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Seasonal dynamics and bioavailability of dissolved organic matter in two contrasting temperate estuaries

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Abstract

Production and bioavailability of dissolved organic matter (DOM) were followed during a year in the nutrient-rich estuary, Roskilde Fjord (RF), and the more oligotrophic strait, Great Belt (GB), in Denmark. Bioavailability of dissolved organic carbon (DOC), nitrogen (DON), and phosphorous (DOP) was determined during incubations over six months. Overall, RF had three to five times larger pools of total nitrogen (TN) and total phosphorous (TP) and five to eight times higher concentrations of inorganic nutrients compared to GB. However, the allocation of carbon, nitrogen, and phosphorous into different pools were remarkably similar between the two systems. DON and DOP contributed with about equal relative fractions in the two systems: 72 ± 13% of total nitrogen and 21 ± 12% of total phosphorous. The average bioavailability of DOM was 25 ± 15, 17 ± 5.5, and 49 ± 29% for carbon, nitrogen, and phosphorous, respectively. The observed release of DIN from degradation of DON amounted to between 0.1 (RF winter) and 14 times (GB summer) the loadings from land and contributed with half of the total input of bioavailable nitrogen during summer. Hence, this study shows that nitrogen in DOM is important for the nitrogen cycling, especially during summer. The sum of inorganic nutrients, particulate organic matter, and bioavailable DOM (the dynamic pools of nutrients) accounted for 42 and 92% of nitrogen, and phosphorous, respectively, and was remarkably similar between the two systems compared to the difference in nutrient richness. It is hypothesized that the pelagic metabolism of nutrients in marine systems dictates a rather uniform distribution of the different fractions of nitrogen and phosphorous containing compounds regardless of eutrophication level.

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References

  • Amon RMW, Fitznar HP, Benner R (2001) Linkages among the bioreactivity, chemical composition, and diagenetic state of marine dissolved organic matter. Limnol Oceanogr 46:287–297

    Article  Google Scholar 

  • Andersen JH, Carstensen J, Conley DJ, Dromph K, Fleming-Lehtinen V, Gustafsson BG, Josefson AB, Norkko A, Villnäs A, Murray C (2015) Long-term temporal and spatial trends in eutrophication status of the Baltic Sea. Biol Rev. doi:10.1111/brv.12221

    Google Scholar 

  • Asmala E, Stedmon CA, Thomas DN (2012) Linking CDOM spectral absorption to dissolved organic carbon concentrations and loadings in boreal estuaries. Estuar Coast Shelf Sci 111:107–117

    Article  Google Scholar 

  • Bendtsen J, Gustafsson KE, Soederkvist J, Hansen JLS (2009) Ventilation of bottom water in the North Sea-Baltic Sea transition zone. J Mar Syst 75:138–149

    Article  Google Scholar 

  • Bentzon-Tilia M, Traving SJ, Mantikci M, Knudsen-Leerbeck H, Hansen JLS, Markager S, Riemann L (2015) Significant N2 fixation by heterotrophs, photoheterotrophs and heterocystous cyanobacteria in two temperate estuaries. ISME J 9:273–285

    Article  Google Scholar 

  • Berman T (2001) The role of DON and the effect of N:P ratios on occurrence of cyanobacterial blooms: Implications from the outgrowth of Aphanizomenon in Lake Kinneret. Limnol Oceanogr 46:443–447

    Article  Google Scholar 

  • Berman T, Bronk DA (2003) Dissolved organic nitrogen: a dynamic participant in aquatic ecosystems. Aquat Microb Ecol 31:279–305

    Article  Google Scholar 

  • Bronk DA (2002) Dynamics of DON. In: Hansell DA, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic Press, Cambridge, pp 153–247

    Chapter  Google Scholar 

  • Bronk DA, Glibert PM, Ward BB (1994) Nitrogen uptake, dissolved organic nitrogen release, and new production. Science 265:1843–1846

