Abstract
The frequency and duration of lake ice cover is rapidly declining in the Northern Hemisphere. Limited research in oligotrophic and mesotrophic lakes suggests that extended periods of ice cover influence nitrogen (N) cycling by promoting nitrate (NO3−) accumulation. However, ice cover impacts on N cycling in shallow, high-nutrient, eutrophic lakes remains poorly understood. To understand drivers of under-ice water column N concentrations, we examined concurrent under-ice N concentration, hydro-meterological, and physicochemical time series from two shallow eutrophic systems during sustained cold and thaw periods. We compared data from both lakes during a historically cold winter to assess how different lake-watershed physical configurations and algal biomass affected under-ice N cycling. We also used time series data from consecutive winters to assess the influence of a mild versus a historically cold winter on under-ice N cycling in one of the lakes. We found that ice cover promoted NO3− depletion when sustained cold disconnected lakes from watershed loading, but the amount of depletion varied between lakes and was enhanced during the colder winter. Thaw events increased NO3− concentrations compared to late winter and altered the concentration and distribution of N species in the water column, but the degree and nature of increased NO3− varied with thaw severity, the source of meltwater, timing, and lake-watershed morphometry. Our results suggest that winters with shorter ice duration and more thaw events may result in less NO3− depletion and higher peak NO3− concentrations in shallow eutrophic lakes, with potential implications for N cycling and phytoplankton ecology.
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Data and metadata are available in the Environmental Data Initiative data repository (https://doi.org/10.6073/pasta/c9acd134e9b5b641e143420edfeedffb). Data and R scripts used to analyze and visualize these data are also available on Github (https://github.com/dustinkincaid/bree_frozeN).
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References
Akima H, Gebhart A (2020) akima: Interpolation of irregularly and regularly spaced data, R package version 0.6–2.1. https://CRAN.R-project.org/package=akima
Andersen IM, Williamson TJ, González MJ, Vanni MJ (2020) Nitrate, ammonium, and phosphorus drive seasonal nutrient limitation of chlorophytes, cyanobacteria, and diatoms in a hyper-eutrophic reservoir. Limnol Oceanogr 65:962–978. https://doi.org/10.1002/lno.11363
APHA (2005) Standard Methods for the Examination of Water and Wastewater, 21st ed. American Public Health Association (APHA), the American Water Works Association (AWWA), and the Water Environment Federation (WEF), Washington, D.C., USA
Barica J, Mathias JA (1979) Oxygen depletion and winterkill risk in small prairie lakes under extended ice cover. J Fish Board Can 36:980–986. https://doi.org/10.1139/f79-136
Baron JS, Hall EK, Nolan BT et al (2013) The interactive effects of excess reactive nitrogen and climate change on aquatic ecosystems and water resources of the United States. Biogeochemistry 114:71–92. https://doi.org/10.1007/s10533-012-9788-y
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57:289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Bertilsson S, Burgin A, Carey CC et al (2013) The under-ice microbiome of seasonally frozen lakes. Limnol Oceanogr 58:1998–2012. https://doi.org/10.4319/lo.2013.58.6.1998
Block BD, Denfeld BA, Stockwell JD et al (2019) The unique methodological challenges of winter limnology. Limnol Oceanogr Methods 17:42–57. https://doi.org/10.1002/lom3.10295
Bolsenga SJ, Vanderploeg HA (1992) Estimating photosynthetically available radiation into open and ice-covered freshwater lakes from surface characteristics; a high transmittance case study. Hydrobiologia 243–244:95–104. https://doi.org/10.1007/bf00007024
Carlucci AF, McNally PM (1969) Nitrification by marine bacteria in low concentrations of substrate and oxygen. Limnol Oceanogr 14:736–739. https://doi.org/10.4319/lo.1969.14.5.0736
