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Effects of flood inundation, invasion by Phalaris arundinacea, and nitrogen enrichment on extracellular enzyme activity in an Upper Mississippi River floodplain forest

  • Nathan R. De JagerEmail author
  • Whitney Swanson
  • Daniel L. Hernández
  • Julia Reich
  • Richard Erickson
  • Eric A. Strauss
Short Communication

Abstract

The community structures and ecosystem functions of floodplains are primarily driven by variation in flood inundation. However, global changes, such as invasive species and nutrient enrichment, may alter the effects of flooding in these systems. We added nitrogen (N) to correspond with twice the annual atmospheric deposition rate of the south-west Wisconsin, USA region within mature floodplain forest plots and patches of an invasive grass (reed canarygrass, Phalaris arundinacea) along a floodplain elevation gradient in an Upper Mississippi River floodplain forest. We measured soil physicochemical properties and the activity of six extracellular enzymes during 3 months that varied in flooding conditions. Multivariate analyses (distance-based redundancy analysis) revealed that floodplain elevation, month of sampling, and vegetation type were all significant predictors of variation in soil physicochemical properties, while elevation and month were significant predictors of multivariate extracellular enzyme activity (EEA). The best model for predicting EEA consisted of nitrogen availability, soil porosity, and water filled pore space. Although the categorical fertilization and invasion treatments were not significant predictors of EEA, our results suggest that their effects depend on the degree to which they modify N availability and soil moisture. In this system, spatial and temporal patterns in flooding appear to be the main driver of these properties, but N enrichment and invasion may have the potential to further modify them.

Keywords

Extracellular enzyme activity Fertilization Flood pulse Invasion Nitrogen 

Notes

Acknowledgements

Funding for this research was provided by the U.S. Army Corps of Engineer’s Upper Mississippi River Restoration Program and through a cooperative agreement between the U.S. Geological Survey Upper Midwest Environmental Sciences Center and the University of Wisconsin La Crosse River Studies Center. Rebecca M. Kreiling and two anonymous reviewers provided comments that greatly improved an earlier version of this manuscript. Any use of trade names of products does not imply endorsement by the United States Government.

Supplementary material

11273_2018_9651_MOESM1_ESM.docx (36 kb)
Supplementary material 1 (DOCX 35 kb)