    Article  Google Scholar 

  • Bronk DA, Glibert PM, Malone TC, Banahan S, Sahlsten E (1998) Inorganic and organic nitrogen cycling in Chesapeake Bay: autotrophic versus heterotrophic processes and relationships to carbon flux. Aquat Microb Ecol 15:177–189

    Article  Google Scholar 

  • Bronk DA, See JH, Bradley P, Killberg L (2007) DON as a source of bioavailable nitrogen for phytoplankton. Biogeosciences 4:283–296

    Article  Google Scholar 

  • Bronk DA, Killberg-Thoreson L, Sipler RE, Mulholland MR, Roberts QN, Bernhardt PW, Garrett M, O’Neil JM, Heil CA (2014) Nitrogen uptake and regeneration (ammonium regeneration, nitrification and photoproduction) in waters of the West Florida Shelf prone to blooms of Karenia brevis. Harmful Algae 38:50–62

    Article  Google Scholar 

  • Bushaw KL, Zepp RG, Tarr MA, SchulzJander D, Bourbonniere RA, Hodson RE, Miller WL, Bronk DA, Moran MA (1996) Photochemical release of biologically available nitrogen from aquatic dissolved organic matter. Nature 381:404–407

    Article  Google Scholar 

  • Carlson CA (2002) Production and removal processes. In: Dennis AH, Craig AC (eds) Biogeochemistry of marine dissolved organic matter. Academic Press, Cambridge, pp 91–139

    Chapter  Google Scholar 

  • Carstensen J, Henriksen P (2009) Phytoplankton biomass response to nitrogen inputs: a method for WFD boundary setting applied to Danish coastal waters. Hydrobiologia 633:137–149

    Article  Google Scholar 

  • Carstensen J, Conley DJ, Andersen JH, Ærtebjerg G (2006) Coastal eutrophication and trend reversal: a Danish case study. Limnol Oceanogr 51:398–408

    Article  Google Scholar 

  • Cauwet G (1999) Determination of dissolved organic carbon and nitrogen by high temperature combustion. In: Grasshof K, Kremling K, Ehrhard M (eds) Methods of seawater analysis. Wiley, Weinheim, pp 407–420

    Chapter  Google Scholar 

  • Cloern JE (2001) Our evolving conceptual model of the coastal eutrophication problem. Mar Ecol Prog Ser 210:223–253

    Article  Google Scholar 

  • Conley DJ, Kaas H, Mohlenberg F, Rasmussen B, Windolf J (2000) Characteristics of Danish estuaries. Estuaries 23:820–837

    Article  Google Scholar 

  • Davis J, Benner R (2005) Seasonal trends in the abundance, composition and bioavailability of particulate and dissolved organic matter in the Chukchi/Beaufort Seas and western Canada Basin. Deep-Sea Res II 52:3396–3410

    Article  Google Scholar 

  • Ellermann T, Andersen HV, Bossi R, Christensen JH, Lofstrom P, Monies C, Grundahl L, Geels C (2013) Atmosfærisk deposition 2012 NOVANA. Scientific report no. 73, Aarhus University, Aarhus, Denmark, p 85. http://dce2.au.dk/pub/SR73.pdf

  • Fajon C, Cauwet G, Lebaron P, Terzic S, Ahel M, Malej A, Mozetic P, Turk V (1999) The accumulation and release of polysaccharides by planktonic cells and the subsequent bacterial response during a controlled experiment. FEMS Microbiol Ecol 29:351–363

    Article  Google Scholar 

  • Fanning KA, Carder KL, Betzer PR (1982) Sediment resuspension by coastal waters—a potential mechanism for nutrient re-cycling on the oceans margins. Deep-Sea Res a Oceanogr Res Pap 29:953–965

