Wetlands Ecology and Management

, Volume 26, Issue 3, pp 425–439 | Cite as

Microbial ecoenzyme stoichiometry, nutrient limitation, and organic matter decomposition in wetlands of the conterminous United States

  • Brian H. HillEmail author
  • Colleen M. Elonen
  • Alan T. Herlihy
  • Terri M. Jicha
  • Gregg Serenbetz
Original Paper


Microbial respiration (Rm) and ecoenzyme activities (EEA) related to microbial carbon, nitrogen, and phosphorus acquisition were measured in 792 freshwater and estuarine wetlands (representing a cumulative area of 217,480 km2) across the continental United States as part of the US EPA’s 2011 National Wetland Condition Assessment. EEA stoichiometry was used to construct models for and assess nutrient limitation, carbon use efficiency (CUE), and organic matter decomposition (− k). The wetlands were classified into ten groups based on aggregated ecoregion and wetland type. The wetlands were also assigned to least, intermediate, and most disturbed classes, based on the extent of human influences. Ecoenzyme activity related to C, N and P acquisition, Rm, CUE, and − k differed among ecoregion–wetland types and, with the exception of C acquisition and − k, among disturbance classes. Rm and EEA were positively correlated with soil C, N and P content (r = 0.15–0.64) and stoichiometry (r = 0.15–0.48), and negatively correlated with an index of carbon quality (r = − 0.22 to − 0.39). EEA stoichiometry revealed that wetlands were more often P- than N-limited, and that P-limitation increases with increasing disturbance. Our enzyme-based approach for modeling C, N, and P acquisition, and organic matter decomposition, all rooted in stoichiometric theory, provides a mechanism for modeling resource limitations of microbial metabolism and biogeochemical cycling in wetlands. Given the ease of collecting and analyzing soil EEA and their response to wetland disturbance gradients, enzyme stoichiometry models are a cost-effective tool for monitoring ecosystem responses to resource availability and the environmental drivers of microbial metabolism, including those related to global climate changes.


Climate Decomposition Ecoenzymes Respiration Soil Stoichiometry Wetlands 



The data from the 2011 NWCA used in this paper resulted from the collective efforts of dedicated field crews, laboratory staff, data management and quality control staff, analysts and many others from EPA, states, tribes, federal agencies, universities and other organizations. For questions about these data, please contact This work was partially supported by Grant #RD-83425201 from the National Center for Environmental Research (NCER) STAR Program of the US Environmental Protection Agency to ATH. ATH was also supported on this project via an intergovernmental personnel agreement with the US EPA Office of Water. The authors thank Dr. Anett Trebitz for her comments on an earlier draft of this paper. The views expressed in this paper are those of the authors and do not necessarily reflect the views or policies of the US Environmental Protection Agency. Mention of trade names or commercial products do not constitute endorsement or recommendation for use.

Supplementary material

11273_2017_9584_MOESM1_ESM.pdf (61 kb)
Supplementary material 1 (PDF 61 kb)


