Aquatic Ecology

, Volume 53, Issue 4, pp 719–744 | Cite as

Hierarchy of factors controls denitrification rates in temperate intermittently closed and open coastal lakes/lagoons (ICOLLS)

  • Josie A. CrawshawEmail author
  • Marc Schallenberg
  • Candida Savage
  • Robert Van Hale


Intermittently closed and open lakes/lagoons (ICOLLs) can occur in alternate stable states: clear and turbid, with nitrogen inputs from high-intensity agricultural land use often fuelling phytoplankton growth in ICOLLs. Due to their limited water exchange, ICOLLs are particularly susceptible to eutrophication. In these environments, denitrification may remove a substantial proportion of the land-derived nitrogen load, reducing their vulnerability to eutrophication; however, the factors that influence denitrification in ICOLLs are poorly understood. In this study, we addressed the relative importance of physico-chemical and biotic factors related to nitrate-saturated denitrification rates (including temperature, nutrient/organic matter supply, oxygen conditions, sediment type and benthic macroinvertebrates) in two eutrophic ICOLL ecosystems: one supports some submerged macrophytes, while the other is in a persistent, turbid, phytoplankton-dominated system. Flexible in situ enclosures and denitrification enzyme assay measurements were employed to determine denitrification rates in response to new nitrate pulses, which are commonly observed in these systems. In situ denitrification rates were inhibited in both ICOLLs in winter, whereas in summer they were positively correlated with organic matter availability. Denitrification rates were greater in the shallow, marginal sediments of the ICOLLs. Bioturbating macrofauna significantly enhanced in situ sediment oxygenation and probably transported sediment organic carbon and nitrate simultaneously to sites of denitrification at the sediment oxic–anoxic interface. Our study found that nitrate-saturated sediment denitrification rates were controlled by a hierarchy of temporally and spatially structured physico-chemical and biotic factors in the following order of importance: temperature → organic matter availability → water depth → bioturbation.


Nitrogen cycling Isotope pairing Denitrification enzyme activity Bioturbation Oxygen penetration depth (OPD) 



J.C. was supported by a University of Otago PhD Scholarship and additional research money from the Brenda Shore Award (University of Otago), the New Zealand Coastal Society (Masters Scholarship) and the Hutton Fund (Royal Society of New Zealand). M.S. was also supported by a subcontract from the National Institute of Water and Atmospheric Research (NIWA; C01X1005). We thank T. Davie from the Canterbury Regional Council and also the Whakaora Te Waihora Board for supporting this work and Environment Canterbury for sharing their water quality data from Lake Ellesmere with us. A. Santoso and D. Hamilton at the Environmental Research Institute, University of Waikato, ran the denitrification enzyme assays. N. McHugh (University of Otago Zoology Department) kindly carried out the nutrient samples. Finally, we thank A. Innes and the Tomahawk Lagoon Citizen Science Team for providing nitrate concentration time-series data for Tomahawk Lagoon. We thank the anonymous reviewers whose comments have enhanced the quality of this manuscript.