    Article  Google Scholar 

  • Flindt MR, Kamp-Nielsen L, Marques JC, Pardal MA, Bocci M, Bendoricchio G, Salomonsen J, Nielsen SN, Jorgensen SE (1997) Description of the three shallow estuaries: Mondego River (Portugal), Roskilde Fjord (Denmark) and the Lagoon of Venice (Italy). Ecol Model 102:17–31

    Article  Google Scholar 

  • Floderus S, Hakanson L (1989) Resuspension, ephemeral mud blankets and nitrogen cycling in laholmsbukten, south east kattegat. Hydrobiologia 176:61–75

    Article  Google Scholar 

  • Grasshoff, K. 1976. Methods for seawater analysis. Verlag Chemie

  • Hansell DA, Carlson CA (2002) Biogeochemistry of marine dissolved organic matter. Academic Press, Cambridge

    Google Scholar 

  • Hopkinson CS, Fry B, Nolin AL (1997) Stoichiometry of dissolved organic matter dynamics on the continental shelf of the northeastern USA. Cont Shelf Res 17:473–489

    Article  Google Scholar 

  • Hopkinson CS, Vallino JJ, Nolin A (2002) Decomposition of dissolved organic matter from the continental margin. Deep-Sea Res Part II 49:4461–4478

    Article  Google Scholar 

  • Howarth RW, Billen G, Swaney D, Townsend A, Jaworski N, Lajtha K, Downing JA, Elmgren R, Caraco N, Jordan T, Berendse F, Freney J, Kudeyarov V, Murdoch P, Zhu ZL (1996) Regional nitrogen budgets and riverine N & P fluxes for the drainages to the North Atlantic Ocean: Natural and human influences. Biogeochemistry 35:75–139

    Article  Google Scholar 

  • Jackson GA, Williams PM (1985) Importance of dissolved organic nitrogen and phosphorus to biological nutrient cycling. Deep Sea Res A Oceanogr Res Pap 32:223–235

    Article  Google Scholar 

  • Jespersen AM, Christoffersen K (1987) Measurements of chlorophyll a from phytoplankton using ethanol as extraction solvent. Arch Hydrobiol 109:445–454

    Google Scholar 

  • Jørgensen L, Markager S, Maar M (2014) On the importance of quantifying bioavailable nitrogen instead of total nitrogen. Biogeochemistry 117:455–472

    Article  Google Scholar 

  • Jakobsen HH, Markager S (2016) Annual dynamics of carbon to chlorophyll ratio in temperate coastal waters. Limnol Oceanogr 61:1853–1866. doi:10.1002/lno.10338

    Article  Google Scholar 

  • Kaas H, Markager S (1998) Technical guidelines for marine monitoring. National Environmental Research Institute, Roskilde, Denmark. http://bios.au.dk/videnudveksling/fagdatacentre/fdcmarintny/tekniske-anvisninger-nova-1998/

  • Kaas H, Møhlenberg F, Forbes V, Pedersen B (1994) Biotilgængelighed af kvælstof og fosfor. Havforskning fra Miljøstyrelsen 40. København, p 47

  • Karl DM, Björkman KM (2002) Dynamics of DOP. In: Hansell D, Carlson CA (eds) Biogeochemistry of marine dissolved organic matter. Academic Press, Cambridge, pp 249–366

    Chapter  Google Scholar 

  • Knudsen-Leerbeck H (2016) The role of dissolved organic matter in the biogeochemical cycling of nutrients in coastal waters. PhD Thesis. Aarhus University

  • Korth F, Deutsch B, Liskow I, Voss M (2012) Uptake of dissolved organic nitrogen by size-fractionated plankton along a salinity gradient from the North Sea to the Baltic Sea. Biogeochemistry 111:347–360

    Article  Google Scholar 

  • Kronvang B, Aertebjerg G, Grant R, Kristensen P, Hovmand M, Kirkegaard J (1993) Nationwide monitoring of nutrients and their ecological effects—state of the danish aquatic environment. Ambio 22:176–187