References

  1. Aber JD (1992) Nitrogen cycling and nitrogen saturation in temperate forest ecosystems. Trends Ecol Evol 7(7):220–224CrossRefGoogle Scholar
  2. Allison SD (2005) Cheaters, diffusion and nutrients constrain decomposition by microbial enzymes in spatially structured environments: constraints on enzymatic decomposition. Ecol Lett 8(6):626–635CrossRefGoogle Scholar
  3. Allison SD, Vitousek PM (2005) Responses of extracellular enzymes to simple and complex nutrient inputs. Soil Biol Biochem 37(5):937–944.  https://doi.org/10.1016/j.soilbio.2004.09.014 CrossRefGoogle Scholar
  4. Alster CJ, GermanDP LuY, Allison SD (2013) Microbial enzymatic responses to drought and to nitrogen addition in a southern California grassland. Soil Biol Biochem 64:68–79CrossRefGoogle Scholar
  5. Amador JA, Glucksman AM, Lyons JB, Görres JH (1997) Spatial distribution of soil phosphatase activity within a riparian forest. Soil Sci 162(11):808–825CrossRefGoogle Scholar
  6. Baron JS, Hall EK, Nolan BT, Finlay JC, Bernhardt ES, Harrison JA, Chan F, Boyer EW (2013) The interactive effects of excess reactive nitrogen and climate change on aquatic ecosystems and water resources of the United States. Biogeochemistry 114:71–92CrossRefGoogle Scholar
  7. Batten KM, Scow KM, Espeland EK (2008) Soil microbial community associated with an invasive grass differentially impacts native plant performance. Microb Ecol 55(2):220–228CrossRefGoogle Scholar
  8. Bayley PB (1995) Understanding large river: floodplain ecosystems. Bioscience 45:153–158CrossRefGoogle Scholar
  9. Bormann FH, Likens H (1979) Pattern and process in a forested ecosystem: disturbance and the steady state based on the Hubbard Brook Ecosystem Study. Springer, New YorkCrossRefGoogle Scholar
  10. Burns A, Ryder DS (2001) Response of bacterial extracellular enzymes to inundation of floodplain sediments. Freshw Biol 46(10):1299–1307CrossRefGoogle Scholar
  11. De Jager NR, Thomsen MT, Yin Y (2012) Threshold effects of flood duration on the vegetation and soils of the Upper Mississippi River floodplain, USA. For Ecol Manage 270:135–146CrossRefGoogle Scholar
  12. De Jager NR, Cogger BJ, Thomsen MA (2013) Interactive effects of flooding and deer (Odocoileus virginianus) browsing on floodplain forest recruitment. For Ecol Manage 303:11–19CrossRefGoogle Scholar
  13. De Jager NR, Swanson W, Strauss EA, Thomsen M, Yin Y (2015) Flood pulse effects on nitrification in a floodplain forest impacted by herbivory, invasion, and restoration. Wetl Ecol Manag 23:1067–1081CrossRefGoogle Scholar
  14. De Kroon H, Bobbink R (1997) Clonal plant dominance under elevated nitrogen deposition, with special reference to Brachy-podium pinnatum in chalk grassland. In: de Kroon H, van Groenendael J (eds) The ecology and evolution of clonal plants. Backhuys, Leiden, pp 359–379Google Scholar
  15. Dijkstra FA, Hobbie SE, Knops JMH, Reich PB (2004) Nitrogen deposition and plant species interact to influence soil carbon stabilization. Ecol Lett 7(12):1192–1198.  https://doi.org/10.1111/j.1461-0248.2004.00679.x CrossRefGoogle Scholar
  16. Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6(6):503–523CrossRefGoogle Scholar
  17. Esch EH, Hernández DL, Pasari JR, Kantor RSG, Selmants PC (2013) Response of soil microbial activity to grazing, nitrogen deposition, and exotic cover in a serpentine grassland. Plant Soil 366(1–2):671–682CrossRefGoogle Scholar
  18. Forshay KJ, Stanley EH (2005) Rapid nitrate loss and denitrification in a temperate river floodplain. Biogeochemistry 75(1):43–64CrossRefGoogle Scholar
  19. Galatowitsch S, Whited DC, Lehtinen R, Husveth J, Schik K (2000) The vegetation of wet meadows in relation to their land-use. Environ Monit Assess 60(2):121–144CrossRefGoogle Scholar
  20. Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby BJ (2003) The nitrogen cascade. Bioscience 53(4):341CrossRefGoogle Scholar
  21. German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD (2011) Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem 43(7):1387–1397CrossRefGoogle Scholar
  22. Gilliam FS (2006) Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. J Ecol 94(6):1176–1191CrossRefGoogle Scholar
  23. Gotelli NJ, Ellison AM (2013) A primer of ecological statistics, 2nd edn. Sinauer Associates Inc, SunderlandGoogle Scholar
  24. Green EK, Galatowitsch SM (2002) Effects of Phalaris arundinacea and nitrate-N addition on the establishment of wetland plant communities. J Appl Ecol 39:134–144CrossRefGoogle Scholar
  25. Groffman P (1994) Denitrification in freshwater wetlands. Curr Topics Wetl Biogeochem 1:15–35Google Scholar
  26. Groffman et al (1992) Nitrate dynamics in riparian forests: microbial studies. J Environ Qual 21:666–671CrossRefGoogle Scholar
  27. Gutknecht JLM, Henry HAL, Balser TC (2010) Inter-annual variation in soil extra-cellular enzyme activity in response to simulated global change and fire disturbance. Pedobiologia 53(5):283–293CrossRefGoogle Scholar
  28. Hernández DL, Hobbie SE (2010) The effects of substrate composition, quantity, and diversity on microbial activity. Plant Soil 335(1–2):397–411CrossRefGoogle Scholar
  29. Junk WJ, Bayley PB, Sparks RE (1989) The flood pulse concept in river-floodplain systems. Can Spec Publ Fish Aquat Sci 106(1):110–127Google Scholar
  30. Kang H, Freeman C, Lock MA (1998) Trace gas emission from a Welsh fen-role of hydrochemistry and soil enzyme activities. Water Air Soil Pollut 105:107–116CrossRefGoogle Scholar
  31. Kao-Kniffin J, Balser TC (2010) Soil microbial composition and nitrogen cycling in a disturbed wet prairie restoration (Wisconsin). Ecol Restor 28(1):20–22CrossRefGoogle Scholar