Supplementary material

10452_2019_9721_MOESM1_ESM.docx (2 mb)
Supplementary material 1 (DOCX 2011 kb)


  1. An S, Joye SB (2001) Enhancement of coupled nitrification-denitrification by benthic photosynthesis in shallow estuarine sediments. Limnol Oceanogr 46:62–74CrossRefGoogle Scholar
  2. Arango CP, Tank JL, Johnson LT, Hamilton SK (2008) Assimilatory uptake rather than nitrification and denitrification determines nitrogen removal patterns in streams of varying land use. Limnol Oceanogr 53:2558–2572. CrossRefGoogle Scholar
  3. Asmus RM, Jensen MH, Jensen KM, Kristensen E, Asmus H, Wille A (1998) The role of water movement and spatial scaling for measurement of dissolved inorganic nitrogen fluxes in intertidal sediments. Estuar Coast Shelf Sci 46(2):221–232CrossRefGoogle Scholar
  4. Banks JL, Ross DJ, Keough MJ, Macleod CK, Keane J, Eyre BD (2013) Influence of a burrowing, metal-tolerant polychaete on benthic metabolism, denitrification and nitrogen regeneration in contaminated estuarine sediments. Mar Pollut Bull 68:30–37. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bernard RJ, Mortazavi B, Kleinhuizen AA (2015) Dissimilatory nitrate reduction to ammonium (DNRA) seasonally dominates NO3-reduction pathways in an anthropogenically impacted sub-tropical coastal lagoon. Biogeochemistry 125:47–64. CrossRefGoogle Scholar
  6. Bianchi TS (2011) The role of terrestrially derived organic carbon in the coastal ocean: a changing paradigm and the priming effect. Proc Natl Acad Sci 108:19473–19481. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Bianchi TS, Allison MA, Cai W-J (2014) Biogeochemical dynamics at major river-coastal interfaces: linkages with global change. Cambridge University Press, New YorkGoogle Scholar
  8. Biswas JK, Ranaa S, Bhakta JN, Jana BB (2009) Bioturbation potential of chironomid larvae for the sediment–water phosphorus exchange in simulated pond systems of varied nutrient enrichment. Ecol Eng 35:1444–1453CrossRefGoogle Scholar
  9. Bruesewitz D, Hamilton D, Schipper L (2011) Denitrification potential in lake sediment increases across a gradient of catchment agriculture. Ecosystems 14:341–352. CrossRefGoogle Scholar
  10. 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.;2 CrossRefGoogle Scholar
  11. Colt J (2012) 2—solubility of atmospheric gases in brackish and marine waters. In: Colt J (ed) Computation of dissolved gas concentration in water as functions of temperature, salinity and pressure, 2nd edn. Elsevier, London, pp 73–131. CrossRefGoogle Scholar
  12. Cook PLM et al (2006) Quantification of denitrification in permeable sediments: insights from a two-dimensional simulation analysis and experimental data. Limnol Oceanogr Methods 4:294–307CrossRefGoogle Scholar
  13. Cornwell J, Kemp WM, Kana T (1999) Denitrification in coastal ecosystems: methods, environmental controls, and ecosystem level controls, a review. Aquat Ecol 33:41–54. CrossRefGoogle Scholar
  14. Crawshaw JA (2018) Sinks of agriculturally derived nitrogen in coastal and estuarine ecosystems. Ph.D. Dissertation, University of Otago, New ZealandGoogle Scholar
  15. Crawshaw JA, Schallenberg M, Savage C (2019) Physical and biological drivers of sediment oxygenation and denitrification in a New Zealand intermittently closed and open lake lagoon. NZ J Mar Freshw Res 53:33–59CrossRefGoogle Scholar
  16. Dalsgaard T (2000) Protocol handbook for NICE: nitrogen cycling in estuaries: a project under the EU research programme Marine Science and Technology (MAST III). National Environmental Research Institute, NagpurGoogle Scholar
