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Biogeochemistry

, Volume 145, Issue 3, pp 315–335 | Cite as

Source of organic detritus and bivalve biomass influences nitrogen cycling and extracellular enzyme activity in estuary sediments

  • Josie CrawshawEmail author
  • Theresa O’Meara
  • Candida Savage
  • Blair Thomson
  • Federico Baltar
  • Simon F. Thrush
Article

Abstract

In aquatic ecosystems, natural processes that remove nitrogen from the biologically available pool (e.g. denitrification) have been intensively studied as an ecosystem function that reduces eutrophication. The quantity of sediment organic matter is a key driver of denitrification with percent organic content positively related to rates of nitrogen removal; however, few studies have investigated the influence of the quality of organic matter on nitrogen cycling in estuarine sediments despite shifts in primary producers with eutrophication. This laboratory study using intact benthic communities investigates the influence of various organic detritus sources, which vary in their C:N ratio, on nitrogen gas (N2) and solute fluxes and extracellular enzyme activity in estuarine sediments. A custom-built tank with a removable front plate was used with a planar optode film to image sediment oxygenation. Mangrove leaf detritus significantly increased the net N2 production in sediments, while the deposition of other detrital sources and control sediments produced net N2 consumption. Sulfatase activity was significantly reduced in the mangrove leaves and seagrass treatments, suggesting alteration of heterotrophic microbial activity with reducing oxygen conditions. Leucine aminopeptidase activity, indicating nitrogen cycling, was reduced in all treatments, suggesting the organic detritus provided a nitrogen supplement or reduced the activity of extracellular enzymes producing microbes. Bivalve biomass increased net nitrogen gas fluxes in some treatments. Our results indicate different detrital sources may have varying impacts on the removal of bioavailable nitrogen through denitrification and show that feedbacks in biogeochemical cycles may occur with changes in organic detrital source pools.

Keywords

Denitrification Nitrogen fixation Organic detritus Extracellular enzyme activity Bioturbation Bivalve Planar optode Sediment 

Notes

Acknowledgements

The authors would like to thank K. Pearson and E. Murray for technical assistance through the duration of this experiment. We thank N. McHugh for analysing the dissolved nutrient samples. J. Crawshaw was supported by a PhD Scholarship from the University of Otago. This research was funded by the New Zealand Sustainable Seas National Science Challenge (Estuary Tipping Points 4.2.1). We thank the editor and three anonymous reviewers for very helpful comments that improved the manuscript.

Supplementary material

10533_2019_608_MOESM1_ESM.docx (248 kb)
Supplementary material 1 (DOCX 247 kb)
10533_2019_608_MOESM2_ESM.eps (35 kb)
Supplementary material 2 (EPS 34 kb)
10533_2019_608_MOESM3_ESM.eps (13 kb)
Supplementary material 3 (EPS 12 kb)

