Advertisement

Wetlands

pp 1–15 | Cite as

Wetland Conditions Differentially Influence Nitrogen Processing within Waterfowl Impoundments

  • Brian R. Hinckley
  • J. Randall Etheridge
  • Ariane L. PeraltaEmail author
General Wetland Science

Abstract

Manipulating hydrologic conditions at the land-water interface is critical for managing wetland functions. Hydrologic manipulation to increase retention time of water is used to promote wetland conditions, enhance nitrogen (N) processing for reduced N export, and attract migratory bird populations. Human managed wetlands such as waterfowl impoundments are intended to attract waterfowl for tourism. The limited literature has shown that waterfowl impoundments export N during seasonally prescribed drawdowns; however, it is unknown how impoundment-specific characteristics and different types of impoundments influence N cycling transformations. We compared seasonal N cycling between and within moist-soil managed (MSM) and agricultural (Ag) waterfowl impoundment soils. Potential nitrification, denitrification, and N mineralization rates and soil physicochemical properties were analyzed. Potential nitrification and denitrification rates were higher in the Ag compared to MSM impoundment even when the MSM site is actively managed to promote wetland conditions year-round. Despite the higher soil organic carbon and soil moisture content at MSM compared to Ag site, the high extractable soil ammonium, low nitrate, and low nitrification rates at MSM are evidence of substrate limitation for denitrification but not nitrification. These results indicate that decoupling of nitrification and denitrification could explain the reduced N removal capacity in these managed wetlands.

Keywords

Denitrification Hydrologic management Mineralization Nitrification 

Abbreviations

Ag

agricultural

DM

dry mass

C:N ratio

carbon to nitrogen ratio

MSM

moist-soil managed

N

nitrogen

NH4+

ammonium

NO3

nitrate

ON

organic nitrogen

SAV

submerged aquatic vegetation

Notes

Acknowledgements

We thank Holly Whitmyer, Shawn Harbin, Morgan Randolph, Gina Bledsoe, Casey Eakins, and Luise Armstrong for laboratory and field assistance. We also thank M. McCoy, M. Piehler, and anonymous reviewers for constructive feedback on earlier versions of this manuscript. We acknowledge the Soil Science Laboratory at North Carolina State University and the Environmental Research Laboratory at East Carolina University for laboratory analyses. We extend gratitude to the US Fish and Wildlife Service and a local farmer for opportunity to use land for field sampling. This work was supported by East Carolina University.

Author Contributions

BRH, JRE, and ALP conceived and designed the research; BH collected and analyzed the data; BH wrote the manuscript; all authors performed field work and edited the manuscript.

Compliance with Ethical Standards

Conflict of Interest

All authors declare they have no conflict of interest.

Supplementary material

13157_2019_1246_MOESM1_ESM.docx (284 kb)
ESM 1 (DOCX 283 kb)