  17. Dalsgaard T, Thamdrup B, Canfield DE (2005) Anaerobic ammonium oxidation (anammox) in the marine environment. Res Microbiol 156:457–464. CrossRefPubMedPubMedCentralGoogle Scholar
  18. Damashek J, Francis CA (2018) Microbial nitrogen cycling in estuaries: from genes to ecosystem processes. Estuar Coasts 41(3):626–660CrossRefGoogle Scholar
  19. de Wit R et al (2001) ROBUST: the ROle of BUffering capacities in STabilising coastal lagoon ecosystems. Cont Shelf Res 21:2021–2041. CrossRefGoogle Scholar
  20. Devol AH (2015) Denitrification, anammox, and N2 production in marine sediments. Ann Rev Mar Sci 7:403–423PubMedCrossRefPubMedCentralGoogle Scholar
  21. Dodla SK, Wang JJ, DeLaune RD, Cook RL (2008) Denitrification potential and its relation to organic carbon quality in three coastal wetland soils. Sci Total Environ 407:471–480. CrossRefPubMedPubMedCentralGoogle Scholar
  22. Drake DC, Kelly D, Schallenberg M (2011) Shallow coastal lakes in New Zealand: current conditions, catchment-scale human disturbance, and determination of ecological integrity. Hydrobiologia 658:87–101. CrossRefGoogle Scholar
  23. Eyre BD, Ferguson AJP (2002) Comparison of carbon production and decomposition, benthic nutrient fluxes and denitrification in seagrass, phytoplankton, benthic microalgae-and macroalgae-dominated warm-temperate Australian lagoons. Mar Ecol Prog Ser 229:43–59CrossRefGoogle Scholar
  24. Fanjul E, Bazterrica MC, Escapa M, Grela MA, Iribarne O (2011) Impact of crab bioturbation on benthic flux and nitrogen dynamics of Southwest Atlantic intertidal marshes and mudflats. Estuar Coast Shelf Sci 92(4):629–638CrossRefGoogle Scholar
  25. Ferrón S, Alonso-Pérez F, Anfuso E, Murillo FJ, Ortega T, Castro CG, Forja JM (2009) Benthic nutrient recycling on the northeastern shelf of the Gulf of Cádiz (SW Iberian Peninsula). Mar Ecol Prog Ser 390:79–95CrossRefGoogle Scholar
  26. Fulweiler RW, Nixon SW, Buckley BA, Granger SL (2008) Net sediment N2 fluxes in a coastal marine system—experimental manipulations and a conceptual model. Ecosystems 11:1168–1180. CrossRefGoogle Scholar
  27. Gerbeaux P (1989) Aquatic plant decline in Lake Ellesmere: a case for macrophyte management in a shallow New Zealand lake. Ph.D. Dissertation, Lincoln University, New ZealandGoogle Scholar
  28. Gerbeaux P (1993) Potential for re-establishment of aquatic plants in Lake Ellesmere (New Zealand). J Aquat Plant Manag 31:122–128Google Scholar
  29. Gerbeaux P, Ward JC (1991) Factors affecting water clarity in Lake Ellesmere, New Zealand. NZ J Mar Freshw Res 25:289–296. CrossRefGoogle Scholar
  30. Gerino M, Stora G, Francious-Caraillet F, Gilbert F, Poggiale JC, Mermillod-Blondin F, Desrosiers G, Vervier P (2003) Macro-invertebrate functional groups in freshwater and marine sediments: a common mechanistic classification. Vie et Milieu 53(4):221–231Google Scholar
  31. 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 26:124–131CrossRefGoogle Scholar
  32. Gilbert F, Bonin P, Stora G (1995) Effect of bioturbation on denitrification in a marine sediment from the West Mediterranean littoral. Hydrobiologia 304:49–58CrossRefGoogle Scholar
  33. Gilbert F, Aller RC, Hulth S (2003) The influence of macrofaunal burrow spacing and diffusive scaling on sedimentary nitrification and denitrification: an experimental and model approach. J Mar Res 61:101–125CrossRefGoogle Scholar