References

  1. 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 67:1171–1178CrossRefGoogle Scholar
  2. Babbin AR, Keil RG, Devol AH, Ward BB (2014) Organic matter stoichiometry, flux, and oxygen control nitrogen loss in the ocean. Science 344:406–408CrossRefGoogle Scholar
  3. Babbin AR, Jayakumar A, Ward BB (2016) Organic matter loading modifies the microbial community responsible for nitrogen loss in estuarine sediments. Microb Ecol 71:555–565CrossRefGoogle Scholar
  4. Baltar F, Morán XAG, Lønborg C (2017) Warming and organic matter sources impact the proportion of dissolved to total activities in marine extracellular enzymatic rates. Biogeochemistry 133:307–316.  https://doi.org/10.1007/s10533-017-0334-9 CrossRefGoogle Scholar
  5. Barnes J, Upstill-Goddard RC (2011) N2O seasonal distributions and air-sea exchange in UK estuaries: implications for the tropospheric N2O source from European coastal waters. J Geophys Res 116:G01006.  https://doi.org/10.1029/2009JG001156 CrossRefGoogle Scholar
  6. Batchelor B, Lawrence AW (1978) Autotrophic denitrification using elemental sulfur. Journal (Water Pollution Control Federation) 50:1986–2001Google Scholar
  7. Bell CW, Fricks BE, Rocca JD, Steinweg JM, McMahon SK, Wallenstein MD (2013) High-throughput fluorometric measurement of potential soil extracellular enzyme activities. J Vis Exp e50961:1–16.  https://doi.org/10.3791/50961 CrossRefGoogle Scholar
  8. Belley R, Snelgrove PVR, Archambault P, Juniper SK (2016) Environmental drivers of benthic flux variation and ecosystem functioning in Salish Sea and northeast Pacific sediments. PLoS ONE 11:e0151110CrossRefGoogle Scholar
  9. Boynton WR, Kemp WM (1985) Nutrient regeneration and oxygen consumption by sediments along an estuarine salinity gradient. Mar Ecol Prog Ser 23:45–55CrossRefGoogle Scholar
  10. Brito A, Newton A, Tett P, Fernandes TF (2009) Development of an optimal methodology for the extraction of microphytobenthic chlorophyll. J Int Environ Appl Sci 4:42–54Google Scholar
  11. Burgin AJ, Hamilton SK (2007) Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Front Ecol Environ 5:89–96CrossRefGoogle Scholar
  12. Burkhardt BG, Watkins-Brandt KS, Defforey D, Paytan A, White AE (2014) Remineralization of phytoplankton-derived organic matter by natural populations of heterotrophic bacteria. Mar Chem 163:1–9.  https://doi.org/10.1016/j.marchem.2014.03.007 CrossRefGoogle Scholar
  13. Bushaw KL et al (1996) Photochemical release of biologically available nitrogen from aquatic dissolved organic matter. Nature 381:404.  https://doi.org/10.1038/381404a0 CrossRefGoogle Scholar
  14. Caffrey JM, Sloth NP, Kaspar HF, Blackburn TH (1993) Effect of organic loading on nitrification and denitrification in a marine sediment microcosm. FEMS Microbiol Ecol 12:159–167CrossRefGoogle Scholar
  15. Caffrey JM, Hollibaugh JT, Mortazavi B (2016) Living oysters and their shells as sites of nitrification and denitrification. Mar Pollut Bull 112:86–90.  https://doi.org/10.1016/j.marpolbul.2016.08.038 CrossRefGoogle Scholar
  16. Cebron A, Berthe T, Garnier J (2003) Nitrification and nitrifying bacteria in the lower Seine River and Estuary (France). Appl Environ Microbiol 69:7091–7100CrossRefGoogle Scholar
  17. Chang BX et al (2014) The effect of organic carbon on fixed nitrogen loss in the eastern tropical South Pacific and Arabian Sea oxygen deficient zones. Limnol Oceanogr 59:1267–1274CrossRefGoogle Scholar
  18. Cloern JE (2001) Our evolving conceptual model of the coastal eutrophication problem. Mar Ecol Prog Ser 210:223–253CrossRefGoogle Scholar
  19. Corbett DR (2010) Resuspension and estuarine nutrient cycling: insights from the Neuse River Estuary. Biogeosciences 7:3289–3300CrossRefGoogle Scholar
