Abstract
Freshwaters are a significant yet understudied component of the global nitrous oxide (N2O) budget. Despite the potential importance of the Laurentian Great Lakes in the freshwater N2O budget, studies have been extremely limited to date. This study evaluated the production pathways, concentrations, and atmospheric emissions of N2O across the two trophic extremes of the Great Lakes: the deep oligotrophic waters of Lake Superior and shallow eutrophic zones of western Lake Erie. Production pathways via denitrification and nitrification were evaluated through stable isotope analysis, and atmospheric emissions were determined from surface concentrations and wind speed. Across all sites and dates, N2O saturation ranged from 98 to 129% in Lake Superior and 93 to 676% in Sandusky Bay, Lake Erie, indicating these lakes are net sources of N2O to the atmosphere. Isotopic site preference values (SP) suggest a mix of production pathways, with nitrification dominating most time periods and denitrification occurring under conditions of high nutrient availability and microbial activity. N2O atmospheric emissions were strong but highly variable in Lake Erie, and emissions in Lake Superior were consistently low (− 0.26 to 33.03 and − 0.14 to 1.41 μmol N m−2 day−1, respectively). Our findings highlight two paradigms of N2O production and emissions: low, wind-driven rates in deep oligotrophic zones and temporally dynamic rates driven by N loading in shallow eutrophic zones. Offshore regions likely make up the majority of the N2O budget for the Great Lakes, yet nearshore regions have a greater capacity for increased N2O emissions in the face of increased nutrient loading.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bange H, Freing A, Kock A, Löscher C (2010) Marine pathways to nitrous oxide. In: Smith K (ed) Nitrous oxide and climate change. Earthscan, London, pp 36–62
Beaulieu JJ, Tank JL, Hamilton SK et al (2011) Nitrous oxide emission from denitrification in stream and river networks. Proc Natl Acad Sci USA 108:214–219. https://doi.org/10.1073/pnas.1011464108
Beaulieu JJ, Nietch CT, Young JL (2015) Controls on nitrous oxide production and consumption in reservoirs of the Ohio River Basin: N2O in reservoirs. J Geophys Res Biogeosci 120:1995–2010. https://doi.org/10.1002/2015jg002941
Bennett EB (1978) Characteristics of the thermal regime of Lake Superior. J Gt Lakes Res 4:310–319. https://doi.org/10.1016/s0380-1330(78)72200-8
Bianchi D, Dunne JP, Sarmiento JL, Galbraith ED (2012) Data-based estimates of suboxia, denitrification, and N2O production in the ocean and their sensitivities to dissolved O2: data-based suboxia and denitrification. Glob Biogeochem Cycles. https://doi.org/10.1029/2011gb004209
Breider F, Yoshikawa C, Abe H et al (2015) Origin and fluxes of nitrous oxide along a latitudinal transect in western North Pacific: controls and regional significance: origin of N2O in the North Pacific Ocean. Glob Biogeochem Cycles 29:1014–1027. https://doi.org/10.1002/2014gb004977
Cavaliere E, Baulch HM (2018) Denitrification under lake ice. Biogeochemistry 137:285–295. https://doi.org/10.1007/s10533-018-0419-0
Chaffin JD, Bridgeman TB, Bade DL (2013) Nitrogen constrains the growth of late summer cyanobacterial blooms in Lake Erie. Adv Microbiol 03:16–26. https://doi.org/10.4236/aim.2013.36a003
Charpentier J, Farias L, Yoshida N et al (2007) Nitrous oxide distribution and its origin in the central and eastern South Pacific Subtropical Gyre. Biogeosci Discuss 4:1673–1702
Crowe SA, Treusch AH, Forth M et al (2017) Novel anammox bacteria and nitrogen loss from Lake Superior. Sci Rep 7:13757. https://doi.org/10.1038/s41598-017-12270-1
Denk TRA, Mohn J, Decock C et al (2017) The nitrogen cycle: a review of isotope effects and isotope modeling approaches. Soil Biol Biochem 105:121–137. https://doi.org/10.1016/j.soilbio.2016.11.015
Finlay JC, Sterner RW, Kumar S (2007) Isotopic evidence for in-lake production of accumulating nitrate in Lake Superior. Ecol Appl 17:2323–2332. https://doi.org/10.1890/07-0245.1
Fujii A, Toyoda S, Yoshida O et al (2013) Distribution of nitrous oxide dissolved in water masses in the eastern subtropical North Pacific and its origin inferred from isotopomer analysis. J Oceanogr 69:147–157. https://doi.org/10.1007/s10872-012-0162-4
Hamilton SK, Ostrom NE (2007) Measurement of the stable isotope ratio of dissolved N2 in 15N tracer experiments: dissolved N2 in 15N tracer experiments. Limnol Oceanogr Methods 5:233–240. https://doi.org/10.4319/lom.2007.5.233