  32. Keeler BL, Hobbie SE, Kellogg LE (2009) Effects of long-term nitrogen addition on microbial enzyme activity in eight forested and grassland sites: implications for litter and soil organic matter decomposition. Ecosystems 12(1):1–15CrossRefGoogle Scholar
  33. Koch AL (1985) The macroeconomics of bacterial growth. In: Fletcher M, Floodgate GD (eds) Bacteria in their natural environments. Academic Press, London, pp 1–42Google Scholar
  34. Koschorreck M, Darwich A (2003) Nitrogen dynamics in seasonally flooded soils in the Amazon floodplain. Wetl Ecol Manag 11(5):317–330CrossRefGoogle Scholar
  35. Kourtev PS, Ehrenfeld JG, Häggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83(11):3152–3166CrossRefGoogle Scholar
  36. Kourtev PS, Ehrenfeld JG, Haggblom M (2003) Experimental analysis of the effect of exotic and native plant species on the structure and function of soil microbial communities. Soil Biol Biochem 35(7):895–905CrossRefGoogle Scholar
  37. Kreiling RM, De Jager NR, Swanson W, Strauss EA, Thomsen M (2015) Effects of flooding on ion exchange rates in an Upper Mississippi River floodplain forest impacted by herbivory, invasion, and restoration. Wetlands 35(5):1005–1012CrossRefGoogle Scholar
  38. Lavergne S, Molofsky J (2004) Reed canary grass (Phalaris arundinacea) as a biological model in the study of plant invasions. Crit Rev Plant Sci 23(5):415–429CrossRefGoogle Scholar
  39. Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multi-factorial ecological experiments. Ecol Monogr 69:1–24CrossRefGoogle Scholar
  40. Matson P, Lohse KA, Hall SJ (2002) The globalization of nitrogen deposition: consequences for terrestrial ecosystems. Ambio 31(2):113–119CrossRefGoogle Scholar
  41. McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297CrossRefGoogle Scholar
  42. McLatchey GP, Reddy KR (1998) Regulation of organic matter decomposition and nutrient release in a wetland soil. J Environ Qual 27:1268–1274CrossRefGoogle Scholar
  43. National Atmospheric Deposition Program (2013). http://nadp.sws.uiuc.edu/data/sites/siteDetails.aspx?net=NTN&id=WI98. Accessed 1 June 2017
  44. Noe GB, Hupp CR, Rybicki NB (2013) Hydrogeomorphology influences soil nitrogen and phosphorus mineralization in floodplain wetlands. Ecosystems 16(1):75–94CrossRefGoogle Scholar
  45. Peralta AL, Ludmer S, Matthews JW, Kent AD (2014) Bacterial community response to changes in soil redox potential along a moisture gradient in restored wetlands. Ecol Eng 73:246–253CrossRefGoogle Scholar
  46. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org
  47. Rabalais NN, Turner ER (2001) Coastal hypoxia: consequences for living resources and ecosystems. American Geophysical Union, Washington, DCCrossRefGoogle Scholar
  48. Robertson G, Coleman D, Bledsoe C, Sollins P (1999) Standard soil methods for long-term ecological research. Oxford University Press, OxfordGoogle Scholar
  49. Romano SP (2010) Our current understanding of the Upper Mississippi River System floodplain forest. Hydrobiologia 640(1):115–124CrossRefGoogle Scholar
  50. Souza-Alonzo P, Novoa A, Gonzalez L (2014) Soil biochemical alterations and microbial community responses under Acacia dealbata invasion. Soil Biol Biochem 79:100–108CrossRefGoogle Scholar
  51. Stursova M, Crenshaw CL, Sinsabaugh RL (2006) Microbial responses to long-term N deposition in a semiarid grassland. Microb Ecol 51(1):90–98CrossRefGoogle Scholar
  52. Swanson W, De Jager NR, Strauss EA, Thomsen MT (2017) Effects of flooding and invasion by Phalaris arundinacea on nitrogen cycling in an Upper Mississippi River floodplain forest. Ecohydrology. 10:e1877CrossRefGoogle Scholar
  53. Thomsen M, Brownell K, Groshek M, Kirsch E (2012) Control of reed canarygrass promotes wetland herb and tree seedling establishment in an Upper Mississippi River Floodplain forest. Wetlands 32(3):543–555CrossRefGoogle Scholar
  54. Turner MM, Henry HAL (2010) Net nitrogen mineralization and leaching in response to warming and nitrogen deposition in a temperate old field: the importance of winter temperature. Oecologia 162(1):227–236CrossRefGoogle Scholar
  55. Vankoughnett MR, Henry HAL (2013) Combined effects of soil freezing and N addition on losses and interception of N over winter and summer. Ecosystems 16(4):694–703CrossRefGoogle Scholar
  56. Vitousek PM, Aber J, Howarth RW, Likens GE, Matson PA, Schindler D, WTilman GD (1997) Human alteration of the global nitrogen cycle: causes and consequences. Ecological Society of America, Washington, DCGoogle Scholar
  57. Werner KJ, Zedler JB (2002) How sedge meadow soils, microtopography, and vegetation respond to sedimentation. Wetlands 22(3):451–466CrossRefGoogle Scholar
  58. Wilson JS, Baldwin DS, Rees GN, Wilson BP (2010) The effects of short-term inundation on carbon dynamics, microbial community structure and microbial activity in floodplain soil. River Res Appl 27(11):213–225Google Scholar
  59. Woo I, Zedler JB (2002) Can nutrients alone shift a sedge meadow towards dominance by the invasive Typha × glauca. Wetlands 22(3):509–521CrossRefGoogle Scholar
  60. Yesmin L, Gammack SM, Cresser MS (1996) Effects of atmospheric nitrogen deposition on ericoid mycorrhizal infection of Calluna vulgaris growing in peat soils. App Soil Ecol 4(1):49–60CrossRefGoogle Scholar
  61. Zeglin LH, Stursova M, Sinsabaugh RL, Collins SL (2007) Microbial responses to nitrogen addition in three contrasting grassland ecosystems. Oecologia 154(2):349–359CrossRefGoogle Scholar

Copyright information

© This is a U.S. Government work and not under copyright protection in the US; foreign copyright protection may apply 2019

Authors and Affiliations

  1. 1.U.S. Geological Survey Upper Midwest Environmental Sciences CenterLa CrosseUSA
  2. 2.University of Wisconsin-La CrosseLa CrosseUSA
  3. 3.Carleton CollegeNorthfieldUSA

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