  34. Gluckman P (2017) New Zealand’s fresh waters: values, state, trends and human impacts. Office of the Prime Ministers Chief Science Advisor. PO Box 108-117, Symonds Street, Auckland 1150, New ZealandGoogle Scholar
  35. Glud RN, Berg P, Stahl H, Hume A, Larsen M, Eyre BD, Cook PLM (2016) Benthic carbon mineralization and nutrient turnover in a Scottish sea loch: an integrative in situ study. Aquat Geochem. CrossRefGoogle Scholar
  36. Gongol CL (2010) Denitrification, oxygen consumption, and anaerobic ammonium oxidation in sediments of four New Zealand estuaries. Ph.D. Dissertation, University of Otago, New ZealandGoogle Scholar
  37. Gongol C, Savage C (2016) Spatial variation in rates of benthic denitrification and environmental controls in four New Zealand estuaries. Mar Ecol Prog Ser 556:59–77CrossRefGoogle Scholar
  38. Gooderham J, Tsyrlin E (2002) The waterbug book: a guide to the freshwater macroinvertebrates of temperate Australia. CSIRO Publishing, ClaytonCrossRefGoogle Scholar
  39. Groffman PM et al (2009) Challenges to incorporating spatially and temporally explicit phenomena (hotspots and hot moments) in denitrification models. Biogeochemistry 93:49–77CrossRefGoogle Scholar
  40. Hamill KD, Schallenberg M (2013) Mechanisms that drive in-lake nutrient processing with Te Waihora/Lake Ellesmere: inter-annual water quality variability. Report prepared for Whakaora Te Waihora by River Lake Ltd, Whakatane, New ZealandGoogle Scholar
  41. Hamill KD, Kelly D, Hamilton D, Howard-Wiliams C, Robertson B, Schallenberg M, Vant B, Ward N (2014) Attributes for Intermittently Open and Closed Lakes and Lagoons (ICOLLs) applicable to the National Objectives Framework for Fresh Water. Report prepared for Ministry for the Environment by River Lake Ltd, Whakatane, New ZealandGoogle Scholar
  42. Hamilton DP, Mitchell SF (1997) Wave-induced shear stresses, plant nutrients & chlorophyll in seven shallow lakes. Freshw Biol 38:159–168CrossRefGoogle Scholar
  43. Hamilton SK, Ostrom NE (2007) Measurement of the stable isotope ratio of dissolved N2 in 15N tracer experiments. Limnol Oceanogr Methods 5:233–240. CrossRefGoogle Scholar
  44. Hardison AK, Canuel EA, Anderson IC, Tobias CR, Veuger B, Waters MN (2013) Microphytobenthos and benthic macroalgae determine sediment organic matter composition in shallow photic sediments. Biogeosciences 10:5571–5588. CrossRefGoogle Scholar
  45. Hardison AK, Algar CK, Giblin AE, Rich JJ (2015) Influence of organic carbon and nitrate loading on partitioning between dissimilatory nitrate reduction to ammonium (DNRA) and N2 production. Geochim Cosmochim Acta 164:146–160. CrossRefGoogle Scholar
  46. Hawes I, Ward JC (1996) The factors controlling the growth and abundance of phytoplankton in Lake Ellesmere. Report prepared for Environment Canterbury by NIWA, Christchurch, New ZealandGoogle Scholar
  47. Hearnshaw EJS, Hughey KFD (2012) A novel tolerance range approach for the quantitative assessment of ecosystems. Sci Total Environ 420:13–23. CrossRefPubMedPubMedCentralGoogle Scholar
  48. Heggie K, Savage C (2009) Nitrogen yields from New Zealand coastal catchments to receiving estuaries. NZ J Mar Freshw Res 43:1039–1052. CrossRefGoogle Scholar
  49. Herbert RA (1999) Nitrogen cycling in coastal marine ecosystems. FEMS Microbiol Rev 23:563–590PubMedCrossRefPubMedCentralGoogle Scholar
