJ, Tank JL, Sanzone DM, Wollheim WM, Peterson BJ, Webster JR, Meyer JL (2000) Nitrogen cycling in a forest stream determined by a 15N tracer addition. Ecol Monogr 70:471–493

    Google Scholar 

  • Nixon SW (1981) Remineralization and nutrient cycling in coastal marine sediments. In: Nielsen B, Cronin L (eds) Estuaries and nutrients. Humana Press, New Jersey, pp 111–138

    Chapter  Google Scholar 

  • Nixon SW, Ammerman JW, Atkinson LP, Berounsky VM, Billen G, Voicourt 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

    Article  Google Scholar 

  • Ohte N, Sebestyen SD, Kendall C, Shanley JB, Wankel SD, Doctor DH, Boyer EW (2004) Tracing sources of nitrate in snowmelt runoff using a high-resolution isotopic technique. Geophys Res Lett 31:L21506. doi:10.1029/2004GL020908

    Article  Google Scholar 

  • Pattinson SN, Garcia-Ruiz R, Whitton BA (1998) Spatial and seasonal variation in denitrification in the Swale-Ouse system, a river continuum. Sci Total Environ 210:289–305

    Article  Google Scholar 

  • Pellerin BA, Saraceno JF, Shanley JB, Sebestyen SD, Aiken GR, Wollheim WM, Bergamaschi BA (2012) Taking the pulse of snowmelt: in situ sensors reveal seasonal, event and diurnal patterns of nitrate and dissolved organic matter variability in an upland forest stream. Biogeochemistry 108:183–198

    Article  Google Scholar 

  • Peterson BJ, Wollheim WM, Mulholland PJ, Webster JR, Meyer JL, Tank JL, Martí E, Bowden WB, Valett HM, Hershey AE, McDowell WH, Dobbs WK, Hamilton SK, Gregory S, Morrall DD (2001) Control of nitrogen export from watersheds by headwater streams. Science 292:86–90

    Article  Google Scholar 

  • Philips EJ, Cichra M, Aldridge FJ, Jembeck J, Hendrickson J, Brody R (2000) Light availability and variations in phytoplankton standing crops in a nutrient-rich blackwater river. Limnol Oceanogr 45:916–929

    Article  Google Scholar 

  • Piña-Ochoa E, Álvarez-Cobelas M (2006) Denitrification in aquatic environments: a cross-system analysis. Biogeochemistry 81:111–130

    Article  Google Scholar 

  • Richardson WB, Strauss EA, Bartsch LA, Monroe EM, Cavanaugh JC, Vingum L, Soballe DM (2004) Denitrification in the Upper Mississippi River: rates, controls, and contribution to nitrate flux. Can J Fish Aquat Sci 61:1102–1112

    Article  Google Scholar 

  • Roach WJ, Grimm NB (2011) Denitrification mitigates N flux through the stream–floodplain complex of a desert city. Ecol Appl 21:2618–2636

    Article  Google Scholar 

  • Saint Louis River Alliance (2013) Saint Louis River Aliance. http://stlouisriver.org/. Accessed 9 March, 2013

  • Schindler DW, Hecky RE, Findlay DL, Stainton MP, Parker BR, Paterson MJ, Beaty KG, Lyng M, Kasian SEM (2008) Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37-year whole-ecosystem experiment. Proc Natl Acad Sci 105:11254–11258

    Article  Google Scholar 

  • Seitzinger SP, Nielsen LP, Caffrey J, Christensen PB (1993) Denitrification measurements in aquatic sediments: a comparison of three methods. Biogeochemistry 23:147–167

    Article  Google Scholar 

  • Seitzinger SP, Harrison JA, Böhlke JK, Bouwman AF, Lowrance R, Peterson B, Tobias C, Van Drecht G (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16:2064–2090

    Article  Google Scholar 

  • Sierszen ME, Morrice JA, Trebitz AS, Hoffman JC (2012) A review of selected ecosystem services provided by coastal wetlands of the Laurentian Great Lakes. Aquat Ecosyst Health Manag 15:92–106

    Article  Google Scholar 

  • Small GE, Bullerjahn GS, Sterner RW, Beall BFN, Brovold S, Finlay JC, McKay RML, Mukherjee M (2013) Rates and controls of nitrification in a large oligotrophic lake. Limnol Oceanogr 58:276–286

    Article  Google Scholar 

  • Smith MS, Tiedje JM (1979) Phases of denitrification following oxygen depletion in soil. Soil Biol Biochem 11:261–267

    Article  Google Scholar 

  • Smyth AR, Thompson SP, Siporin KN, Gardner WS, McCarthy MJ, Piehler MF (2013) Assessing nitrogen dynamics throughout the estuarine landscape. Estuar Coasts 36:44–55

    Article  Google Scholar 

  • Sorensen J, Sydor M, Huls H, Costello M (2004) Analyses of Lake Superior seiche activity for estimating effects on pollution transport in the St. Louis River Estuary under extreme conditions. J Great Lakes Res 30:293–300