References

  1. Allen M, Poggiali D, Whitaker K, Marshall TR, Kievit R (2018) Raincloud plots: a multi-platform tool for robust data visualization. doi:  https://doi.org/10.7287/peerj.preprints.27137v1
  2. Arango CP, Tank JL (2008) Land use influences the spatiotemporal controls on nitrification and denitrification in headwater streams. Journal of the North American Benthological Society 27:90–107.  https://doi.org/10.1899/07-024.1 CrossRefGoogle Scholar
  3. Arguez A, Durre I, Applequist S, Squires M, Vose R, Yin X, and Bilotta R (2010) NOAA's U.S. Climate Normals (1981-2010). 1981-2010 Climate Normals. NOAA National Centers for Environmental Information.  https://doi.org/10.7289/V5PN93JP [18 Dec. 2018]
  4. Balaine N, Clough TJ, Kelliher FM, van Koten C (2015) Soil aeration affects the degradation rate of the nitrification inhibitor dicyandiamide. Soil Research 53:137–143.  https://doi.org/10.1071/SR14162 CrossRefGoogle Scholar
  5. Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology 68:1–13.  https://doi.org/10.1111/j.1574-6941.2009.00654.x CrossRefPubMedGoogle Scholar
  6. Bonaglia S, Deutsch B, Bartoli M, Marchant HK, Brüchert V (2014) Seasonal oxygen, nitrogen and phosphorus benthic cycling along an impacted Baltic Sea estuary: regulation and spatial patterns. Biogeochemistry 119:139–160.  https://doi.org/10.1007/s10533-014-9953-6 CrossRefGoogle Scholar
  7. Booth MS, Stark JM, Rastetter E (2005) Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecological Monographs 75:139–157.  https://doi.org/10.1890/04-0988 CrossRefGoogle Scholar
  8. Borken W, Matzner E (2009) Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Global Change Biology 15:808–824.  https://doi.org/10.1111/j.1365-2486.2008.01681.x CrossRefGoogle Scholar
  9. Burger M, Jackson LE (2003) Microbial immobilization of ammonium and nitrate in relation to ammonification and nitrification rates in organic and conventional cropping systems. Soil Biology and Biochemistry 35:29–36.  https://doi.org/10.1016/S0038-0717(02)00233-X CrossRefGoogle Scholar
  10. Burgin AJ, Hamilton SK (2007) Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Frontiers in Ecology and the Environment 5:89–96.  https://doi.org/10.1890/1540-9295(2007)5[89:HWOTRO]2.0.CO;2 CrossRefGoogle Scholar
  11. Burton SAQ, Prosser JI (2001) Autotrophic ammonia oxidation at low pH through urea hydrolysis. Applied and Environmental Microbiology 67:2952–2957.  https://doi.org/10.1128/AEM.67.7.2952-2957.2001 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Castaldelli G, Colombani N, Vincenzi F, Mastrocicco M (2013) Linking dissolved organic carbon, acetate and denitrification in agricultural soils. Environmental Earth Sciences 68:939–945.  https://doi.org/10.1007/s12665-012-1796-7 CrossRefGoogle Scholar
  13. Damashek J, Francis CA (2018) Microbial nitrogen cycling in estuaries: from genes to ecosystem processes. Estuaries and Coasts 41:626–660.  https://doi.org/10.1007/s12237-017-0306-2 CrossRefGoogle Scholar
  14. Danczak RE, Sawyer AH, Williams KH, Stegen JC, Hobson C, Wilkins MJ (2016) Seasonal hyporheic dynamics control coupled microbiology and geochemistry in Colorado River sediments. Journal of Geophysical Research: Biogeosciences 121:2976–2987.  https://doi.org/10.1002/2016JG003527 CrossRefGoogle Scholar
  15. Drinkwater LE, Cambardella CA, Reeder JD, Rice CW (1996) Potentially mineralizable nitrogen as an indicator of biologically active soil nitrogen. Methods for Assessing Soil Quality 217–229. doi:  https://doi.org/10.2136/sssaspecpub49.c13 Google Scholar
  16. Edmisten K, Collins G, Crozier C, York A, Hardy D, Reisig D, Bullen G et al (2018) Cotton information. NC State Extension Publications. https://content.ces.ncsu.edu/cotton-information
  17. Eickenscheidt T, Heinichen J, Augustin J, Freibauer A, Drösler M (2014) Nitrogen mineralization and gaseous nitrogen losses from waterlogged and drained organic soils in a black alder (Alnus glutinosa (L.) Gaertn.) forest. Biogeosciences 11:2961–2976.  https://doi.org/10.5194/bg-11-2961-2014 CrossRefGoogle Scholar