  50. Highton MP, Roosa S, Crawshaw J, Schallenberg M, Morales SE (2016) Physical factors correlate to microbial community structure and nitrogen cycling gene abundance in a nitrate fed eutrophic lagoon. Front Microbiol. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Hughes HR, McColl RHS, Rawlence DJ (1974) Lake Ellesmere, Canterbury, New Zealand. A review of the lake and its catchment. DSIR, WellingtonGoogle Scholar
  52. Inwood S, Tank J, Bernot M (2007) Factors controlling sediment denitrification in midwestern streams of varying land use. Microb Ecol 53:247–258. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Joye SB, Hollibaugh JT (1995) Influence of sulphide inhibition of nitrification on nitrogen regeneration in sediments. Science 270(5236):623–625CrossRefGoogle Scholar
  54. Kana TM, Sullivan MB, Cornwell JC, Groxzkowski KM (1998) Denitrification in estuarine sediments determined by membrane inlet mass spectrometry. Limnol Oceanogr 43:334–339. CrossRefGoogle Scholar
  55. Kennish MJ, Paerl HW (2010) Coastal lagoons: critical habitats of environmental change. CRC Press, Boca RatonCrossRefGoogle Scholar
  56. Kessler AJ, Roberts KL, Bissett A, Cook PLM (2018) Biogeochemical controls on the relative importance of denitrification and dissimilatory nitrate reduction to ammonium in estuaries. Global Biogeochem Cycles 32(7):1045–1057CrossRefGoogle Scholar
  57. Kreiling RM, Richardson WB, Cavanaugh JC, Bartsch LA (2011) Summer nitrate uptake and denitrification in an upper Mississippi River backwater lake: the role of rooted aquatic vegetation. Biogeochemistry 104:309–324CrossRefGoogle Scholar
  58. Kristensen E, Jensen MH, Andersen TK (1985) The impact of polychaete (Nereis virens Sars) burrows on nitrification and nitrate reduction in estuarine sediments. J Exp Mar Biol Ecol 85(1):75–91CrossRefGoogle Scholar
  59. Lagauzère S, Pischedda L, Cuny P, Gilbert F, Stora G, Bonzom JM (2009) Influence of Chironomus riparius (Diptera, Chironomidae) and Tubifex tubifex (Annelida, Oligochaeta) on oxygen uptake by sediments. Consequences of uranium contamination. Environ Pollut 157(4):1234–1242PubMedCrossRefPubMedCentralGoogle Scholar
  60. Landcare Research (2015) Identification guide: what freshwater insect is this? Landcare Research. Accessed June 2015
  61. Lewicka-Szczebak D, Well R, Giesemann A, Rohe L, Wolf U (2013) An enhanced technique for automated determination of 15N signatures of N2, (N2 + N2O) and N2O in gas samples. Rapid Commun Mass Spectrom 27:1548–1558. CrossRefPubMedPubMedCentralGoogle Scholar
  62. Loken LC, Small GE, Finlay JC, Sterner RW, Stanley EH (2016) Nitrogen cycling in a freshwater estuary. Biogeochemistry 127:199–216. CrossRefGoogle Scholar
  63. Macreadie PI, Ross DJ, Longmore AR, Keough MJ (2006) Denitrification measurements of sediments using cores and chambers. Mar Ecol Prog Ser 326:49–59CrossRefGoogle Scholar
  64. Mayer MS, Schaffner L, Kemp WM (1995) Nitrification potentials of benthic macrofaunal tubes and burrow walls: effects of sediment NH4 + and animal irrigation behaviour. Mar Ecol Prog Ser 121:157–169CrossRefGoogle Scholar
  65. McDowell RW, Wilcock RJ (2008) Water quality and the effects of different pastoral animals. NZ Vet J 56:289–296. CrossRefGoogle Scholar
  66. McGlathery KJ, Sundbäck K, Anderson IC (2007) Eutrophication in shallow coastal bays and lagoons: the role of plants in the coastal filter. Marine Ecology Progress Series 348Google Scholar
  67. McMillan SK, Piehler MF, Thompson SP, Paerl HW (2010) Denitrification of nitrogen released from senescing algal biomass in coastal agricultural headwater streams. J Environ Qual 39:274–281PubMedCrossRefPubMedCentralGoogle Scholar