  20. Crawshaw JA, Schallenberg M, Savage C (2018) 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(1):33–59.  https://doi.org/10.1080/00288330.2018.1476388 CrossRefGoogle Scholar
  21. Damashek J, Francis CA (2018) Microbial nitrogen cycling in estuaries: from genes to ecosystem processes. Estuaries Coasts 41:626–660.  https://doi.org/10.1007/s12237-017-0306-2 CrossRefGoogle Scholar
  22. Devol AH (2015) Denitrification, anammox, and N2 production in marine sediments. Annu Rev Mar Sci 7:403–423CrossRefGoogle Scholar
  23. Diaz F, Raimbault P, Boudjellal B, Garcia N, Moutin T (2001) Early spring phosphorus limitation of primary productivity in a NW Mediterranean coastal zone (Gulf of Lions). Mar Ecol Prog Ser 211:51–62CrossRefGoogle Scholar
  24. Douglas EJ, Pilditch CA, Kraan C, Schipper LA, Lohrer AM, Thrush SF (2017) Macrofaunal functional diversity provides resilience to nutrient enrichment in coastal sediments. Ecosystems 20:1324–1336CrossRefGoogle Scholar
  25. Duarte B, Reboreda R, Caçador I (2008) Seasonal variation of extracellular enzymatic activity (EEA) and its influence on metal speciation in a polluted salt marsh. Chemosphere 73:1056–1063.  https://doi.org/10.1016/j.chemosphere.2008.07.072 CrossRefGoogle Scholar
  26. Dunn C, Jones TG, Girard A, Freeman C (2014) Methodologies for extracellular enzyme assays from wetland soils. Wetlands 34:9–17.  https://doi.org/10.1007/s13157-013-0475-0 CrossRefGoogle Scholar
  27. Erler DV, Welsh DT, Bennet WW, Meziane T, Hubas C, Nizzoli D, Ferguson AJP (2017) The impact of suspended oyster farming on nitrogen cycling and nitrous oxide production in a sub-tropical Australian estuary. Estuar Coast Shelf Sci 192:117–127.  https://doi.org/10.1016/j.ecss.2017.05.007 CrossRefGoogle Scholar
  28. Eyre B, Rysgaard S, Dalsgaard T, Christensen P (2002) Comparison of isotope pairing and N2: Ar methods for measuring sediment denitrification—assumptions, modifications, and implications. Estuaries 25:1077–1087.  https://doi.org/10.1007/BF02692205 CrossRefGoogle Scholar
  29. Eyre BD, Ferguson AJP, Webb A, Maher D, Oakes JM (2011) Denitrification, N-fixation and nitrogen and phosphorus fluxes in different benthic habitats and their contribution to the nitrogen and phosphorus budgets of a shallow oligotrophic sub-tropical coastal system (southern Moreton Bay, Australia). Biogeochemistry 102:111–133.  https://doi.org/10.1007/s10533-010-9425-6 CrossRefGoogle Scholar
  30. Eyre BD, Maher DT, Squire P (2013) Quantity and quality of organic matter (detritus) drives N2 effluxes (net denitrification) across seasons, benthic habitats, and estuaries. Global Biogeochem Cycles 27:1083–1095.  https://doi.org/10.1002/2013GB004631 CrossRefGoogle Scholar
  31. Fernandes SO, Michotey VD, Guasco S, Bonin PC, Loka Bharathi PA (2012) Denitrification prevails over anammox in tropical mangrove sediments (Goa, India). Mar Environ Res 74:9–19.  https://doi.org/10.1016/j.marenvres.2011.11.008 CrossRefGoogle Scholar
  32. Fernandes SO, Dutta P, Gonsalves M-J, Bonin PC, Loka Bharathi PA (2016) Denitrification activity in mangrove sediments varies with associated vegetation. Ecol Eng 95:671–681.  https://doi.org/10.1016/j.ecoleng.2016.06.102 CrossRefGoogle Scholar
  33. Fulweiler RW, Nixon SW, Buckley BA, Granger SL (2007) Reversal of the net dinitrogen gas flux in coastal marine sediments. Nature 448:180–182. http://www.nature.com/nature/journal/v448/n7150/suppinfo/nature05963_S1.html
  34. 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.  https://doi.org/10.1007/s10021-008-9187-3 CrossRefGoogle Scholar
  35. Fulweiler RW, Brown SM, Nixon SW, Jenkins BD (2013) Evidence and a conceptual model for the co-occurrence of nitrogen fixation and denitrification in heterotrophic marine sediments. Mar Ecol Prog Ser 482:57–68CrossRefGoogle Scholar