  18. Fang Y, Singh BP, Badgery W, He X (2016) In situ assessment of new carbon and nitrogen assimilation and allocation in contrastingly managed dryland wheat crop–soil systems. Agriculture, Ecosystems & Environment 235:80–90.  https://doi.org/10.1016/j.agee.2016.10.010 CrossRefGoogle Scholar
  19. Fleming KS, Kaminski RM, Tietjen TE, Schummer ML, Ervin GN, Nelms KD (2012) Vegetative forage quality and moist-soil management on wetlands reserve program lands in Mississippi. Wetlands 32:919–929.  https://doi.org/10.1007/s13157-012-0325-5 CrossRefGoogle Scholar
  20. Foulquier A, Volat B, Neyra M, Bornette G, Montuelle B (2013) Long-term impact of hydrological regime on structure and functions of microbial communities in riverine wetland sediments. FEMS Microbiology Ecology 85:211–226.  https://doi.org/10.1111/1574-6941.12112 CrossRefPubMedGoogle Scholar
  21. Fraterrigo JM, Balser TC, Turner MG (2006) Microbial community variation and its relationship with nitrogen mineralization in historically altered forests. Ecology 87:570–579.  https://doi.org/10.1890/05-0638 CrossRefPubMedGoogle Scholar
  22. Garcia-Ruiz R, Pattinson SN, Whitton BA (1998) Denitrification in river sediments: relationship between process rate and properties of water and sediment. Freshwater Biology 39:467–476CrossRefGoogle Scholar
  23. Gray MJ, Hagy HM, Nyman JA, Stafford JD (2013) Management of wetlands for wildlife. In: Anderson JT, Davis CA (eds) Wetland Techniques: Volume 3: Applications and management. Springer Netherlands, Dordrecht, pp 121–180Google Scholar
  24. Groffman PM, Altabet MA, Böhlke J, 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. Ecological Applications 16:2091–2122CrossRefGoogle Scholar
  25. Hawkes CV, Keitt TH (2015) Resilience vs. historical contingency in microbial responses to environmental change. Ecology Letters 18:612–625.  https://doi.org/10.1111/ele.12451 CrossRefPubMedGoogle Scholar
  26. Heiniger R, Spears J, Bowman D, Carson ML, Crozier C, Dunphy J, Koenning S et al (2018) Corn production guide. NC State Extension Publications. https://content.ces.ncsu.edu/corn-production-guide
  27. Hinckley BR, Etheridge JR, Peralta AL (In revision) Storm event nitrogen dynamics in waterfowl impoundmentsGoogle Scholar
  28. Hope, RM (2013) Rmisc: Ryan Miscellaneous. https://cran.r-project.org/web/packages/Rmisc/index.html
  29. Jayakumar A, O’Mullan GD, Naqvi SWA, Ward BB (2009) Denitrifying bacterial community composition changes associated with stages of denitrification in oxygen minimum zones. Microbial Ecology 58:350–362.  https://doi.org/10.1007/s00248-009-9487-y CrossRefPubMedGoogle Scholar
  30. Jickells T, Baker AR, Cape JN, Cornell SE, Nemitz E (2013) The cycling of organic nitrogen through the atmosphere. Philosophical Transactions of the Royal Society B: Biological Sciences 368:20130115.  https://doi.org/10.1098/rstb.2013.0115 CrossRefGoogle Scholar
  31. Kandeler E (1996) Potential nitrification. Methods in soil biology. F. Schinner, R. Öhlinger, E. Kandeler, and R. Margesin (editors). Springer, Berlin, Germay, pp 146–148Google Scholar
  32. Kemp MJ, Dodds WK (2002) Comparisons of nitrification and denitrification in prairie and agriculturally influenced streams. Ecological Applications 12:998–1009.  https://doi.org/10.1890/1051-0761(2002)012[0998:CONADI]2.0.CO;2 CrossRefGoogle Scholar
  33. Kessler AJ, Glud RN, Cardenas MB, Cook PLM (2013) Transport zonation limits coupled nitrification-denitrification in permeable sediments. Environmental Science & Technology 47:13404–13411.  https://doi.org/10.1021/es403318x CrossRefGoogle Scholar
  34. Kim D-J, Lee D-I, Keller J (2006) Effect of temperature and free ammonia on nitrification and nitrite accumulation in landfill leachate and analysis of its nitrifying bacterial community by FISH. Bioresource Technology 97:459–468.  https://doi.org/10.1016/j.biortech.2005.03.032 CrossRefPubMedGoogle Scholar
