Environmental Earth Sciences

, Volume 74, Issue 7, pp 6027–6038 | Cite as

Nitrogen uptake and cycling in Phragmites australis in a lake-receiving nutrient-rich mine water: a 15N tracer study

  • Sara ChlotEmail author
  • Anders Widerlund
  • Björn Öhlander
Original Article


Uptake and cycling of nitrogen (N) in the littoral zone of a lake-receiving nutrient-rich mine water located in Boliden, northern Sweden, was investigated. Stable isotope tracer solutions of 15N as NH4 + (NAM mesocosm) or NO3 (NOX mesocosm) were added to mesocosms enclosing plants of common reed (Phragmites australis). The 15N abundance in various plant parts was measured at pre-defined time intervals over an experimental period of 22 days. During the course of the experiment, plant parts from the NAM mesocosms were significantly more enriched in 15N than plant parts from the NOX mesocosms. On day 13, Δδ15N values of the fine roots from the NAM mesocosms had reached +8220 ‰, while the maximum Δδ15N value in NOX roots was considerably lower at +4430 ‰. Using 15N values in macrophyte tissues present at the end of the experiment enabled calculations of uptake rates and % of tracer N recovered in the plant (%tracerNrecov). Maximum tracer uptake rates were higher for the NAM mesocosms (1.4 µg g−1 min−1 or 48 mg N m−2 d−1) compared to the NOX mesocosms (0.23 µg g−1 min−1 or 8.5 mg N m−2 d−1). Calculations of %tracerNrecov indicated that 1–8 and 25–44 % of added N was assimilated by plants in the NOX and NAM mesocosms, respectively. Hence, P. australis was more effective in assimilating NH4 +, and a larger portion of the tracer N accumulated in the roots compared to the other plant parts. Consequently, macrophyte N removal is most effective for cold-climate aquatic systems receiving mine water dominated by NH4 +. For permanent removal of N, the whole plant (including the roots) should be harvested.


Mine water Northern Sweden Nitrogen Phragmites australis Mesocosm Stable isotope labelling 



The study was supported by grants from the Swedish Governmental Agency for Innovation Systems (VINNOVA) to B. Öhlander (Grant No. 2007-01680) and the mining companies LKAB, Boliden Mineral AB, the Adolf H. Lundin Charitable Foundation, and J Gust Richert Foundation. We wish to thank Milan Vnuk for final drawing of the figures. We also wish to thank Skellefteå Kommun for permission to use the bathymetric map of Lake Bruträsket. This is a CAMM (Centre of Advanced Mining and Metallurgy) publication.