  36. Galloway JN et al (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226.  https://doi.org/10.1007/s10533-004-0370-0 CrossRefGoogle Scholar
  37. Gardner WS, McCarthy MJ, An S, Sobolev D, Sell KS, Brock D (2006) Nitrogen fixation and dissimilatory nitrate reduction to ammonium (DNRA) support nitrogen dynamics in Texas estuaries. Limnol Oceanogr 51:558–568.  https://doi.org/10.4319/lo.2006.51.1_part_2.0558 CrossRefGoogle Scholar
  38. Ghosh S, Leff LG (2013) Impacts of labile organic carbon concentration on organic and inorganic nitrogen utilization by a stream biofilm bacterial community. Appl Environ Microbiol 79:7130–7141CrossRefGoogle Scholar
  39. 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
  40. Gladstone-Gallagher RV, Lundquist CJ, Pilditch CA (2014) Mangrove (Avicennia marina subsp. australasica) litter production and decomposition in a temperate estuary. NZ J Mar Freshw Res 48:24–37.  https://doi.org/10.1080/00288330.2013.827124 CrossRefGoogle Scholar
  41. 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
  42. Hannides AK, Glazer BT, Sansone FJ (2014) Extraction and quantification of microphytobenthic Chl a within calcareous reef sands. Limnol Oceanogr 12:126–138CrossRefGoogle Scholar
  43. 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.  https://doi.org/10.5194/bg-10-5571-2013 CrossRefGoogle Scholar
  44. 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.  https://doi.org/10.1016/j.gca.2015.04.049 CrossRefGoogle Scholar
  45. Hashimoto S, Furukawa K, Shioyama M (1987) Autotrophic denitrification using elemental sulfur. J Ferment Technol 65:683–692.  https://doi.org/10.1016/0385-6380(87)90011-2 CrossRefGoogle Scholar
  46. Hendrickson J, Trahan N, Gordon E, Ouyang Y (2007) Estimating relevance of organic carbon, nitrogen, and phosphorus loads to a blackwater river estuary. JAWRA J Am Water Resour Assoc 43:264–279.  https://doi.org/10.1111/j.1752-1688.2007.00021.x CrossRefGoogle Scholar
  47. Her J-J, Huang J-S (1995) Influences of carbon source and C/N ratio on nitrate/nitrite denitrification and carbon breakthrough. Biores Technol 54:45–51.  https://doi.org/10.1016/0960-8524(95)00113-1 CrossRefGoogle Scholar
  48. Herbert RA (1999) Nitrogen cycling in coastal marine ecosystems. FEMS Microbiol Rev 23:563–590CrossRefGoogle Scholar
  49. Hill AR, Cardaci M (2004) Denitrification and organic carbon availability in riparian wetland soils and subsurface sediments. Soil Sci Soc Am J 68:320–325CrossRefGoogle Scholar
  50. Hill BH, Elonen CM, Anderson LE, Lehrter JC (2014) Microbial respiration and ecoenzyme activity in sediments from the Gulf of Mexico hypoxic zone. Aquat Microb Ecol 72:105–116CrossRefGoogle Scholar
  51. Hiroki M, Nohara S, Hanabishi K, Utagawa H, Yabe T, Satake K (2007) Enzymatic evaluation of decomposition in mosaic landscapes of a tidal flat ecosystem. Wetlands 27:399–405CrossRefGoogle Scholar
  52. Hoppe HG (1983) Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Mar Ecol Prog Ser 11:299–308CrossRefGoogle Scholar
  53. Houlbrooke DJ, Horne DJ, Hedley MJ, Hanly JA, Snow VO (2004) A review of literature on the land treatment of farm-dairy effluent in New Zealand and its impact on water quality. N Z J Agric Res 47:499–511CrossRefGoogle Scholar
  54. Howarth RW (1988) Nutrient limitation of net primary production in marine ecosystems. Annu Rev Ecol Syst 19:89–110CrossRefGoogle Scholar
  55. Huettel M, Rusch A (2000) Transport and degradation of phytoplankton in permeable sediment. Limnol Oceanogr 45:534–549.  https://doi.org/10.4319/lo.2000.45.3.0534 CrossRefGoogle Scholar
  56. Jackson CR, Tyler HL, Millar JJ (2013) Determination of microbial extracellular enzyme activity in waters, soils, and sediments using high throughput microplate assays. J Vis Exp.  https://doi.org/10.3791/50399 CrossRefGoogle Scholar
