Abstract
Ombrotrophic bogs are nutrient-poor systems and important carbon (C) sinks yet there remains a dearth of information on the belowground stoichiometry of C, nitrogen (N), phosphorus (P), and potassium (K), important determinants of substrate quality for microorganisms, in these systems. In this study, we quantified the C, N, P, and K concentrations of both hummock peat and dissolved matter as well as microbial extracellular enzyme activity from 0 to 10 cm depth in the long-term NPK fertilization plots at Mer Bleue bog. Greater N-loading resulted in significantly reduced C:N and greater C:P and C:K (p < 0.05) while the addition of NPK resulted in significantly lower C:P and C:K (p < 0.05) and lower C:N relative to N-only treatments but the difference in C:N was not significant (p > 0.05). Hydrolase enzyme activity followed resource allocation models with significantly suppressed N-acetyl-β-d-glucosaminidase and phosphatase activity (p < 0.05) and enhanced β-d-glucosidase activity with greater N- and P-availability. The concentration of inhibitory phenolics was significantly greater with N-loading (p < 0.05), due in part to shifts in surface vegetation, while phenol oxidase activity was significantly suppressed by N (p < 0.05) with results suggesting greater suppression by NH4 + than NO3 −. Taken together, these results suggest that higher levels of nutrients impact both microbial substrate quality as well as the activity of microbial enzymes that are key to the decomposition process that may ultimately decrease carbon sequestration in bogs.
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References
Aerts R, Wallen B, Malmer N (1992) Growth-limiting nutrients in Sphagnum-dominated bogs subject to low and high atmospheric nitrogen supply. J Ecol 80:131–140
Aldous AR (2002) Nitrogen translocation in Sphagnum mosses: effects of atmospheric nitrogen deposition. New Phytol 156(2):241–253
Basiliko N, Moore TR, Jeannotte R, Bubier JL (2006) Nutrient input and carbon and microbial dynamics in an ombrotrophic bog. Geomicrobiol J 23(7):531–543
Berendse F, Van Breemen N, Rydin H, Buttler A, Heijmans M, Hoosbeek MR, Lee JA, Mitchell E, Saarinen T, Vasander H, Wallen B (2001) Raised atmospheric CO2 levels and increased N deposition cause shifts in plant species composition and production in Sphagnum bogs. Glob Change Biol 7(5):591–598
Bobbink R, Hornung M, Roelofs JG (1998) The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. J Ecol 86(5):717–738
Box J (1983) Investigation of the Folin–Ciocalteau phenol reagent for the determination of polyphenolic substances in natural waters. Water Res 17(5):511–525
Bragazza L, Freeman C, Jones T, Rydin H, Limpens J, Fenner N, Ellis T, Gerdol R, Hájek M, Hájek T (2006) Atmospheric nitrogen deposition promotes carbon loss from peat bogs. P Natl Acad Sci 103(51):19386–19389
Bragazza L, Buttler A, Habermacher J, Brancaleoni L, Gerdol R, Fritze H, Hanajík P, Laiho R, Johnson D (2012) High nitrogen deposition alters the decomposition of bog plant litter and reduces carbon accumulation. Glob Chang Biol 18(3):1163–1172
Bridgham SD, Pastor J, Janssens JA, Chapin C, Malterer TJ (1996) Multiple limiting gradients in peatlands: a call for a new paradigm. Wetlands 16(1):45–65
Brouns K, Verhoeven JT, Hefting MM (2014) Short period of oxygenation releases latch on peat decomposition. Sci Total Environ 481:61–68
Bubier JL, Moore TR, Bledzki LA (2007) Effects of nutrient addition on vegetation and carbon cycling in an ombrotrophic bog. Glob Change Biol 13(6):1168–1186
Bubier JL, Smith R, Juutinen S, Moore TR, Minocha R, Long S, Minocha S (2011) Effects of nutrient addition on leaf chemistry, morphology, and photosynthetic capacity of three bog shrubs. Oecologia 167(2):355–368
Burns R (1982) Enzyme activity in soil: location and a possible role in microbial ecology. Soil Biol Biochem 14(5):423–427
Carreiro M, Sinsabaugh R, Repert D, Parkhurst D (2000) Microbial enzyme shifts explain litter decay responses to simulated nitrogen deposition. Ecology 81(9):2359–2365
Clarholm M, Rosengrenbrinck U (1995) Phosphorus and nitrogen-fertilization of a Norway spruce forest—Effects on needle concentrations and acid-phosphatase-activity in the humus layer. Plant Soil 175(2):239–249