Catalan J (1992) Evolution of dissolved and particulate matter during the ice-covered period in a deep, high-mountain lake. Can J Fish Aquat Sci 49:945–955. https://doi.org/10.1139/f92-105
Cavaliere E, Baulch HM (2018) Denitrification under lake ice. Biogeochemistry 137:285–295. https://doi.org/10.1007/s10533-018-0419-0
Cavaliere E, Baulch HM (2020) Winter in two phases: Long-term study of a shallow reservoir in winter. Limnol Oceanogr. https://doi.org/10.1002/lno.11687
Cébron A, Garnier J, Billen G (2005) Nitrous oxide production and nitrification kinetics by natural bacterial communitites of the lower Seine river (France). Aquat Microb Ecol 41:25–38. https://doi.org/10.3354/ame041025
Donald DB, Bogard MJ, Finlay K, Leavitt PR (2011) Comparative effects of urea, ammonium, and nitrate on phytoplankton abundance, community composition, and toxicity in hypereutrophic freshwaters. Limnol Oceanogr 56:2161–2175. https://doi.org/10.4319/lo.2011.56.6.2161
Downing JA, Cole JJ, Middelburg JJ et al (2008) Sediment organic carbon burial in agriculturally eutrophic impoundments over the last century. Global Biogeochem Cycles 22:GB1018. https://doi.org/10.1029/2006gb002854
Ferber LR, Levine SN, Lini A, Livingston GP (2004) Do cyanobacteria dominate in eutrophic lakes because they fix atmospheric nitrogen? Freshwater Biol 49:690–708. https://doi.org/10.1111/j.1365-2427.2004.01218.x
Filazzola A, Blagrave K, Imrit MA, Sharma S (2020) Climate change drives increases in extreme events for lake ice in the Northern Hemisphere. Geophys Res Lett. https://doi.org/10.1029/2020gl089608
Gardner WS, Newell SE, McCarthy MJ et al (2017) Community biological ammonium demand: a conceptual model for cyanobacteria blooms in eutrophic lakes. Environ Sci Technol 51:7785–7793. https://doi.org/10.1021/acs.est.6b06296
George G, Järvinen M, Nõges T et al (2010) The impact of the changing climate on the supply and recycling of nitrate. In: George G (ed) The impact of climate change on European lakes. Springer, Netherlands, pp 161–178
Giles CD, Isles PDF, Manley T et al (2016) The mobility of phosphorus, iron, and manganese through the sediment–water continuum of a shallow eutrophic freshwater lake under stratified and mixed water-column conditions. Biogeochemistry 127:15–34. https://doi.org/10.1007/s10533-015-0144-x
Glibert PM, Wilkerson FP, Dugdale RC et al (2016) Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen-enriched conditions. Limnol Oceanogr 61:165–197. https://doi.org/10.1002/lno.10203
Goering JJ, Dugdale VA (1966) Estimates of the rates of denitrification in a subarctic lake. Limnol Oceanogr 11:113–117. https://doi.org/10.4319/lo.1966.11.1.0113
Goreau TJ, Kaplan WA, Wofsy SC et al (1980) Production of NO2- and N2O by nitrifying bacteria at reduced concentrations of oxygen. Appl Environ Microb 40:526–532. https://doi.org/10.1128/aem.40.3.526-532.1980
Gu B (2012) Stable isotopes as indicators for seasonally dominant nitrogen cycling processes in a subarctic lake. Int Rev Hydrobiol 97:233–243. https://doi.org/10.1002/iroh.201111466
Gu B, Alexander V (1993a) Seasonal variations in dissolved inorganic nitrogen utilization in a subarctic Alaskan lake. Arch Hydrobiol 126:273–288
Gu B, Alexander V (1993b) Dissolved nitrogen uptake by a cyanobacterial bloom (Anabaena flos-aquae) in a subarctic lake. Appl Environ Microbiol 59:422–430
Hamersley MR, Woebken D, Boehrer B et al (2009) Water column anammox and denitrification in a temperate permanently stratified lake (Lake Rassnitzer, Germany). Syst Appl Microbiol 32:571–582. https://doi.org/10.1016/j.syapm.2009.07.009
Hampton SE, Galloway AWE, Powers SM et al (2017) Ecology under lake ice. Ecol Lett 20:98–111. https://doi.org/10.1111/ele.12699
Hrycik AR, Stockwell JD (2021) Under-ice mesocosms reveal the primacy of light but the importance of zooplankton in winter phytoplankton dynamics. Limnol Oceanogr 66:481–495. https://doi.org/10.1002/lno.11618
Huntington TG, Richardson AD, McGuire KJ, Hayhoe K (2009) Climate and hydrological changes in the Northeastern United States: recent trends and implications for forested and aquatic ecosystems. Can J Forest Res 39:199–212. https://doi.org/10.1139/x08-116