  35. Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest Package. Tests in Linear Mixed Effects Models. Journal of Statistical Software 82(13):1–26.  https://doi.org/10.18637/jss.v082.i13
  36. Lenth RV (2016) Least-Squares Means: The R Package lsmeans. Journal of Statistical Software 69(1):1–33Google Scholar
  37. Marchant HK, Holtappels M, Lavik G, Ahmerkamp S, Winter C, Kuypers MMM (2016) Coupled nitrification–denitrification leads to extensive N loss in subtidal permeable sediments. Limnology and Oceanography 61:1033–1048.  https://doi.org/10.1002/lno.10271 CrossRefGoogle Scholar
  38. Maricle BR, Lee RW (2002) Aerenchyma development and oxygen transport in the estuarine cordgrasses Spartina alterniflora and S. anglica. Aquatic Botany 74:109–120.  https://doi.org/10.1016/S0304-3770(02)00051-7 CrossRefGoogle Scholar
  39. Maul JD, Cooper CM (2000) Water quality of seasonally flooded agricultural fields in Mississippi, USA. Agriculture, Ecosystems & Environment 81:171–178.  https://doi.org/10.1016/S0167-8809(00)00157-2 CrossRefGoogle Scholar
  40. Mazerolle MJ (2017) Package ‘AICcmodavg’. Model selection and multimodel inference based on (Q)AIC(c). R packageGoogle Scholar
  41. Menning DM, Carraher-Stross WA, Graham ED, Thomas DN, Phillips AR, Scharping RJ, Garey JR (2018) Aquifer discharge drives microbial community change in karst estuaries. Estuaries and Coasts 41:430–443.  https://doi.org/10.1007/s12237-017-0281-7 CrossRefGoogle Scholar
  42. Moorman MC, Augspurger T, Stanton JD, Smith A (2017) Where’s the grass? Disappearing submerged aquatic vegetation and declining water quality in Lake Mattamuskeet. Journal of Fish and Wildlife Management 8:401–417.  https://doi.org/10.3996/082016-JFWM-068 CrossRefGoogle Scholar
  43. Nelms K, Ballinger B, Boyles A (2007) Wetland Management For Waterfowl Handbook. 136Google Scholar
  44. Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environmental Microbiology 10:2966–2978.  https://doi.org/10.1111/j.1462-2920.2008.01701.x CrossRefPubMedGoogle Scholar
  45. Oosterkamp MJ, Boeren S, Plugge CM, Schaap PJ, Stams AJM (2013) Metabolic response of Alicycliphilus denitrificans strain BC toward electron acceptor variation. PROTEOMICS 13:2886–2894.  https://doi.org/10.1002/pmic.201200571 CrossRefPubMedGoogle Scholar
  46. Pansu M, Thuriès L (2003) Kinetics of C and N mineralization, N immobilization and N volatilization of organic inputs in soil. Soil Biology and Biochemistry 35:37–48.  https://doi.org/10.1016/S0038-0717(02)00234-1 CrossRefGoogle Scholar
  47. Peralta AL, Johnston ER, Matthews JW, Kent AD (2016) Abiotic correlates of microbial community structure and nitrogen cycling functions vary within wetlands. Freshwater Science 35:573–588.  https://doi.org/10.1086/685688 CrossRefGoogle Scholar
  48. Peralta AL, Ludmer S, Kent AD (2013) Hydrologic history influences microbial community composition and nitrogen cycling under experimental drying/wetting treatments. Soil Biology and Biochemistry 66:29–37.  https://doi.org/10.1016/j.soilbio.2013.06.019 CrossRefGoogle Scholar
  49. Peralta AL, Matthews JW, Kent AD (2010) Microbial community structure and denitrification in a wetland mitigation bank. Applied and Environmental Microbiology 76:4207–4215.  https://doi.org/10.1128/AEM.02977-09 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Post DM, Taylor JP, Kitchell JF, Olson MH, Schindler DE, Herwig BR (1998) The role of migratory waterfowl as nutrient vectors in a managed wetland. Conservation Biology 12:910–920.  https://doi.org/10.1111/j.1523-1739.1998.97112.x CrossRefGoogle Scholar
  51. Prosser JI (2007) Chapter 15 - the ecology of nitrifying bacteria. In: Bothe H, Ferguson SJ, Newton WE (eds) Biology of the nitrogen cycle. Elsevier, Amsterdam, pp 223–243CrossRefGoogle Scholar