Herdendorf CE (1990) Great Lakes estuaries. Estuaries 13:493–503. https://doi.org/10.2307/1351795
Hsu T-C, Kao S-J (2013) Technical Note: simultaneous measurement of sedimentary N2 and N2O production and a modified 15N isotope pairing technique. Biogeosciences 10:7847–7862. https://doi.org/10.5194/bg-10-7847-2013
IPCC (2007) Climate change 2007: the physical science basis. In: Solomon S et al (eds) Contribution of working group I to the fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, New York
IPCC (2013) Climate change 2013: the physical science Basis. In: Stocker TF et al (eds) Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, New York
Jinuntuya-Nortman M, Sutka RL, Ostrom PH et al (2008) Isotopologue fractionation during microbial reduction of N2O within soil mesocosms as a function of water-filled pore space. Soil Biol Biochem 40:2273–2280. https://doi.org/10.1016/j.soilbio.2008.05.016
Law CS, Owens NJP (1990) Denitrification and nitrous oxide in the North Sea. Neth J Sea Res 25:65–74. https://doi.org/10.1016/0077-7579(90)90009-6
Lemon E, Lemon D (1981) Nitrous oxide in fresh waters of the Great Lakes Basin. Limnol Oceanogr 26:867–879. https://doi.org/10.4319/lo.1981.26.5.0867
Lewicka-Szczebak D, Well R, Bol R et al (2015) Isotope fractionation factors controlling isotopocule signatures of soil-emitted N2O produced by denitrification processes of various rates: isotope fractionation factors of soil-denitrification of various rates. Rapid Commun Mass Spectrom 29:269–282. https://doi.org/10.1002/rcm.7102
McCarthy MJ, Gardner WS, Lavrentyev PJ et al (2007) Effects of hydrological flow regime on sediment–water interface and water column nitrogen dynamics in a Great Lakes Coastal Wetland (Old Woman Creek, Lake Erie). J Gt Lakes Res 33:219–231. https://doi.org/10.3394/0380-1330(2007)33%5b219:eohfro%5d2.0.co;2
Michalak AM, Anderson EJ, Beletsky D et al (2013) Record-setting algal bloom in Lake Erie caused by agricultural and meteorological trends consistent with expected future conditions. Proc Natl Acad Sci USA 110:6448–6452. https://doi.org/10.1073/pnas.1216006110
Michmerhuizen CM, Striegl RG, McDonald ME (1996) Potential methane emission from north-temperate lakes following ice melt. Limnol Oceanogr 41:985–991. https://doi.org/10.4319/lo.1996.41.5.0985
Moon JB, Carrick HJ (2007) Seasonal variation of phytoplankton nutrient limitation in Lake Erie. Aquat Microb Ecol 48:61–71. https://doi.org/10.3354/ame048061
North RL, Guildford SJ, Smith REH et al (2007) Evidence for phosphorus, nitrogen, and iron colimitation of phytoplankton communities in Lake Erie. Limnol Oceanogr 52:315–328. https://doi.org/10.4319/lo.2007.52.1.0315
Ostrom NE, Gandhi H, Coplen TB et al (2018) Preliminary assessment of stable nitrogen and oxygen isotopic composition of USGS51 and USGS52 nitrous oxide reference gases and perspectives on calibration needs. Rapid Commun Mass Spectrom 32:1207–1214. https://doi.org/10.1002/rcm.8157
Robertson DM, Saad DA (2011) Nutrient inputs to the Laurentian Great Lakes by source and watershed estimated using SPARROW watershed models. J Am Water Resour Assoc 47:1011–1033. https://doi.org/10.1111/j.1752-1688.2011.00574.x
Royer TV, David MB, Gentry LE (2006) Timing of riverine export of nitrate and phosphorus from agricultural watersheds in Illinois: implications for reducing nutrient loading to the Mississippi River. Environ Sci Technol 40:4126–4131. https://doi.org/10.1021/es052573n
Salk KR, Ostrom PH, Biddanda BA et al (2016) Ecosystem metabolism and greenhouse gas production in a mesotrophic northern temperate lake experiencing seasonal hypoxia. Biogeochemistry 131:303–319. https://doi.org/10.1007/s10533-016-0280-y
Salk KR, Bullerjahn GS, McKay RML et al (2018) Nitrogen cycling in Sandusky Bay, Lake Erie: oscillations between strong and weak export and implications for harmful algal blooms. Biogeosciences 15:2891–2907. https://doi.org/10.5194/bg-15-2891-2018
Small GE, Cotner JB, Finlay JC et al (2014) Nitrogen transformations at the sediment–water interface across redox gradients in the Laurentian Great Lakes. Hydrobiologia 731:95–108. https://doi.org/10.1007/s10750-013-1569-7
Small GE, Finlay JC, McKay RML et al (2016) Large differences in potential denitrification and sediment microbial communities across the Laurentian Great Lakes. Biogeochemistry 128:353–368. https://doi.org/10.1007/s10533-016-0212-x
Steffen MM, Belisle BS, Watson SB et al (2014) Status, causes and controls of cyanobacterial blooms in Lake Erie. J Gt Lakes Res 40:215–225. https://doi.org/10.1016/j.jglr.2013.12.012