Currey PM, Johnson D, Sheppard LJ, Leith ID, Toberman H, Van Der Wal R, Dawson LA, Artz RR (2010) Turnover of labile and recalcitrant soil carbon differ in response to nitrate and ammonium deposition in an ombrotrophic peatland. Glob Change Biol 16(8):2307–2321
Dick R, Rasmussen P, Kerle E (1988) Influence of long-term residue management on soil enzyme activities in relation to soil chemical properties of a wheat-fallow system. Biol Fert Soils 6(2):159–164
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
Dorrepaal E, Cornelissen JHC, Aerts R, Wallén B, Van Logtestijn RSP (2005) Are growth forms consistent predictors of leaf litter quality and decomposability across peatlands along a latitudinal gradient? J Ecol 93(4):817–828
Dunn C, Jones TG, Girard A, Freeman C (2014) Methodologies for extracellular enzyme assays from wetland soils. Wetlands 34(1):9–17
Durán N, Rosa MA, D’Annibale A, Gianfreda L (2002) Applications of laccases and tyrosinases (phenoloxidases) immobilized on different supports: a review. Enzyme Microb Tech 31(7):907–931
Fellman JB, D’Amore DV, Hood E, Boone RD (2008) Fluorescence characteristics and biodegradability of dissolved organic matter in forest and wetland soils from coastal temperate watersheds in southeast Alaska. Biogeochemistry 88(2):169–184
Fog K (1988) The effect of added nitrogen on the rate of decomposition of organic matter. Biol Rev 63(3):433–462
Freeman C, Liska G, Ostle N, Lock M, Reynolds B, Hudson J (1996) Microbial activity and enzymic decomposition processes following peatland water table drawdown. Plant Soil 180(1):121–127
Freeman C, Ostle N, Kang H (2001a) An enzymic ‘latch’ on a global carbon store. Nature 409(6817):149–149
Freeman C, Evans C, Monteith D, Reynolds B, Fenner N (2001b) Export of organic carbon from peat soils. Nature 412(6849):785–785
Freeman C, Ostle N, Fenner N, Kang H (2004) A regulatory role for phenol oxidase during decomposition in peatlands. Soil Biol Biochem 36(10):1663–1667
Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. Forest Ecol Manag 196(1):159–171
Gorham E (1957) The development of peat lands. Q Rev Biol 22(2):145–166
Heijmans MM, Berendse F, Arp WJ, Masselink AK, Klees H, De Visser W, Van Breemen N (2001) Effects of elevated carbon dioxide and increased nitrogen deposition on bog vegetation in the Netherlands. J Ecol 89(2):268–279
Hill BH, Elonen CM, Jicha TM, Kolka RK, Lehto LL, 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 peatland types. Biogeochemistry 120(1–3):203–224
Hoosbeek MR, Van Breemen N, Vasander H, Buttler A, Berendse F (2002) Potassium limits potential growth of bog vegetation under elevated atmospheric CO2 and N deposition. Glob Change Biol 8(11):1130–1138
Hugelius G, Bockheim JG, Camill P, Elberling B, Grosse G, Harden JW, Johnson K, Jorgenson T, Koven CD, Kuhry P, Michaelson G, Mishra U, Palmtag J, Ping C-L, O’Donnell J, Schuur EAG, Sheng Y, Smith LC, Strauss J, Yu Z (2013) A new data set for estimating organic carbon storage to 3 m depth in soils of the northern circumpolar permafrost region. Earth Syst Sci Data 5(2):393–402
Hunt A, Parry JD, Hamilton-Taylor J (2000) Further evidence of elemental composition as an indicator of the bioavailability of humic substances to bacteria. Limnol Oceanogr 45(1):237–241
Johnston CA (1991) Sediment and nutrient retention by fresh-water wetlands—Effects on surface-water quality. Crit Rev Env Contr 21(5–6):491–565
Juma N, Tabatabai M (1978) Distribution of phosphomonoesterases in soils. Soil Sci 126(2):101–108
Juutinen S, Bubier JL, Moore TR (2010) Responses of vegetation and ecosystem CO2 exchange to nine years of fertilization at Mer Bleue bog. Ecosystems 13:874–887
Juutinen S, Moore T, Bubier JL, Tuittila ES, DeYoung A, Chong M (in press) Responses of mosses Sphagnum capillifolium and Polytrichum strictum to nitrogen deposition in a bog: height growth, ground cover, and CO2 exchange. Botany
Kang H, Freeman C (1999) Phosphatase and arylsulphatase activities in wetland soils: annual variation and controlling factors. Soil Biol Biochem 31(3):449–454
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):1–15
Kellogg LE, Bridgham SD (2003) Phosphorus retention and movement across an ombrotrophic-minerotrophic peatland gradient. Biogeochemistry 63(3):299–315
Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86(12):3252–3257