  57. Janssen F, Huettel M, Witte U (2005) Pore-water advection and solute fluxes in permeable marine sediments (II): benthic respiration at three sandy sites with different permeabilities (German Bight, North Sea). Limnol Oceanogr 50:779–792CrossRefGoogle Scholar
  58. Jäntti H, Leskinen E, Stange CF, Hietanen S (2012) Measuring nitrification in sediments—comparison of two techniques and three 15NO measurement methods. Isot Environ Health Stud 48:313–326.  https://doi.org/10.1080/10256016.2012.641543 CrossRefGoogle Scholar
  59. Jones HFE, Pilditch CA, Hamilton DP, Bryan KR (2017) Impacts of a bivalve mass mortality event on an estuarine food web and bivalve grazing pressure. NZ J Mar Freshw Res 51:370–392.  https://doi.org/10.1080/00288330.2016.1245200 CrossRefGoogle Scholar
  60. 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.  https://doi.org/10.1021/ac00095a009 CrossRefGoogle Scholar
  61. Keller AA, Riebesell U (1989) Phytoplankton carbon dynamics during a winter-spring diatom bloom in an enclosed marine ecosystem: primary production, biomass and loss rates. Mar Biol 103:131–142.  https://doi.org/10.1007/BF00391071 CrossRefGoogle Scholar
  62. Kelly S (2009) Whangateau catchment and harbour study: Review of marine environment information. Prepared for Auckland Regional Council. Auckland Regional Council Technical Report 2009/003. Auckland, New ZealandGoogle Scholar
  63. Kessler AJ, Cardenas MB, Santos IR, Cook PLM (2014) Enhancement of denitrification in permeable carbonate sediment due to intra-granular porosity: a multi-scale modelling analysis. Geochim Cosmochim Acta 141:440–453.  https://doi.org/10.1016/j.gca.2014.06.028 CrossRefGoogle Scholar
  64. Knapp AN (2012) The sensitivity of marine N2 fixation to dissolved inorganic nitrogen. Front Microbiol 3:374.  https://doi.org/10.3389/fmicb.2012.00374 CrossRefGoogle Scholar
  65. Le Guitton M, Soetaert K, Damsté JSS, Middelburg JJ (2015) Biogeochemical consequences of vertical and lateral transport of particulate organic matter in the southern North Sea: a multiproxy approach. Estuar Coast Shelf Sci 165:117–127.  https://doi.org/10.1016/j.ecss.2015.09.010 CrossRefGoogle Scholar
  66. Leynaert A, Longphuirt SN, Claquin P, Chauvaud L, Ragueneau O (2009) No limit? The multiphasic uptake of silicic acid by benthic diatoms. Limnol Oceanogr 54:571–576.  https://doi.org/10.4319/lo.2009.54.2.0571 CrossRefGoogle Scholar
  67. Livingstone MW, Smith RV, Laughlin RJ (2000) A spatial study of denitrification potential of sediments in Belfast and Strangford Loughs and its significance. Sci Total Environ 251–252:369–380.  https://doi.org/10.1016/S0048-9697(00)00417-4 CrossRefGoogle Scholar
  68. Lorenzen CJ (1967) Determination of chlorophyll and pheopigments: spectrophotometric equations. Limnol Oceanogr 12:343–346CrossRefGoogle Scholar
  69. Marks BM, Chambers L, White JR (2016) Effect of fluctuating salinity on potential denitrification in coastal wetland soil and sediments. Soil Sci Soc Am J 80:516–526.  https://doi.org/10.2136/sssaj2015.07.0265 CrossRefGoogle Scholar
  70. McDowell RW, Wilcock RJ (2008) Water quality and the effects of different pastoral animals. N Z Vet J 56:289–296.  https://doi.org/10.1080/00480169.2008.36849 CrossRefGoogle Scholar
  71. Middelboel M, Borch NH, Kirchman DL (1995) Bacterial utilization of dissolved free amino acids, dissolved combined amino acids and ammonium in the Delaware Bay estuary: effects of carbon and nitrogen limitation. Mar Ecol Prog Ser 128:109–120CrossRefGoogle Scholar
  72. Miskell B (2009) Whangateau catchment and harbour study: Review of environmental and socio-economic information. Prepared by Boffa Miskell Limited for Auckland Regional Council. Auckland Regional Council Technical Report 2009/004. Auckland, New ZealandGoogle 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 61:1589–1604.  https://doi.org/10.1002/lno.10305 CrossRefGoogle Scholar