  52. Racchetti E, Bartoli M, Soana E, Longhi D, Christian RR, Pinardi M, Viaroli P (2011) Influence of hydrological connectivity of riverine wetlands on nitrogen removal via denitrification. Biogeochemistry 103:335–354.  https://doi.org/10.1007/s10533-010-9477-7 CrossRefGoogle Scholar
  53. Racchetti E, Longhi D, Ribaudo C, Soana E, Bartoli M (2017) Nitrogen uptake and coupled nitrification–denitrification in riverine sediments with benthic microalgae and rooted macrophytes. Aquatic Sciences 79:487–505.  https://doi.org/10.1007/s00027-016-0512-1 CrossRefGoogle Scholar
  54. R Core Team. (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  55. Robertson GP, Sollins P, Ellis BG, Lajtha K (1999) Exchangeable ions, pH, and cation exchange capacity. Standard Soil Methods for Long-Term Ecological Research. Oxford University Press, New York, pp 106–114Google Scholar
  56. Sahrawat KL (2008) Factors affecting nitrification in soils. Communications in Soil Science and Plant Analysis 39:1436–1446.  https://doi.org/10.1080/00103620802004235 CrossRefGoogle Scholar
  57. Schuerings J, Jentsch A, Hammerl V, Lenz K, Henry HAL, Malyshev AV, Kreyling J (2014) Increased winter soil temperature variability enhances nitrogen cycling and soil biotic activity in temperate heathland and grassland mesocosms. Biogeosciences 11:7051–7060.  https://doi.org/10.5194/bg-11-7051-2014 CrossRefGoogle Scholar
  58. Seago JL, Marsh LC, Stevens KJ, Soukup A, Votrubova O, Enstone DE (2005) A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma. Annals of Botany 96:565–579.  https://doi.org/10.1093/aob/mci211 CrossRefPubMedGoogle Scholar
  59. Seo DC, DeLaune RD (2010) Fungal and bacterial mediated denitrification in wetlands: influence of sediment redox condition. Water Research 44:2441–2450.  https://doi.org/10.1016/j.watres.2010.01.006 CrossRefPubMedGoogle Scholar
  60. Shang F, Ren S, Yang P, Li C, Ma N (2015) Effects of different fertilizer and irrigation water types, and dissolved organic matter on soil C and N mineralization in crop rotation farmland. Water, Air, & Soil Pollution 226:396–325.  https://doi.org/10.1007/s11270-015-2667-0 CrossRefGoogle Scholar
  61. Smith EL, Kellman LM (2011) Nitrate loading and isotopic signatures in subsurface agricultural drainage systems. Journal of Environmental Quality 40:1257–1265.  https://doi.org/10.2134/jeq2010.0489 CrossRefPubMedGoogle Scholar
  62. Sporer AJ, Kahl LJ, Price-Whelan A, Dietrich LEP (2017) Redox-based regulation of bacterial development and behavior. Annual Review of Biochemistry 86:777–797.  https://doi.org/10.1146/annurev-biochem-061516-044453 CrossRefPubMedGoogle Scholar
  63. Stark JM, Hart SC (1997) High rates of nitrification and nitrate turnover in undisturbed coniferous forests. Nature 385:61.  https://doi.org/10.1038/385061a0 CrossRefGoogle Scholar
  64. Subbarao GV, Ito O, Sahrawat KL, Berry WL, Nakahara K, Ishikawa T, Watanabe T, Suenaga K, Rondon M, Rao IM (2006) Scope and strategies for regulation of nitrification in agricultural systems—challenges and opportunities. Critical Reviews in Plant Sciences 25:303–335.  https://doi.org/10.1080/07352680600794232 CrossRefGoogle Scholar
  65. Tiedje JM, Simkins S, Groffman PM (1989) Perspectives on measurement of denitrification in the field including recommended protocols for acetylene-based methods. Plant and Soil 115:261–284.  https://doi.org/10.1007/BF02202594 CrossRefGoogle Scholar
  66. Toma Y, Hatano R (2007) Effect of crop residue C:N ratio on N2O emissions from Gray lowland soil in Mikasa, Hokkaido, Japan. Soil Science and Plant Nutrition 53:198–205.  https://doi.org/10.1111/j.1747-0765.2007.00125.x CrossRefGoogle Scholar
  67. Turner RE, Rabalais NN (2003) Linking landscape and water quality in the Mississippi River basin for 200 years. BioScience 53:563–572.  https://doi.org/10.1641/0006-3568(2003)053[0563:LLAWQI]2.0.CO;2 CrossRefGoogle Scholar