Kunito T, Akagi Y, Park HD, Toda H (2009) Influences of nitrogen and phosphorus addition on polyphenol oxidase activity in a forested andisol. Eur J For Res 128(4):361–366
Lachat Instruments (2008) Data Pack Lachat Applications in Standard Methods, 21st edn. Lachat Instruments, Milwaukee
Lamers LP, Bobbink R, Roelofs JG (2000) Natural nitrogen filter fails in polluted raised bogs. Glob Change Biol 6(5):583–586
Larmola T, Bubier JL, Kobyljanec C, Basiliko N, Juutinen S, Humphreys E, Preston M, Moore TR (2013) Vegetation feedbacks of nutrient addition lead to a weaker carbon sink in an ombrotrophic bog. Glob Change Biol 19:3729–3739
Li Y, Vitt DH (1997) Patterns of retention and utilization of aerially deposited nitrogen in boreal peatlands. Ecoscience 4(1):106–116
Limpens J, Berendse F (2003) How litter quality affects mass loss and N loss from decomposing Sphagnum. Oikos 103(3):537–547
Loisel J et al (2014) A database and synthesis of northern peatland soil properties and Holocene carbon and nitrogen accumulation. Holocene 24:1043–1053
Lund M, Christensen TR, Mastepanov M, Lindroth A, Ström L (2009) Effects of N and P fertilization on the greenhouse gas exchange in two northern peatlands with contrasting N deposition rates. Biogeosciences 6:2135–2144
Malhotra A, Roulet NT, Wilson P, Giroux-Bougard X, Harris LI (2016) Ecohydrological feedbacks in peatlands: an empirical test of the relationship among vegetation, microtopography and water table. Ecohydrology. doi:10.1002/eco.1731
Maynard D, Kalra Y, Crumbaugh JA (1993) Nitrate and exchangeable ammonium nitrogen. In: Carter MR, Gregorich EG (eds) Soil sampling and methods of analysis. Lewis Publishing, Boca Raton, pp 71–80
McCarty G, Shogren D, Bremner J (1992) Regulation of urease production in soil by microbial assimilation of nitrogen. Biol Fert Soils 12(4):261–264
McGill W, Cole C (1981) Comparative aspects of cycling of organic C, N, S and P through soil organic matter. Geoderma 26(4):267–286
Moore T, Basiliko N (2006) Decomposition in Boreal Peatlands. In: Wieder RK, Vitt D (eds) Boreal Peatland Ecosystems. Springer, Berlin, pp 126–143
Moore TR, Bubier JL, Frolking SE, Lafleur PM, Roulet NT (2002) Plant biomass and production and CO2 exchange in an ombrotrophic bog. J Ecol 90(1):25–36
Moore TR, De Young A, Bubier JL, Humphreys ER, Lafleur PM, Roulet NT (2011) A multi-year record of methane flux at the Mer Bleue Bog, Southern Canada. Ecosystems 14(4):646–657
National Atmospheric Deposition Program (NRSP-3) (2012) NADP Program Office. State Water Survey, University of Illinois, Champaign
Neff JC, Townsend AR, Gleixner G, Lehman SJ, Turnbull J, Bowman WD (2002) Variable effects of nitrogen additions on the stability and turnover of soil carbon. Nature 419(6910):915–917
Olander LP, Vitousek PM (2000) Regulation of soil phosphatase and chitinase activityby N and P availability. Biogeochemistry 49(2):175–191
Parkinson J, Allen S (1975) A wet oxidation procedure suitable for the determination of nitrogen and mineral nutrients in biological material. Commun Soil Sci Plant Anal 6(1):1–11
Patton CJ, Kryskalla JR (2003) Methods of analysis by the US Geological Survey National Water Quality Laboratory: evaluation of alkaline persulfate digestion as an alternative to kjeldahl digestion for determination of total and dissolved nitrogen and phosphorus in water. United States Geological Survey, Series 2003-4174
Pinsonneault AJ, Moore TR, Roulet NT, Lapierre JF (2016a) Biodegradability of vegetation-derived dissolved organic carbon in a cool temperate ombrotrophic bog. Ecosystems: 1–14
Pinsonneault AJ, Moore TR, Roulet NT (2016b) Temperature the dominant control on the enzyme-latch across a range of temperate peatland types. Soil Biol Biochem 97:121–130
Reddy KR, DeLaune RD (2008) Biogeochemistry of wetlands. CRC Press, New York
Richardson CJ (1985) Mechanisms controlling phosphorus retention capacity in fresh-water wetlands. Science 228(4706):1424–1427
Roulet NT, Lafleur PM, Richard PJH, Moore TR, Humphreys ER, Bubier J (2007) Contemporary carbon balance and late Holocene carbon accumulation in a northern peatland. Glob Change Biol 13(2):397–411
Roy C (2015) Mer Bleue Fertilization Plot Survey. Unpublished data
Rudolph H, Hohlfeld J, Jacubowski S, Von der Lage P, Matlok H, Schmidt H (1993) Nitrogen metabolism of Sphagnum. Adv Bryol 5(79):105
Rydin H, Jeglum JK (2013) The Biology of Peatlands (2e). Oxford University Press, New York