    Google Scholar 

  • Lønborg C, Alvarez-Salgado XA (2012) Recycling versus export of bioavailable dissolved organic matter in the coastal ocean and efficiency of the continental shelf pump. Global Biogeochem Cycles. doi:10.1029/2012GB004353

    Google Scholar 

  • Lønborg C, Søndergaard M (2009) Microbial availability and degradation of dissolved organic carbon and nitrogen in two coastal areas. Estuar Coast Shelf Sci 81:513–520

    Article  Google Scholar 

  • Lønborg C, Davidson K, Alvarez-Salgado XA, Miller AEJ (2009) Bioavailability and bacterial degradation rates of dissolved organic matter in a temperate coastal area during an annual cycle. Mar Chem 113:219–226

    Article  Google Scholar 

  • Markager S, Sand-Jensen K (1996) Implications of thallus thickness for growth-irradiance relationship of marine macroalgae. Eur J Phycol 31:79–87

    Article  Google Scholar 

  • Markager S, Stedmon CA, Tranvik LJ, Kronberg L, Kulovaara M (2007) Final report for DONKEY—dissolved organic nitrogen as a key nutrient in the Baltic Sea. http://meeting.helcom.fi/c/document_library/get_file?p_l_id=18967&folderId=381607&name=DLFE-37410.pdf

  • Markager S, Stedmon CA, Søndergaard M (2011) Seasonal dynamics and conservative mixing of dissolved organic matter in the temperate eutrophic estuary Horsens Fjord. Estuar Coast Shelf Sci 92:376–388

    Article  Google Scholar 

  • Meybeck M (1982) Carbon, nitrogen, and phosphorus transport by world rivers. Am J Sci 282:401–450

    Article  Google Scholar 

  • Monbet Y (1992) Control of phytoplankton biomass in estuaries - a comparative-analysis of microtidal and macrotidal estuaries. Estuaries 15:563–571

    Article  Google Scholar 

  • Mulholland MR, Bernhardt PW, Blanco-Garcia JL, Mannino A, Hyde K, Mondragon E, Turk K, Moisander PH, Zehr JP (2012) Rates of dinitrogen fixation and the abundance of diazotrophs in North American coastal waters between Cape Hatteras and Georges Bank. Limnol Oceanogr 57:1067–1083

    Article  Google Scholar 

  • Myklestad SM (1995) Release of extracellular products by phytoplankton with special emphasis on polysaccharides. Sci Total Environ 165:155–164

    Article  Google Scholar 

  • Nagata T (2000) Production mechanisms of dissolved organic matter. In: Kirchman DL (ed) Microbial ecology of the oceans. Wiley, Weinheim, pp 121–152

    Google Scholar 

  • Nielsen K, Risgaard-Petersen N, Somod B, Rysgaard S, Bergo T (2001) Nitrogen and phosphorus retention estimated independently by flux measurements and dynamic modelling in the estuary, Randers Fjord, Denmark. Mar Ecol Prog Ser 219:25–40

    Article  Google Scholar 

  • Nixon SW (1995) Coastal marine eutrophication - a definition, social causes, and future concerns. Ophelia 41:199–219

    Article  Google Scholar 

  • Obernosterer I, Reitner B, Herndl GJ (1999) Contrasting effects of solar radiation on dissolved organic matter and its bioavailability to marine bacterioplankton. Limnol Oceanogr 44:1645–1654

    Article  Google Scholar 

  • Pedersen TM, Sand-Jensen K, Markager S, Nielsen SL (2014) Optical changes in a eutrophic estuary during reduced nutrient loadings. Estuar Coasts 37:880–892

    Article  Google Scholar 

  • Petersen JK, Hasler B, Timmermann K, Nielsen P, Tørring DB, Larsen MM, Holmer M (2014) Mussels as a tool for mitigation of nutrients in the marine environment. Mar Pollut Bull 82:137–143