  68. McSweeney SL, Kennedy DM, Rutherfurd ID, Stout JC (2017) Intermittently closed/open lakes and lagoons: their global distribution and boundary conditions. Geomorphology 292:142–152. CrossRefGoogle Scholar
  69. Mengis M, Gächter R, Wehrli B, Bernasconi S (1997) Nitrogen elimination in two deep eutrophic lakes. Limnol Oceanogr 42(7):1530–1543CrossRefGoogle Scholar
  70. Mitchell SF (1989) Primary production in a shallow eutrophic lake dominated alternately by phytoplankton and by submerged macrophytes. Aquat Bot 33:101–110. CrossRefGoogle Scholar
  71. Mitchell SF, Hamilton DP, Macgibbon WS, Nayar PKB, Reynolds RN (1988) Interrelations between phytoplankton, submerged macrophytes, black swans (Cygnus atratus) and zooplankton in a shallow New Zealand lake. Internationale Revue der gesamten Hydrobiologie und Hydrographie 73:145–170. CrossRefGoogle Scholar
  72. Moore SC (1997) A photographic guide to the freshwater invertebrates of New Zealand. Otago Regional Council, DunedinGoogle Scholar
  73. Murphy AE, Anderson IC, Smyth AR, Song B, Luckenbach MW (2016) Microbial nitrogen processing in hard clam (Mercenaria mercenaria) aquaculture sediments: the relative importance of denitrification and dissimilatory nitrate reduction to ammonium (DNRA). Limnol Oceanogr 61(5):1589–1604CrossRefGoogle Scholar
  74. Nielsen LP (1992) Denitrification in sediment determined from nitrogen isotope pairing. Microbiol Ecol 86:357–362CrossRefGoogle Scholar
  75. Nielsen LP, Glud RN (1996) Denitrification in a coastal sediment measured in situ by the nitrogen isotope pairing technique applied to a benthic flux chamber. Mar Ecol Prog Ser 137:181–186CrossRefGoogle Scholar
  76. Nizzoli D, Welsh D, Longhi D, Viaroli P (2014) Influence of Potamogeton pectinatus and microphytobenthos on benthic metabolism, nutrient fluxes and denitrification in a freshwater littoral sediment in an agricultural landscape: N assimilation versus N removal. Hydrobiologia 737:183–200. CrossRefGoogle Scholar
  77. Nogaro G, Burgin A (2014) Influence of bioturbation on denitrification and dissimilatory nitrate reduction to ammonium (DNRA) in freshwater sediments. Biogeochemistry 120:279–294. CrossRefGoogle Scholar
  78. O’Brien JM, Hamilton SK, Podzikowski L, Ostrom N (2012) The fate of assimilated nitrogen in streams: an in situ benthic chamber study. Freshw Biol 57:1113–1125. CrossRefGoogle Scholar
  79. Olafsson JS, Paterson DM (2004) Alteration of biogenic structure and physical properties by tube-building chironomid larvae in cohesive sediments. Aquat Ecol 38:219–229CrossRefGoogle Scholar
  80. Oldham CE, Lavery PS (1999) Porewater nutrient fluxes in a shallow fetch-limited estuary. Mar Ecol Prog Ser 183:39–47CrossRefGoogle Scholar
  81. Olsen S et al (2017) Effect of a nitrogen pulse on ecosystem N processing at different temperatures: a mesocosm experiment with 15NO3 addition. Freshw Biol 62:1232–1243. CrossRefGoogle Scholar
  82. Pelegri SP, Blackburn TH (1995) Effects of Tubifex tubifex (Oligochaeta: Tubificidae) on N-mineralization in freshwater sediments, measured with 15N isotopes. Aquat Microb Ecol 9:289–294CrossRefGoogle Scholar
  83. Pérez-Villalona H, Cornwell JC, Ortiz-Zayas JR, Cuevas E (2015) Sediment denitrification and nutrient fluxes in the San José Lagoon, a tropical lagoon in the highly urbanized San Juan Bay Estuary, Puerto Rico. Estuar Coasts 38:2259–2278. CrossRefGoogle Scholar
  84. Piña-Ochoa E, Álvarez-Cobelas M (2006) Denitrification in aquatic environments: a cross-system analysis. Biogeochemistry 81:111–130. CrossRefGoogle Scholar