Sterner R (2011) C:N:P stoichiometry in Lake Superior: freshwater sea as end member. Inland Waters 1:29–46. https://doi.org/10.5268/iw-1.1.365
Sterner RW, Anagnostou E, Brovold S et al (2007) Increasing stoichiometric imbalance in North America’s largest lake: nitrification in Lake Superior. Geophys Res Lett. https://doi.org/10.1029/2006gl028861
Sutka RL, Ostrom NE, Ostrom PH et al (2003) Nitrogen isotopomer site preference of N2O produced by Nitrosomonas europaea and Methylococcus capsulatus Bath. Rapid Commun Mass Spectrom 17:738–745. https://doi.org/10.1002/rcm.968
Sutka RL, Ostrom NE, Ostrom PH et al (2006) Distinguishing nitrous oxide production from nitrification and denitrification on the basis of isotopomer abundances. Appl Environ Microbiol 72:638–644. https://doi.org/10.1128/aem.72.1.638-644.2006
Sutka RL, Adams GC, Ostrom NE, Ostrom PH (2008) Isotopologue fractionation during N2O production by fungal denitrification. Rapid Commun Mass Spectrom 22:3989–3996. https://doi.org/10.1002/rcm.3820
Toyoda S, Mutobe H, Yamagishi H et al (2005) Fractionation of N2O isotopomers during production by denitrifier. Soil Biol Biochem 37:1535–1545. https://doi.org/10.1016/j.soilbio.2005.01.009
Walker JT, Stow CA, Geron C (2010) Nitrous oxide emissions from the Gulf of Mexico hypoxic zone. Environ Sci Technol 44:1617–1623. https://doi.org/10.1021/es902058t
Wang H, Wang W, Yin C et al (2006) Littoral zones as the “hotspots” of nitrous oxide (N2O) emission in a hyper-eutrophic lake in China. Atmos Environ 40:5522–5527. https://doi.org/10.1016/j.atmosenv.2006.05.032
Wanninkhof R (1992) Relationship between wind speed and gas exchange over the ocean. J Geophys Res 97:7373. https://doi.org/10.1029/92jc00188
Weiss RF, Price BA (1980) Nitrous oxide solubility in water and seawater. Mar Chem 8:347–359. https://doi.org/10.1016/0304-4203(80)90024-9
Well R, Eschenbach W, Flessa H et al (2012) Are dual isotope and isotopomer ratios of N2O useful indicators for N2O turnover during denitrification in nitrate-contaminated aquifers? Geochim Cosmochim Acta 90:265–282. https://doi.org/10.1016/j.gca.2012.04.045
Wenk CB, Frame CH, Koba K et al (2016) Differential N2O dynamics in two oxygen-deficient lake basins revealed by stable isotope and isotopomer distributions: differential N2O dynamics in two lake basins. Limnol Oceanogr 61:1735–1749. https://doi.org/10.1002/lno.10329
Westley MB, Yamagishi H, Popp BN, Yoshida N (2006) Nitrous oxide cycling in the Black Sea inferred from stable isotope and isotopomer distributions. Deep Sea Res II 53:1802–1816. https://doi.org/10.1016/j.dsr2.2006.03.012
Whitfield CJ, Aherne J, Baulch HM (2011) Controls on greenhouse gas concentrations in polymictic headwater lakes in Ireland. Sci Total Environ 410–411:217–225. https://doi.org/10.1016/j.scitotenv.2011.09.045
Wrage N, Velthof GL, van Beusichem ML, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol 33:1723–1732
Yang H, Gandhi H, Ostrom NE, Hegg EL (2014) Isotopic fractionation by a fungal P450 nitric oxide reductase during the production of N2O. Environ Sci Technol 48:10707–10715. https://doi.org/10.1021/es501912d
Yang H, Andersen T, Dörsch P et al (2015) Greenhouse gas metabolism in Nordic boreal lakes. Biogeochemistry 126:211–225. https://doi.org/10.1007/s10533-015-0154-8
Acknowledgements
Special thanks to the field sampling crews in Sandusky Bay (Taylor Tuttle, Emily Davenport) and on the R/V Blue Heron in Lake Superior (Doug Ricketts, Nigel D’Souza, Christopher Filstrup, Tristan Horner, Andrew Thaler). Hasand Gandhi provided considerable help and insight for laboratory analyses. This research was supported by the University-National Oceanographic Laboratory System, National Science Foundation Graduate Research Fellowship (No. 497 DGE1424871), The Michigan State University (MSU) College of Natural Science Hensley Fellowship, The MSU Rose Fellowship in Water Research, The MSU WaterCube Program, The Ohio Department of Higher Education’s Harmful Algal Bloom Research Initiative (No. R/HAB-2-BOR), and The Ohio Sea Grant College Program (No. R/ER-114).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsbile Editor: Stuart Grandy.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Online Resource
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Salk, K.R., Ostrom, N.E. Nitrous oxide in the Great Lakes: insights from two trophic extremes. Biogeochemistry 144, 233–243 (2019). https://doi.org/10.1007/s10533-019-00583-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-019-00583-4