Saiya-Cork K, Sinsabaugh R, Zak D (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34(9):1309–1315
Seifert-Monson L (2013) Effects of altered deposition chemistry on dissolved organic carbon, pore water nutrients, and microbial enzyme activities in a northern peatland. Master’s Thesis, University of Minnesota, Minneapolis
Sen Tran T, Simard RR (1993) Mehlich III—Extractable elements. Chapter 6 in peat sampling and methods of analysis. M.R. Carter (eds), Lewis Publishers, Boca Raton, FL
Sinsabaugh R (1994) Enzymic analysis of microbial pattern and process. Biol Fert Soils 17(1):69–74
Sinsabaugh R, Moorhead D (1994) Resource allocation to extracellular enzyme production: a model for nitrogen and phosphorus control of litter decomposition. Soil Biol Biochem 26(10):1305–1311
Spiers G, McGill W (1979) Effects of phosphorus addition and energy supply on acid phosphatase production and activity in soils. Soil Biol Biochem 11(1):3–8
Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton
Tarnocai C, Canadell JG, Schuur EAG, Kuhry P, Mazhitova G, Zimov S (2009) Soil organic carbon pools in the northern circumpolar permafrost region. Global Biogeochem Cy 23(2):GB2023
Van Breemen N (1995) How Sphagnum bogs down other plants. Trends Ecol Evol 10(7):270–275
Vitt DH, Wieder K, Halsey LA, Turetsky M (2003) Response of Sphagnum fuscum to nitrogen deposition: a case study of ombrogenous peatlands in Alberta Canada. Bryologist 106(2):235–245
Walbridge MR, Struthers JP (1993) Phosphorus retention in non-tidal palustrine forested wetlands of the mid-Atlantic region. Wetlands 13(2):84–94
Waldrop MP, Zak DR, Sinsabaugh RL (2004) Microbial community response to nitrogen deposition in northern forest ecosystems. Soil Biol Biochem 36(9):1443–1451
Wang M, Murphy MT, Moore TR (2014) Nutrient resorption of two evergreen shrubs in response to long-term fertilization in a bog. Oecologia 174(2):365–377
Wang H, Richardson CJ, Ho M (2015a) Dual controls on carbon loss during drought in peatlands. Nat clim chang 5(6):584–587
Wang M, Moore TR, Talbot J, Riley JL (2015b) The stoichiometry of carbon and nutrients in peat formation. Global Biogeochem Cy 29(2):113–121
Wiegner TN, Seitzinger SP (2004) Seasonal bioavailability of dissolved organic carbon and nitrogen from pristine and polluted freshwater wetlands. Limnol Oceanogr 49(5):1703–1712
Williams CJ, Shingara EA, Yavitt JB (2000) Phenol oxidase activity in peatlands in New York State: response to summer drought and peat type. Wetlands 20(2):416–421
Xing Y, Bubier J, Moore T, Murphy M, Basiliko N, Wendel S, Blodau C (2010) The fate of 15N-nitrate in a northern peatland impacted by long term experimental nitrogen, phosphorus and potassium fertilization. Biogeochemistry 103(1–3):281–296
Yang K, Zhu J, Xu S (2014) Influences of various forms of nitrogen additions on carbon mineralization in natural secondary forests and adjacent larch plantations in Northeast China. Can J Forest Res 44(5):441–448
Yu Z, Loisel J, Brosseau DP, Beilman DW, Hunt SJ (2010) Global peatland dynamics since the Last Glacial Maximum. Geophys Res Lett 37(13):L13402
Acknowledgments
We would like to thank the two anonymous reviewers and the Associate Editor for their constructive comments that significantly improved the quality of this manuscript. We also gratefully acknowledge the field and laboratory assistance of Kellie Foster, Shannon Gregory, Hélène Lalande, and Mike Dalva as well as the precipitation data set provided by Elyn Humphreys at Carleton University. A.J.P was awarded both an Alexander Graham Bell Canada Graduate Scholarship by the Natural Sciences and Engineering Research Council of Canada and a Graduate Stipend Award by the Global Environmental and Climate Change Centre (GEC3) and this research was funded by a Natural Sciences and Engineering Research Council Discovery Grant to T.R.M. We thank the National Capital Commission for access to Mer Bleue.
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Pinsonneault, A.J., Moore, T.R. & Roulet, N.T. Effects of long-term fertilization on peat stoichiometry and associated microbial enzyme activity in an ombrotrophic bog. Biogeochemistry 129, 149–164 (2016). https://doi.org/10.1007/s10533-016-0224-6
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DOI: https://doi.org/10.1007/s10533-016-0224-6