  1. Ahn C, Mitsch MJ (2002) Scaling considerations of mesocosm wetlands in simulating large created freshwater marshes. Ecol Eng 18:327–342CrossRefGoogle Scholar
  2. Allen RL, Weihed P, Svensson SÅ (1997) Setting of Zn-Cu-Au-Ag Massive Sulfide Deposits in the Evolution and Facies Architecture of a 1.9 Ga Marine Volcanic Arc, Skellefte District, Sweden. Econ Geol 91:1022–1053CrossRefGoogle Scholar
  3. Barko JW, Gunnison D, Carpenter SR (1991) Sediment interactions with submersed macrophyte growth and community dynamics. Aquat Bot 41:41–65CrossRefGoogle Scholar
  4. Barraclough D (1995) 15N isotope dilution techniques to study soil nitrogen transformations and plant uptake. Fert Res 42:185–192CrossRefGoogle Scholar
  5. Barrón C, Middelbrug JJ, Duarte CM (2006) Phytoplankton trapped within seagrass (Posidonia oceanica) sediments are a nitrogen source: an in situ labelling experiment. Limnol Oceanogr 51:1648–1653CrossRefGoogle Scholar
  6. Best MD, Mantai KE (1978) Growth of Myriophyllum: sediment or lake water as the source of nitrogen and phosphorus. Ecology 59:1075–1080CrossRefGoogle Scholar
  7. Campbell CS, Ogden MH (1999) Constructed wetlands in the sustainable landscape. Wiley, New YorkGoogle Scholar
  8. Carpenter SR (1996) Microcosm experiments have limited relevance for community and ecosystem ecology. Ecology 77:677–680CrossRefGoogle Scholar
  9. Carpenter SR, Cole JJ, Pace ML, Van de Bogert M, Bade DL, Bastviken D, Gille CM, Hogsdon JR, Kitchell JF, Kritzberg ES (2005) Ecosystem subsidies: terrestrial support of aquatic food webs from 13C addition to contrasting lakes. Ecology 86:2737–2750CrossRefGoogle Scholar
  10. Chlot S, Widerlund A, Siergieiev D, Ecke F, Husson E, Öhlander B (2011) Modelling nitrogen transformations in waters receiving mine effluents. Sci Total Environ 49:4585–4595CrossRefGoogle Scholar
  11. Chlot S, Widerlund A, Husson E, Öhlander B, Ecke F (2013) Effects on nutrient regime in two recipients of nitrogen rich mine effluents in northern Sweden. Appl Geochem 31:12–24CrossRefGoogle Scholar
  12. Dahlin AS, Stenberg M, Marstorp H (2011) Mulch N recycling in green manure leys under Scandinavian conditions. Nutr Cycl Agroecosyst 91:119–129CrossRefGoogle Scholar
  13. Dugdale RC, Wilkerson FP (1986) The use of 15N to measure nitrogen uptake in eutrophic oceans; experimental considerations. Limnol Oceanogr 31:673–689CrossRefGoogle Scholar
  14. Ehaliotis C, Cadish G, Killer KE (1998) Substrate amendments can alter dynamics and N availability from maize residues to subsequent crops. Soil Biol Biochem 30:1281–1292CrossRefGoogle Scholar
  15. Epstein DM, Wurtsbaugh WA, Baker MA (2012) Nitrogen portioning and transport through a subalpine lake measured with an isotope tracer. Watershed Sciences Faculty Publications Paper 547, Utah UniversityGoogle Scholar
  16. Eriksson PG, Weisner SEB (1999) An experimental study on effects of submersed effects of macrophytes on nitrification and denitrification in ammonium-rich aquatic systems. Limnol Oceanogr 44:1993–1999CrossRefGoogle Scholar
  17. Forshay KJ, Dodson SI (2011) Macrophyte presence is an indicator of enhanced denitrification and nitrification in sediments of a temperate restored agricultural stream. Hydrobiologia 668:21–34CrossRefGoogle Scholar
  18. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai ZC, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions and potential solutions. Science 320:889–892CrossRefGoogle Scholar
  19. Golterman HL (2004) The chemistry of phosphate and nitrogen compounds in sediments. Springer, DordrechtGoogle Scholar
  20. González-Sagrario M, Jeppesen E, Gomá J, Søndergaard M, Jensen JP, Lauridsen T, Landkildehus F (2005) Does high nitrogen loading prevent clear-water conditions in shallow lakes at moderately high phosphorus concentrations? Freshw Biol 50:27–41CrossRefGoogle Scholar