  74. Newcomer TA, Kaushal SS, Mayer PM, Shields AR, Canuel EA, Groffman PM, Gold AJ (2012) Influence of natural and novel organic carbon sources on denitrification in forest, degraded urban, and restored streams. Ecol Monogr 82:449–466CrossRefGoogle Scholar
  75. Newell SE, McCarthy MJ, Gardner WS, Fulweiler RW (2016a) Sediment nitrogen fixation: a call for re-evaluating coastal N budgets. Estuar Coasts 39:1626–1638.  https://doi.org/10.1007/s12237-016-0116-y CrossRefGoogle Scholar
  76. Newell SE, Pritchard KR, Foster SQ, Fulweiler RW (2016b) Molecular evidence for sediment nitrogen fixation in a temperate New England estuary. PeerJ.  https://doi.org/10.7717/peerj.1615 CrossRefGoogle Scholar
  77. Nordhaus I, Salewski T, Jennerjahn TC (2011) Food preferences of mangrove crabs related to leaf nitrogen compounds in the Segara Anakan Lagoon, Java, Indonesia. J Sea Res 65:414–426.  https://doi.org/10.1016/j.seares.2011.03.006 CrossRefGoogle Scholar
  78. Nordhaus I, Salewski T, Jennerjahn TC (2017) Interspecific variations in mangrove leaf litter decomposition are related to labile nitrogenous compounds. Estuar Coast Shelf Sci 192:137–148.  https://doi.org/10.1016/j.ecss.2017.04.029 CrossRefGoogle Scholar
  79. O’Meara T, Thompson SP, Piehler MF (2015) Effects of shoreline hardening on nitrogen processing in estuarine marshes of the U.S. mid-Atlantic coast. Wetl Ecol Manag 23:385–394.  https://doi.org/10.1007/s11273-014-9388-9 CrossRefGoogle Scholar
  80. Park S (2011) Sea lettuce and nutrient monitoring in Tauranga Harbour 1991-2010. Bay of Plenty Regional Council Environmental Publication 2011/06. Whakatane, New ZealandGoogle Scholar
  81. Parsons TR, Maita Y, Lalli CM (1984) Fluorometric determination of phaeo-pigments. A manual of chemical and biological methods for seawater analysis. Pergamon Press, Amsterdam, pp 109–110CrossRefGoogle Scholar
  82. Piña-Ochoa E, Álvarez-Cobelas M (2006) Denitrification in aquatic environments: a cross-system analysis. Biogeochemistry 81:111–130.  https://doi.org/10.1007/s10533-006-9033-7 CrossRefGoogle Scholar
  83. Precht E, Huettel M (2004) Rapid wave-driven advective pore water exchange in a permeable coastal sediment. J Sea Res 51:93–107CrossRefGoogle Scholar
  84. R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
  85. Rao AMF, Charette MA (2011) Benthic nitrogen fixation in an eutrophic estuary affected by groundwater discharge. J Coast Res.  https://doi.org/10.2112/JCOASTRES-D-11-00057.1 CrossRefGoogle Scholar
  86. Riekenberg PM, Oakes JM, Eyre BD (2017) Uptake of dissolved organic and inorganic nitrogen in microalgae-dominated sediment: comparing dark and light in situ and ex situ additions of 15N. Mar Ecol Prog Ser 571:29–42CrossRefGoogle Scholar
  87. R Studio Team (2015) RStudio: Integrated Development for R. RStudio, Inc., Boston, MA. http://www.rstudio.com/
  88. Schallenberg M, Burns CW (1997) Phytoplankton biomass and productivity in two oligotrophic lakes of short hydraulic residence time. NZ J Mar Freshw Res 31:119–134.  https://doi.org/10.1080/00288330.1997.9516749 CrossRefGoogle Scholar
  89. Schallenberg M, Crawshaw JA (2016) In-lake nutrient processing in Te Waihora/Lake Ellesmere. Prepared for Environment Canterbury and Whakaora Te Waihora. University of Otago, DunedinGoogle Scholar
  90. Schmidt CA, Clark MW (2013) Deciphering and modeling the physicochemical drivers of denitrification rates in bioreactors. Ecol Eng 60:276–288.  https://doi.org/10.1016/j.ecoleng.2013.07.041 CrossRefGoogle Scholar
  91. 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 87:99–111.  https://doi.org/10.1007/s10533-007-9171-6 CrossRefGoogle Scholar