  85. Poulsen M, Kofoed MVW, Larsen LH, Schramm A, Stief P (2014) Chironomus plumosus larvae increase fluxes of denitrification products and diversity of nitrate-reducing bacteria in freshwater sediment. Syst Appl Microbiol 37:51–59. CrossRefPubMedPubMedCentralGoogle Scholar
  86. Qian Q, Clarke JJ, Voller VR, Stefan HG (2009) Depth-dependant dispersion coefficient for modelling of vertical solute exchange in a lake bed under surface waves. J Hydraul Eng 135(3):187–197CrossRefGoogle Scholar
  87. Queirós AM, Stephens N, Cook R, Ravaglioli C, Nunes J, Dashfield S, Harris C, Tilstone GH, Fishwick J, Braeckman U, Somerfield PJ, Widdicome S (2015) Can benthic community structure be used to predict the process of bioturbation in real ecosystems? Prog Oceanogr 137:559–569CrossRefGoogle Scholar
  88. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  89. Risgaard-Petersen N, Skarup S, Nielsen LP (1999) Denitrification in a soft bottom lake: evaluation of laboratory incubation. Aquat Microb Ecol 17:279–287CrossRefGoogle Scholar
  90. Risgaard-Petersen N, Nielsen LP, Rysgaard S, Dalsgaard T, Meyer RL (2003) Application of the isotope pairing technique in sediments where anammox and denitrification coexist. Limnol Oceanogr Methods 1(1):63–73CrossRefGoogle Scholar
  91. Robertson, H (1999) Dynamics of wind-induced resuspension: shear stress and chlorophyll in a small, shallow lake (Tomahawk Lagoon, Dunedin). Honors Dissertation, University of Otago, New ZealandGoogle Scholar
  92. Robertson BM, Stevens L, Robertson B, Zeldis J, Green M, Madarasz-Smith A, Plew D, Storey R, Hume T, Oliver M (2016) NZ Estuary Trophic Index Screening Tool 1. Determining eutrophication susceptibility using physical and nutrient load data. Prepared for Envirolink Tools Project: Estuarine Trophic Index, MBIE/NIWA Contract No: C01X1420Google Scholar
  93. RStudio Team (2015) RStudio: integrated development for R. RStudio, Inc., Boston, MA.
  94. Salk KR, Erler DV, Eyre BD, Carlson-Perret N, Ostrom NE (2017) Unexpectedly high degree of anammox and DNRA in seagrass sediments: description and application of a revised isotope pairing technique. Geochim Cosmochim Acta 211:64–78CrossRefGoogle Scholar
  95. Saunders DL, Kalff J (2001) Denitrification rates in the sediments of Lake Memphremagog, Canada–USA. Water Res 35:1897–1904. CrossRefPubMedPubMedCentralGoogle Scholar
  96. Schallenberg M, Burns C (1997) Phytoplankton biomass and productivity in two oligotrophic lakes of short hydraulic residence time. NZ J Mar Freshw Res 31(1):119–134CrossRefGoogle Scholar
  97. Schallenberg M, Larned ST, Hayward S, Arbuckle C (2010) Contrasting effects of managed opening regimes on water quality in two intermittently closed and open coastal lakes. Estuar Coast Shelf Sci 86:587–597CrossRefGoogle Scholar
  98. Scheffer M (1998) Ecology of shallow lakes. Population and community biology series. Chapman & Hall, LondonGoogle Scholar
  99. Seitzinger S et al (2006) Denitrification across landscapes & waterscapes: a synthesis. Ecol Appl 16:2064–2090PubMedCrossRefPubMedCentralGoogle Scholar
  100. Shang J, Zhang L, Shi C, Fan C (2013) Influence of Chironomid Larvae on oxygen and nitrogen fluxes across the sediment-water interface (Lake Taihu, China). J Environ Sci 25:978–985CrossRefGoogle Scholar
  101. Smith KA, Ball T, Conen F, Dobbie KE, Massheder J, Rey A (2003) Exchange of greenhouse gases between soil and atmosphere: interactions of soil physical factors and biological processes. Eur J Soil Sci 54:779–791. CrossRefGoogle Scholar