  21. Gribsholt B, Kristensen E (2002) Effects of bioturbation and plant rootson salt marsh biogeochemistry: a mesocosm study. Mar Ecol Prog 241:71–87CrossRefGoogle Scholar
  22. Gribsholt B, Struyf E, Tramper A, De Brandebere L, Bio N, van Damme S, Meire P, Dehairs F, Middelburg JJ, Boschker HTS (2007) Nitrogen assimilation and short term retention in a nutrient-rich tidal freshwater marsh—a whole ecosystem 15N enrichment study. Biogeosciences 4:11–26CrossRefGoogle Scholar
  23. Gribsholt B, Veuger B, Tramper A, Middelburg JJ, Boschker HTS (2009) Long-term 15N-nitrogen retention in tidal freshwater marsh sediments: elucidating the microbial contribution. Limnol Ocenogr 54:13–22CrossRefGoogle Scholar
  24. Gry MB, Gilbert PM, Chen CC (1999) Dimension effects of enclosure on ecological processes in pelagic systems. Limnol Oceanogr 44:1331–1340CrossRefGoogle Scholar
  25. Hansson J (2006) Determination of residual flotation collectors and their possible degradation products in process water from the concentrator in Boliden. Master Thesis, Umeå UniversityGoogle Scholar
  26. Häyrynen K, Langwaldt J, Pongrácz E, Väisänen V, Mänttäri M, Keiski RL (2008) Separation of nutrients from mine water by reverse osmosis for subsequent biological treatment. Miner Eng 21:2–9CrossRefGoogle Scholar
  27. Högberg P (1997) Tansley review No. 95. 15N natural abundance in soil-plant systems. New Phytol 137:179–203CrossRefGoogle Scholar
  28. Hood JLA (2012) The role of submerged macrophytes in river eutrophication and biogeochemical nutrient cycling. PhD thesis, University of WaterlooGoogle Scholar
  29. Horppila J, Nurminen L (2001) The effect of an emergent macrophyte (Typha angustifolia) on sediment resuspension in a shallow north temperate lake. Freshwater Biol 46:1447–1455CrossRefGoogle Scholar
  30. Husson E, Hagner O, Ecke F (2013) Unmanned aircraft systems help to map aquatic vegetation. Appl Veg Sci. doi: 10.1111/avsc.12072 Google Scholar
  31. INAP, Global Acid Rock Drainage (GARD) Guide, 2014. Accessed November 2014
  32. Jing S-R, Lin Y-F (2004) Seasonal effect on ammonia nitrogen removal by constructed wetlands treating polluted river water in southern Taiwan. Environ Pollut 127:291–301CrossRefGoogle Scholar
  33. Kadlec RH, Tanner CC, Hally VW, Gibbs MM (2005) Nitrogen spiralling in subsurface-flow constructed wetlands: implications for treatment response. Ecol Eng 25:365–381CrossRefGoogle Scholar
  34. Koren DW, Gould WD, Bedard P (2000) Biological removal of ammonia and nitrate from simulated mine and mill effluents. Hydrometallurgy 56:127–144CrossRefGoogle Scholar
  35. Koskiaho J, Ekholm P, Räty M, Riihimäki J, Puustinen M (2003) Retaining agricultural nutrients in constructed wetlands—experiences under boreal conditions. Ecol Eng 20:89–103CrossRefGoogle Scholar
  36. Li K, Zhengwen L, Binhe G (2010) The fate of cyanobacterial blooms in vegetated and unvegetated sediments of a shallow eutrophic lake: a stable isotope tracer study. Water Res 44:1591–1597CrossRefGoogle Scholar
  37. Logsdon MJ, Hagelstein K, Mudder TI (1999) The Management of Cyanide in Gold Extraction. International Council on Metals and the EnvironmentGoogle Scholar
  38. Lottermoser B (2010) Mine wastes—characterization, treatment and environmental impacts. Springer, BerlinGoogle Scholar
  39. Maltais-Landry G, Maranger R, Brisson J, Chazarenc F (2009) Nitrogen transformations and retention in planted and artificially constructed wetlands. Water Res 43:535–545CrossRefGoogle Scholar
  40. Mariotti A, Gemon JC, Petal H (1981) Experimental determination of nitrogen kinetic isotope fractionations: some principles, illustration for denitrification and nitrification processes. Plant Soil 62:413–430CrossRefGoogle Scholar
  41. Mattila K, Zaitsev G, Langwaldt J (2007) Biological removal of nutrients from mine waters Biologinen ravinteiden poisto kaivosvedestä Final report—Loppuraportti. RovaniemiGoogle Scholar