    Article  Google Scholar 

  • Spokas K, Wang D, Venterea R (2005) Greenhouse gas production and emission from a forest nursery soil following fumigation with chloropicrin and methyl isothiocyanate. Soil Biol Biochem 37:475–485

    Article  Google Scholar 

  • Stanley EH, Ward AK (1997) Inorganic nitrogen regimes in an Alabama wetland. J North Am Benthol Soc 16:820–832

    Article  Google Scholar 

  • Stephens BM, Minor EC (2010) DOM characteristics along the continuum from river to receiving basin: a comparison of freshwater and saline transects. Aquat Sci 72:403–417

    Article  Google Scholar 

  • Sterner RW, Anagnostou E, Brovold S, Bullerjahn GS, Finlay JC, Kumar S, McKay RML, Sherrell RM (2007) Increasing stoichiometric imbalance in North America’s largest lake: nitrification in Lake Superior. Geophys Res Lett 34:L10406. doi:10.1029/2006GL028861

    Article  Google Scholar 

  • Tomazek JA, Gardner WS, Johengen TH (1997) Denitrification in sediments of a Lake Erie coastal wetland (Old Woman Creek, Huron, Ohio, USA). J Great Lakes Res 23:403–415

    Article  Google Scholar 

  • Trebitz AS (2006) Characterizing seiche and tide-driven daily water level fluctuations affecting coastal ecosystems of the Great Lakes. J Great Lakes Res 32:102–116

    Article  Google Scholar 

  • Trebitz AS, Morrice JA, Cotter AM (2002) Relative role of lake and tributary in hydrology of Lake Superior coastal wetlands. J Great Lakes Res 28:212–227

    Article  Google Scholar 

  • Verbanck M, Vanderborght J-P, Wallast R (1989) Major ion content of urban wastewater: assessment of per capita loading. Res J Water Pollut Control Fed 61:1722–1728

    Google Scholar 

  • Wall LG, Tank JL, Royer TV, Bernot MJ (2005) Spatial and temporal variability in sediment denitrification within an agriculturally influenced reservoir. Biogeochemistry 76:85–111

    Article  Google Scholar 

  • Wankel SD, Kendall C, Paytan A (2009) Using nitrate dual isotopic composition (δ15N and δ18O) as a tool for exploring sources and cycling of nitrate in an estuarine system: Elkhorn Slough, California. J Geophys Res 114:G01011. doi:10.1029/2008JG000729

    Google Scholar 

  • Wollheim WM, Stewart RJ, Aiken GR, Butler KD, Morse NB, Salisbury J (2015) Removal of terrestrial DOC in aquatic ecosystems of a temperate river network. Geophys Res Lett 42:6671–6679

    Article  Google Scholar 

Download references

Acknowledgments

We thank everyone (especially Shon Schooler, Tracey Ledder, and Kim Duernberger) at the Lake Superior National Estuary Research Reserve (LSNERR) for providing logistical support. Thanks to Ryan Hassemer, Nolan Klein, Lauren Reuss, Isaac Bergstrom and others for field and lab work. Thanks to Liz Runde and NTL-LTER (DEB-0822700) at University of Wisconsin and Sandy Brovold at the University of Minnesota-Twin Cities for lab analysis. Thanks to Joe Mayasich at the Western Lake Superior Sanitary District for providing data. Thanks to John Crawford, Nora Casson, Anett Trebitz, and two anonymous reviewers for comments on earlier drafts. This work is the result of research sponsored by the Minnesota and Wisconsin Sea Grant College Programs supported by the NOAA office of Sea Grant, United States Department of Commerce, under Grant No. NA10OAR4170069. The U.S. Government is authorized to reproduce and distribute reprints for government purposes, notwithstanding any copyright notation that may appear hereon. This paper is journal reprint No. JR628 of the Minnesota Sea Grant College Program. Additional support was provided to LC Loken by the University of Wisconsin-Madison—Anna Grant Birge Award.

Author information

Author notes

  1. Robert W. Sterner

    Present address: Large Lakes Observatory, University of Minnesota-Duluth, 2205 E 5th St., Duluth, MN, 55812, USA

Authors and Affiliations

  1. Center for Limnology, University of Wisconsin-Madison, 680 N Park. St., Madison, WI, 53706, USA

    Luke C. Loken & Emily H. Stanley

  2. Department of Biology, University of St. Thomas, 2115 Summit Ave., St. Paul, MN, 55105, USA

    Gaston E. Small

  3. Department of Ecology, Evolution, and Behavior, University of Minnesota-Twin Cities, 1987 Upper Buford Circle, St. Paul, MN, 55108, USA

    Jacques C. Finlay & Robert W. Sterner

Authors
  1. Luke C. Loken
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gaston E. Small
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jacques C. Finlay
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert W. Sterner
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Emily H. Stanley
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luke C. Loken.

Additional information

Responsible Editor: Maren Voss.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Loken, L.C., Small, G.E., Finlay, J.C. et al. Nitrogen cycling in a freshwater estuary. Biogeochemistry 127, 199–216 (2016). https://doi.org/10.1007/s10533-015-0175-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-015-0175-3

Keywords

Search

Navigation