  1. Alvarez S, Guerrero MC (2000) Enzymatic activities associated with decomposition of particulate organic matter in two shallow ponds. Soil Biol Biochem 32:1941–1951CrossRefGoogle Scholar
  2. Bedford BL, Walbridge MR, Aldous A (1999) Patterns of nutrient availability and plant diversity of temperate North American wetlands. Ecology 80:2151–2169CrossRefGoogle Scholar
  3. Bridgham SD, Megonigal JP, Keller JK, Bliss NB, Trettin C (2006) The carbon balance of North American wetlands. Wetlands 26:889–916CrossRefGoogle Scholar
  4. Brinson MM, Lugo AE, Brown S (1981) Primary productivity, decomposition and consumer activity in freshwater wetlands. Ann Rev Ecol Syst 12:123–161CrossRefGoogle Scholar
  5. Broberg A (1985) A modified method for studies of electron transport system activity in freshwater sediments. Hydrobiologia 120:181–187CrossRefGoogle Scholar
  6. Cleveland CC, Liptzin D (2007) C/N/P stoichiometry in soil: is there a “redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252CrossRefGoogle Scholar
  7. Dahl TE (2011) Status and trends of wetlands in the conterminous United States 2004–2009. US Department of the Interior; Fish and Wildlife Service, Washington, DCGoogle Scholar
  8. Dahl TE, Bergeson MT (2009) Technical procedures for conducting status and trends of the Nation’s wetlands. US Fish and Wildlife Service, Division of Habitat and Resource Conservation, Washington, DCGoogle Scholar
  9. Foreman CM, Franchini P, Sinsabaugh RL (1998) The trophic dynamics of riverine bacterioplankton, relationships among substrate availability, ectoenzyme kinetics and growth. Limnol Oceanogr 43:1344–1352CrossRefGoogle Scholar
  10. 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 43:1387–1397CrossRefGoogle Scholar
  11. Gorham E (1991) Northern peatlands, role in the carbon cycle and probable responses to climate warming. Ecol Appl 1:182–195CrossRefPubMedGoogle Scholar
  12. Herlihy AT, Kentula ME, Magee TK, Lomnicky GA, Nahlik AM, Serenbetz G (2008) Striving for consistency in the National wetland condition assessment: developing a reference condition approach for assessing wetlands at a continental scale. Environ Monit Assess 27:860–877Google Scholar
  13. Hill BH, Elonen CM, Jicha TM, Cotter AM, Trebitz AS, Danz NP (2006) Sediment microbial enzyme activity as an indicator of nutrient limitation in Great Lakes coastal wetlands. Freshw Biol 51:1670–1683CrossRefGoogle Scholar
  14. Hill BH, Elonen CM, Jicha TM, Kolka RK, Lehto LLP, Sebestyen SD, Seifert-Monson LR (2014) Ecoenzymatic stoichiometry and microbial processing of organic matter in northern bogs and fens reveals a common P-limitation between peatlands. Biogeochemistry 120:203–224CrossRefGoogle Scholar
  15. Jackson CR, Foreman CM, Sinsabaugh RL (1995) Microbial activities as indicators or organic matter processing rates in a Lake Erie coastal wetland. Freshw Biol 34:329–342CrossRefGoogle Scholar
  16. Kayranli B, Scholz M, Mustafa A, Hedmark A (2010) Carbon storage and fluxes within freshwater wetlands: a critical review. Wetlands 30:111–124CrossRefGoogle Scholar
  17. Keiblinger KM, Hall EK, Wanek W, Szukics U, Hammerle I, Ellerdorfer G, Bock S, Straus J, Sterflinger K, Richter A, Zechmeister-Boltenstern S (2010) The effect of resource quantity and resource stoichiometry on microbial carbon-use-efficiency FEMS. Microb Ecol 73:430–440Google Scholar
  18. Lachat Instruments (2009) Methods list for automated ion analyzers: flow injection, ion chromatography. Lachat Instruments, Loveland, p 40pGoogle Scholar
  19. Manzoni S, Taylor P, Richter A, Porporato A, Agren GI (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91CrossRefPubMedGoogle Scholar
  20. Mitra S, Wassmann R, Vlek PLG (2005) An appraisal of global wetland area and its organic carbon stock. Curr Sci 88:25–35Google Scholar
  21. Mitsch WJ, Bernal B, Nahlik AM, Mander U, Zhang L, Anderson CJ, Jorgensen SE, Brix H (2013) Wetlands, carbon, and climate change. Landsc Ecol 28:583–597CrossRefGoogle Scholar
  22. Moorhead DL, Lashermes G, Sinsabaugh RL (2012) A theoretical model of C- and N-acquiring exoenzyme activities, which balances microbial demands during decomposition. Soil Biol Biochem 53:133–141CrossRefGoogle Scholar
  23. Nahlik AM, Fennessy MS (2016) Carbon storage in US wetlands. Nat Commun 7:13835CrossRefPubMedPubMedCentralGoogle Scholar
  24. Olsen AR, Kincaid TM, Kentula ME, Weber MH. Survey design to assess condition of wetlands in the United States. Environ Monit Assess (in press)Google Scholar
  25. Rejmankova E, Houdkova K (2006) Wetland plant decomposition under different nutrient conditions: what is more important, litter quality or site quality? Biogeochemistry 80:245–262CrossRefGoogle Scholar
  26. Schimel JP, Weintraub MN (2003) The implications or exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem 35:549–563CrossRefGoogle Scholar
  27. Sinsabaugh RL, Follstad Shah JJ (2011) Ecoenzymatic stoichiometry of recalcitrant organic matter decomposition: the growth rate hypothesis in reverse. Biogeochemistry 102:31–43CrossRefGoogle Scholar
  28. Sinsabaugh RL, Foreman CM (2001) Activity profiles of bacterioplankton in a eutrophic river. Freshw Biol 46:1239–1249CrossRefGoogle Scholar
  29. Sinsabaugh RL, Moorhead DL (1994) Resource allocation to extracellular enzyme production: a model for nitrogen and phosphorus control of litter decomposition. Soil Biol Biochem 26:1305–1311CrossRefGoogle Scholar
  30. Sinsabaugh RL, Findlay S, Franchini P, Fisher D (1997) Enzymatic analysis of riverine bacterioplankton production. Limnol Oceanogr 42:29–38CrossRefGoogle Scholar
  31. Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial nutrient acquisition in soil and sediment. Nature 462:795–798CrossRefPubMedGoogle Scholar
  32. Sinsabaugh RL, Follstad Shah JJ, Hill BH, Elonen CM (2012) Ecoenzymatic stoichiometry of stream sediments with comparison to terrestrial soils. Biogeochemistry 111:455–467CrossRefGoogle Scholar
  33. Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modeling. Ecol Lett 16:930–939CrossRefPubMedGoogle Scholar
  34. Stevens DL, Olsen AR (2004) Spatially-balanced sampling of natural resources. J Am Stat Assoc 99:262–278CrossRefGoogle Scholar
  35. USEPA (2011) National wetland condition assessment: field operations manual. EPA-843-R-10-001. US Environmental Protection Agency, Washington, DCGoogle Scholar
  36. USEPA (2016) National wetland condition assessment: 2011 technical report. EPA-843-R-15-006. US Environmental Protection Agency, Washington, DCGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature (outside the USA) 2017

Authors and Affiliations

  • Brian H. Hill
    • 1
    Email author
  • Colleen M. Elonen
    • 1
  • Alan T. Herlihy
    • 2
  • Terri M. Jicha
    • 1
  • Gregg Serenbetz
    • 3
  1. 1.Office of Research and Development, National Health and Environmental Effects Research Laboratory, Mid-Continent Ecology DivisionUS Environmental Protection AgencyDuluthUSA
  2. 2.Department of Fisheries and WildlifeOregon State UniversityCorvallisUSA
  3. 3.Office of Water, Office of Wetlands, Oceans and WatershedsUS Environmental Protection AgencyWashingtonUSA

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