  42. Morin KA, Hutt NM, (2009) Mine-water leaching of nitrogen species from explosives residues. In: Proceedings of GeoHalifax 2009, the 62nd Canadian Geotechnical Conference and 10th Joint CGS/IAH–CNC Groundwater Conference, Halifax, Nova Scotia, September 20–24. pp 1549–1553Google Scholar
  43. Nijburg JW, Laanbroek HJ (1997) The fate of 15N-nitrate in healthy and declining Phragmites australis stands. Microb Ecol 34:254–262CrossRefGoogle Scholar
  44. Noe GB, Scinto LJ, Taylor J, Childers DL, Jone RD (2003) Phosphorus cycling and partitioning in an oligotrophic Everglades wetland ecosystem: a radioisotope tracer study. Freshw Biol 48:1933–2008CrossRefGoogle Scholar
  45. Odum EP (1984) The mesocosm. Bioscience 34:558–562CrossRefGoogle Scholar
  46. Robbins G, Devuyst E, Malevich A, Agius R, Iamarino P, Lindvall M (2001) Cyanide management at Boliden using the Inco SO 2/AIR Process. Securing the Future, Skellefteå, pp 718–728Google Scholar
  47. Romero JA, Brix H, Comín FA (1999) Interactive effects of N and P growth, nutrient allocation and NH4 uptake kinetics by Phragmites australis. Aquat Bot 64:369–380CrossRefGoogle Scholar
  48. Schindler DW (1998) Replication versus realism: the need for the ecosystem scale. Ecosystems 1:323–334CrossRefGoogle Scholar
  49. Schindler DE, Scheurell MD (2002) Habitat coupling in lake ecosystems. Oikos 98:177–189CrossRefGoogle Scholar
  50. Shaver GR, Mellilo JM (1984) Nutrient budgets of marsh plants: efficiency concepts and relation to availability. Ecology 65:1491–1510CrossRefGoogle Scholar
  51. Sjörs H (1999, 1) The background: Geology climate and zonation Acta Phytogeograhica Suecica 84 5-14. In: Swedish plant geography, Eds: Rydin H, Snoeijs P, Diekmann MGoogle Scholar
  52. Sollie S, Coops H, Verhoeven JTA (2008) Natural and constructed littoral zones as nutrient traps in eutrophic shallow lakes. Hydrobiologia 605:219–233CrossRefGoogle Scholar
  53. Tan Y, Li J, Cheng J, Gu B, Hong J (2013) The sinks of dissolved inorganic nitrogen in surface water of wetland mesocosms. Ecol Eng 52:125–129CrossRefGoogle Scholar
  54. Tanner CC (1996) Plants for constructed wetland treatment systems—a comparison of the growth and nutrient assimilation of eight emergent species. Ecol Eng 7:59–83CrossRefGoogle Scholar
  55. Tunsҫiper B (2009) Nitrogen removal in a combined vertical and horizontal subsurface-flow constructed wetland system. Desalination 247:466–475CrossRefGoogle Scholar
  56. Tylová E, Steinbachová L, Votrubová O, Bent L, Brix H (2008) Different sensitivity of Phragmites australis and Glyceria maxima to high availability of ammonium-N. Aquat Bot 88:93–98CrossRefGoogle Scholar
  57. Tylová-Munzarova W, Lorenzen B, Brix H, Votrubová O (2005) The effects of NH4 + and NO3 on growth, resource allocation and nitrogen uptake kinetics of Phragmites australis and Glyceria maxima. Aquat Bot 81:326–342CrossRefGoogle Scholar
  58. Vymazal J (2013) Emergent plants used in free surface constructed wetlands: a review. Ecol. Eng. doi: 10.1016/j.ecoleng.2013.06.023 Google Scholar
  59. Weihed P, Bergman J, Bergström U (1992) Metallogeny and tectonic evolution of the Early Proterozoic Skellefte district, northern Sweden. Precambrian Res 58:143–167CrossRefGoogle Scholar
  60. Wozniak JR, Childers DL, Anderson WT, Rudnick DT, Madden CJ (2008) An in situ mesocosm method for quantifying nitrogen cycling rates in oligotrophic wetlands using 15N tracer techniques. Wetlands 28:502–512CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Sara Chlot
    • 1
    • 2
    Email author
  • Anders Widerlund
    • 1
  • Björn Öhlander
    • 1
  1. 1.Division of Geosciences and Environmental EngineeringLuleå University of TechnologyLuleåSweden
  2. 2.County Administration Board of NorrbottenLuleåSweden

Personalised recommendations