  102. Smith RL, Böhlke JK, Repert DA, Hart CP (2009) Nitrification and denitrification in a midwestern stream containing high nitrate: in situ assessment using tracers in dome-shaped incubation chambers. Biogeochemistry 96:189–208CrossRefGoogle Scholar
  103. Steingruber SM, Friedrich J, Gachter R, Wehrli B (2001) Measurement of denitrification in sediments with the 15N isotope pairing technique. Appl Environ Microbiol 67:3771–3778. CrossRefPubMedPubMedCentralGoogle Scholar
  104. Sundback K, Miles A, Goransson E (2000) Nitrogen fluxes, denitrification and the role of microphytobenthos in microbial shallow-water sediments: an annual study. Mar Ecol Prog Ser 200:59–76CrossRefGoogle Scholar
  105. Svensson JM (1997) Influence of Chironomus plumosus larvae on ammonium flux and denitrification (measured by the acetylene-blockage and the isotope pairing-technique) in eutrophic lake sediment. Hydrobiologia 346:157–168CrossRefGoogle Scholar
  106. Svensson JM, Enrich-Prast A, Leonardson L (2001) Nitrification and denitrification in a eutrophic lake sediment bioturbated by oligochaetes. Aquat Microb Ecol 23:177–186CrossRefGoogle Scholar
  107. Thamdrup B, Dalsgaard T (2002) Production of N2 through anaerobic ammonium oxidation coupled to nitrate reduction in marine sediments. Appl Environ Microbiol 68(3):1312–1318PubMedPubMedCentralCrossRefGoogle Scholar
  108. Tolhurst TJ, Underwood AJ, Perkins RG, Chapman MG (2005) Content versus concentration: effects of units on measuring the biogeochemical properties of soft sediments. Estuar Coast Shelf Sci 63:665–673. CrossRefGoogle Scholar
  109. Tomaszek JA, Czerwieniec E (2000) In situ chamber denitrification measurements in reservoir sediments: an example from southeast Poland. Ecol Eng 16:61–71CrossRefGoogle Scholar
  110. Tomaszek JA, Czerwieniec E (2003) Dentrification and oxygen consumption in bottom sediments: factors influencing rates of the processes. Hydrobiologia 504:59–65. CrossRefGoogle Scholar
  111. Tomaszek JA, Gardner WS, Johengen TH (1997) Denitrification in sediments of a Lake Erie coastal wetland (Old Woman Creek, Huron, Ohio, USA). J Gt Lakes Res 23(4):401–415CrossRefGoogle Scholar
  112. van Regteren M, ten Boer R, Meesters EH, de Groot AV (2017) Biogeomorphic impact of oligochaetes (Annelida) on sediment properties and Salicornia spp. seedling establishment. Ecosphere 8(7):e01872. CrossRefGoogle Scholar
  113. Veraart AJ, de Klein JJM, Scheffer M (2011) Warming can boost denitrification disproportionately due to altered oxygen dynamics. PLoS ONE 6:e18508. CrossRefPubMedPubMedCentralGoogle Scholar
  114. Vopel K, Wilson PS, Zeldis J (2012) Sediment–seawater solute flux in a polluted New Zealand estuary. Mar Pollut Bull 64:2885–2891PubMedCrossRefPubMedCentralGoogle Scholar
  115. Wrede A, Beermann J, Dannheim J, Gutow L, Brey T (2018) Organism functional traits and ecosystem supporting services—a novel approach to predict bioirrigation. Ecol Ind 91:737–743CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Marine ScienceUniversity of OtagoDunedinNew Zealand
  2. 2.Bay of Plenty Regional Council Toi MoanaTaurangaNew Zealand
  3. 3.Department of ZoologyUniversity of OtagoDunedinNew Zealand
  4. 4.School of Biological Sciences and Marine Research Institute (MaRE)University of Cape TownCape TownSouth Africa
  5. 5.Department of ChemistryUniversity of OtagoDunedinNew Zealand

Personalised recommendations