    Article  Google Scholar 

  • Petrone K, Richards J, Grierson P (2009) Bioavailability and composition of dissolved organic carbon and nitrogen in a near coastal catchment of south-western Australia. Biogeochemistry 92:27–40

    Article  Google Scholar 

  • Rees AP, Gilbert JA, Kelly-Gerreyn BA (2009) Nitrogen fixation in the western English Channel (NE Atlantic Ocean). Mar Ecol Prog Ser 374:7–12

    Article  Google Scholar 

  • Riemann B, Carstensen J, Dahl K, Fossing H, Hansen JW, Jakobsen HH, Josefson AB, Krause-Jensen D, Markager S, Staehr PA, Timmermann K, Windolf J, Andersen JH (2016) Recovery of Danish coastal ecosystems after reductions in nutrient loading: a holistic ecosystem approach. Estuar Coasts 39:82–97

    Article  Google Scholar 

  • Savchuk OP (2005) Resolving the Baltic Sea into seven subbasins: N and P budgets for 1991–1999. J Mar Syst 56:1–15

    Article  Google Scholar 

  • Scott D, Harvey J, Alexander R, Schwarz G (2007) Dominance of organic nitrogen from headwater streams to large rivers across the conterminous United States. Global Biogeochemical Cycles. doi:10.1029/2006GB002730

    Google Scholar 

  • Seitzinger SP, Sanders RW (1997) Contribution of dissolved organic nitrogen from rivers to estuarine eutrophication. Mar Ecol Prog Ser 159:1–12

    Article  Google Scholar 

  • Seitzinger SP, Sanders RW, Styles R (2002) Bioavailability of DON from natural and anthropogenic sources to estuarine plankton. Limnol Oceanogr 47:353–366

    Article  Google Scholar 

  • Sipler RE, Bronk DA, Seitzinger SP, Lauck RJ, McGuinness LR, Kirkpatrick GJ, Heil CA, Kerkhof LJ, Schofield OM (2013) Trichodesmium-derived dissolved organic matter is a source of nitrogen capable of supporting the growth of toxic red tide Karenia brevis. Mar Ecol Prog Ser 483:31–45

    Article  Google Scholar 

  • Spokes L, Jickells T, Weston K, Gustafsson BG, Johnsson M, Liljebladh B, Conley D, Ambelas-Skjodth C, Brandt J, Carstensen J, Christiansen T, Frohn L, Geernaert G, Hertel O, Jensen B, Lundsgaard C, Markager S, Martinsen W, Moller B, Pedersen B, Sauerberg K, Sorensen LL, Hasager CC, Sempreviva AM, Pryor SC, Lund SW, Larsen S, Tjernstrom M, Svensson G, Zagar M (2006) MEAD: an interdisciplinary study of the marine effects of atmospheric deposition in the Kattegat. Environ Pollut 140:453–462

    Article  Google Scholar 

  • Staehr PA, Testa J, Carstensen J (2017) Decadal changes in water quality and net productivity of a shallow Danish estuary following significant nutrient reductions. Estuaries Coasts 40:63–79

    Article  Google Scholar 

  • Stedmon CA, Markager S, Søndergaard M, Vang T, Laubel A, Borch NH, Windelin A (2006) Dissolved organic matter (DOM) export to a temperate estuary: seasonal variations and implications of land use. Estuar Coasts 29:388–400

    Article  Google Scholar 

  • Stedmon CA, Markager S, Tranvik L, Kronberg L, Slatis T, Martinsen W (2007) Photochemical production of ammonium and transformation of dissolved organic matter in the Baltic Sea. Mar Chem 104:227–240

    Article  Google Scholar 

  • Stepanauskas R, Edling H, Tranvik LJ (1999) Differential dissolved organic nitrogen availability and bacterial aminopeptidase activity in limnic and marine waters. Microb Ecol 38:264–272