  68. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecological Applications 7:737–750.  https://doi.org/10.1890/1051-0761(1997)007[0737:HAOTGN]2.0.CO;2 CrossRefGoogle Scholar
  69. Waters MN, Piehler MF, Rodriguez AB, Smoak JM, Bianchi TS (2009) Shallow lake trophic status linked to late Holocene climate and human impacts. Journal of Paleolimnology 42:51–64.  https://doi.org/10.1007/s10933-008-9247-x CrossRefGoogle Scholar
  70. Waters MN, Piehler MF, Smoak JM, Martens CS (2010) The development and persistence of alternative ecosystem states in a large, shallow lake. Freshwater Biology 55:1249–1261.  https://doi.org/10.1111/j.1365-2427.2009.02349.x CrossRefGoogle Scholar
  71. Weedon JT, Aerts R, Kowalchuk GA, van Logtestijn R, Andringa D, van Bodegom PM (2013) Temperature sensitivity of peatland C and N cycling: does substrate supply play a role? Soil Biology and Biochemistry 61:109–120.  https://doi.org/10.1016/j.soilbio.2013.02.019 CrossRefGoogle Scholar
  72. Winton RS, Richardson CJ (2017) Top-down control of methane emission and nitrogen cycling by waterfowl. Ecology 98:265–277.  https://doi.org/10.1002/ecy.1640 CrossRefPubMedGoogle Scholar
  73. Wolf KL, Ahn C, Noe GB (2011) Microtopography enhances nitrogen cycling and removal in created mitigation wetlands. Ecological Engineering 37:1398–1406.  https://doi.org/10.1016/j.ecoleng.2011.03.013 CrossRefGoogle Scholar
  74. Wolf KL, Noe GB, Ahn C (2013) Hydrologic connectivity to streams increases nitrogen and phosphorus inputs and cycling in soils of created and natural floodplain wetlands. Journal of Environmental Quality 42:1245–1255.  https://doi.org/10.2134/jeq2012.0466 CrossRefPubMedGoogle Scholar
  75. Woli KP, David MB, Cooke RA, McIsaac GF, Mitchell CA (2010) Nitrogen balance in and export from agricultural fields associated with controlled drainage systems and denitrifying bioreactors. Ecological Engineering 36:1558–1566.  https://doi.org/10.1016/j.ecoleng.2010.04.024 CrossRefGoogle Scholar
  76. Xiang S-R, Doyle A, Holden PA, Schimel JP (2008) Drying and rewetting effects on C and N mineralization and microbial activity in surface and subsurface California grassland soils. Soil Biology and Biochemistry 40:2281–2289.  https://doi.org/10.1016/j.soilbio.2008.05.004 CrossRefGoogle Scholar
  77. Yao H, Campbell CD, Chapman SJ, Freitag TE, Nicol GW, Singh BK (2013) Multi-factorial drivers of ammonia oxidizer communities: evidence from a national soil survey. Environmental Microbiology 15:2545–2556.  https://doi.org/10.1111/1462-2920.12141 CrossRefPubMedGoogle Scholar
  78. Yao H, Gao Y, Nicol GW, Campbell CD, Prosser JI, Zhang L, Han W, Singh BK (2011) Links between Ammonia oxidizer community structure, abundance, and nitrification potential in acidic soils. Applied and Environmental Microbiology 77:4618–4625.  https://doi.org/10.1128/AEM.00136-11 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Zhang J, Cai Z, Müller C (2018) Terrestrial N cycling associated with climate and plant-specific N preferences: a review. European Journal of Soil Science 69:488–501.  https://doi.org/10.1111/ejss.12533 CrossRefGoogle Scholar
  80. Zhao W, Cai Z, Xu Z (2007) Does ammonium-based N addition influence nitrification and acidification in humid subtropical soils of China? Plant and Soil 297:213–221.  https://doi.org/10.1007/s11104-007-9334-1 CrossRefGoogle Scholar
  81. Zhao W, Zhang J, Müller C, Cai Z (2018) Effects of pH and mineralisation on nitrification in a subtropical acid forest soil. Soil Research 56:275–283.  https://doi.org/10.1071/SR17087 CrossRefGoogle Scholar

Copyright information

© Society of Wetland Scientists 2019

Authors and Affiliations

  1. 1.S301B Howell Science Complex, Department of BiologyEast Carolina UniversityGreenvilleUSA
  2. 2.Department of Marine, Earth, and Atmospheric SciencesNorth Carolina State UniversityRaleighUSA
  3. 3.RW-214 Rivers, Department of EngineeringCenter for Sustainable Energy and Environmental EngineeringGreenvilleUSA

Personalised recommendations