  92. Seitzinger S et al (2006) Denitrification across landscapes & waterscapes: a synthesis. Ecol Appl 16:2064–2090CrossRefGoogle Scholar
  93. Smyth AR, Geraldi NR, Piehler MF (2013) Oyster-mediated benthic-pelagic coupling modifies nitrogen pools and processes. Mar Ecol Prog Ser 493:23–30CrossRefGoogle Scholar
  94. Stelzer RS, Scott JT, Bartsch LA, Parr TB (2014) Particulate organic matter quality influences nitrate retention and denitrification in stream sediments: evidence from a carbon burial experiment. Biogeochemistry 119:387–402CrossRefGoogle Scholar
  95. Steppe TF, Paerl H (2002) Potential N2 fixation by sulfate-reducing bacteria in a marine intertidal microbial mat. Aquat Microb Ecol 28:1–12.  https://doi.org/10.3354/ame028001 CrossRefGoogle Scholar
  96. Stief P (2013) Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications. Biogeosciences 10:7829–7846CrossRefGoogle Scholar
  97. Stief P, Poulsen M, Nielsen LP, Brix H, Schramm A (2009) Nitrous oxide emissions by aquatic macrofauna. PNAS 106:4296–4300CrossRefGoogle Scholar
  98. Svenningsen NB, Heisterkamp IM, Sigby-Clausen M, Larsen LH, Nielsen LP, Stief P, Schramm A (2012) Shell biofilm nitrification and gut denitrification contribute to emission of nitrous oxide by the invasive freshwater mussel Dreissena polymorpha (zebra mussel). Appl Environ Microbiol 78:4505–4509CrossRefGoogle Scholar
  99. Teixeira C, Magalhães C, Boaventura RAR, Bordalo AA (2010) Potential rates and environmental controls of denitrification and nitrous oxide production in a temperate urbanized estuary. Mar Environ Res 70:336–342.  https://doi.org/10.1016/j.marenvres.2010.07.001 CrossRefGoogle Scholar
  100. Tiedje JM (1988) Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In: Zehnder A (ed) Biology of anaerobic microorganisms. Wiley, New York, pp 179–243Google Scholar
  101. Turek KA, Hoellein TJ (2015) The invasive Asian clam (Corbicula fluminea) increases sediment denitrification and ammonium flux in 2 streams in the midwestern USA. Freshw Sci 34:472–484.  https://doi.org/10.1086/680400 CrossRefGoogle Scholar
  102. Volkenborn N et al (2012) Intermittent bioirrigation and oxygen dynamics in permeable sediments: an experimental and modeling study of three tellinid bivalves. J Mar Res 70:794–823CrossRefGoogle Scholar
  103. Welsh DT, Bourgues S, Wit Rd, Herbert RA (1996) Seasonal variation in rates of heterotrophic nitrogen fixation (acetylene reduction) in Zostera noltii meadows and uncolonised sediments of the Bassin d’Arcachon, south-west France. Hydrobiologia 329:161–174CrossRefGoogle Scholar
  104. Welsh DT, Nizzoli D, Fano EA, Viaroli P (2015) Direct contribution of clams (Ruditapes philippinarum) to benthic fluxes, nitrification, denitrification and nitrous oxide emission in a farmed sediment. Estuar Coast Shelf Sci 154:84–93.  https://doi.org/10.1016/j.ecss.2014.12.021 CrossRefGoogle Scholar
  105. Woodin SA, Volkenborn N, Pilditch CA, Lohrer AM, Wethey DS, Hewitt JE, Thrush SF (2016) Same pattern, different mechanism: locking onto the role of key species in seafloor ecosystem process. Sci Rep 6:26678.  https://doi.org/10.1038/srep26678 CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Department of Marine ScienceUniversity of OtagoDunedinNew Zealand
  2. 2.Bay of Plenty Regional Council Toi MoanaWhakataneNew Zealand
  3. 3.Institute of Marine ScienceUniversity of AucklandAucklandNew Zealand
  4. 4.Smithsonian Environmental Research Centre (SERC)EdgewaterUSA
  5. 5.School of Biological Sciences and Marine Research Institute (MaRE)University of Cape TownCape TownSouth Africa
  6. 6.Department of Limnology and Bio-OceanographyUniversity of ViennaViennaAustria

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