    Article  Google Scholar 

  • Stepanauskas R, Jørgensen NOG, Eigaard OR, Zvikas A, Tranvik LJ, Leonardson L (2002) Summer inputs of riverine nutrients to the Baltic Sea: bioavailability and eutrophication relevance. Ecol Monogr 72:579–597

    Article  Google Scholar 

  • Stolte W, Panosso R, Gisselson LA, Graneli E (2002) Utilization efficiency of nitrogen associated with riverine dissolved organic carbon (>1 kDa) by two toxin-producing phytoplankton species. Aquat Microb Ecol 29:97–105

    Article  Google Scholar 

  • Suratman S, Weston K, Jickells T, Fernand L (2009) Spatial and seasonal changes of dissolved and particulate organic C in the North Sea. Hydrobiologia 628:13–25

    Article  Google Scholar 

  • Tamminen T, Seppala J (1999) Nutrient pools, transformations, ratios, and limitation in the Gulf of Riga, the Baltic Sea, during four successional stages. J Mar Syst 23:83–106

    Article  Google Scholar 

  • Timmermann K, Dinesen GE, Markager S, Ravn-Jonsen L, Bassompierre M, Roth E, Støttrup JG (2014) Development and use of a bioeconomic model for management of mussel fisheries under different nutrient regimes in the temperate estuary of the Limfjord, Denmark. Ecol Soc 19:14

    Article  Google Scholar 

  • Tranvik LJ, Bertilsson S (2001) Contrasting effects of solar UV radiation on dissolved organic sources for bacterial growth. Ecol Lett 4:458–463

    Article  Google Scholar 

  • Traving SJ, Bentzon-Tilia M, Knudsen-Leerbeck H, Mantikci M, Hansen JL, Stedmon CA, Sørensen H, Markager S, Riemann L (2016) Coupling bacterioplankton populations and environment to community function in coastal temperate waters. Front Microbiol. doi:10.3389/fmicb.2016.01533

    Google Scholar 

  • Vahatalo AV, Zepp RG (2005) Photochemical mineralization of dissolved organic nitrogen to ammonium in the Baltic Sea. Environ Sci Technol 39:6985–6992

    Article  Google Scholar 

  • Ward BB, Bronk DA (2001) Net nitrogen uptake and DON release in surface waters: importance of trophic interactions implied from size fractionation experiments. Mar Ecol Prog Ser 219:11–24

    Article  Google Scholar 

  • Wiberg-Larsen P,Windolf J, Bogestrand J, Larsen SE, Thodsen H, Ovesen NB, Kronvang B, Kjeldgaard A (2012) Vandløb 2011 NOVANA. Scientific report no. 75, Aarhus University, Aarhus, Denmark, p 84. http://dce2.au.dk/pub/SR75.pdf

  • Williams PJL (1995) Evidence for the seasonal accumulation of carbon-rich dissolved organic material, its scale in comparison with changes in particulate material and the consequential effect on net C/N assimilation ratios. Mar Chem 51:17–29

    Article  Google Scholar 

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Acknowledgements

We wish to thank The Danish Nature Agency for help with water sampling. We also thank Dorete Weysmann Jensen for nutrient analysis, Colin Stedmon for help with TOC/DOC analysis, and Ciarán Murray for help with Fig. 1. This study was supported by the project ‘Integrated management of agriculture, fishery, environment and economy’ (IMAGE) project (09-067259) funded by the Innovation Fund Denmark, and project 11-105450 and 09-066396 from the Danish council for independent research. SJT was supported by the VKR Center of Excellence on Ocean Life, funded by the Villum foundation.

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Knudsen-Leerbeck, H., Mantikci, M., Bentzon-Tilia, M. et al. Seasonal dynamics and bioavailability of dissolved organic matter in two contrasting temperate estuaries. Biogeochemistry 134, 217–236 (2017). https://doi.org/10.1007/s10533-017-0357-2

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