Isles PDF, Giles CD, Gearhart TA et al (2015) Dynamic internal drivers of a historically severe cyanobacteria bloom in Lake Champlain revealed through comprehensive monitoring. J Great Lakes Res 41:818–829. https://doi.org/10.1016/j.jglr.2015.06.006
Järvinen M, Rask M, Ruuhijärvi J, Arvola L (2002) Temporal coherence in water temperature and chemistry under the ice of boreal lakes (Finland). Water Res 36:3949–3956. https://doi.org/10.1016/s0043-1354(02)00128-8
Joung D, Leduc M, Ramcharitar B et al (2017) Winter weather and lake-watershed physical configuration drive phosphorus, iron, and manganese dynamics in water and sediment of ice-covered lakes. Limnol Oceanogr 62:1620–1635. https://doi.org/10.1002/lno.10521
Kincaid DW, Seybold EC, Adair EC et al (2020) Land use and season influence event-scale nitrate and soluble reactive phosphorus exports and export stoichiometry from headwater catchments. Water Resour Res. https://doi.org/10.1029/2020wr027361
Kirillin G, Leppäranta M, Terzhevik A et al (2012) Physics of seasonally ice-covered lakes: a review. Aquat Sci 74:659–682. https://doi.org/10.1007/s00027-012-0279-y
Lehmann MF, Reichert P, Bernasconi SM et al (2003) Modelling nitrogen and oxygen isotope fractionation during denitrification in a lacustrine redox-transition zone. Geochim Cosmochim Ac 67:2529–2542. https://doi.org/10.1016/s0016-7037(03)00085-1
Lescaze MM (1999) Estimation of the relative contribution of atmospheric nitrogen to lake phytoplankton nutrition: a stable isotope approach. Thesis, University of Vermont.
Massé S, Botrel M, Walsh DA, Maranger R (2019) Annual nitrification dynamics in a seasonally ice-covered lake. PLoS ONE 14:e0213748. https://doi.org/10.1371/journal.pone.0213748
Pacheco FS, Roland F, Downing JA (2017) Eutrophication reverses whole-lake carbon budgets. Inland Waters 4:41–48. https://doi.org/10.5268/iw-4.1.614
Palmer MJ, Chételat J, Jamieson HE et al (2020) Hydrologic control on winter dissolved oxygen mediates arsenic cycling in a small subarctic lake. Limnol Oceanogr. https://doi.org/10.1002/lno.11556
Pettersson K, Grust K, Weyhenmeyer G, Blenckner T (2003) Seasonality of chlorophyll and nutrients in Lake Erken—effects of weather conditions. Hydrobiologia 506–509:75–81. https://doi.org/10.1023/b:hydr.0000008582.61851.76
Powers SM, Baulch HM, Hampton SE et al (2017a) Nitrification contributes to winter oxygen depletion in seasonally frozen forested lakes. Biogeochemistry 136:119–129. https://doi.org/10.1007/s10533-017-0382-1
Powers SM, Labou SG, Baulch HM et al (2017b) Ice duration drives winter nitrate accumulation in north temperate lakes. Limnology Oceanogr Lett 2:177–186. https://doi.org/10.1002/lol2.10048
Pulkkanen M, Salonen K (2017) Accumulation of low oxygen water in deep waters of ice-covered lakes cooled below 4 °C. Inland Waters 3:15–24. https://doi.org/10.5268/iw-3.1.514
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria USEPA (1993a) Method 353.2, revision 2.0: Determination of nitrate-nitrite nitrogen by automated colorimetry. United States Environmental Protection Agency
Reddy KR, Fisher MM, Ivanoff D (1996) Resuspension and diffusive flux of nitrogen and phosphorus in a hypereutrophic lake. J Environ Qual 25:363–371. https://doi.org/10.2134/jeq1996.00472425002500020022x
Schroth AW, Giles CD, Isles PDF et al (2015) Dynamic coupling of iron, manganese, and phosphorus behavior in water and sediment of shallow ice-covered eutrophic lakes. Environ Sci Technol 49:9758–9767. https://doi.org/10.1021/acs.est.5b02057
Sebestyen SD, Boyer EW, Shanley JB et al (2008) Sources, transformations, and hydrological processes that control stream nitrate and dissolved organic matter concentrations during snowmelt in an upland forest. Water Resour Res 44:W12410. https://doi.org/10.1029/2008wr006983
Seitzinger S, Harrison JA, Böhlke JK et al (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16:2064–2090. https://doi.org/10.1890/1051-0761(2006)016[2064:dalawa]2.0.co;2
Seybold E, Gold AJ, Inamdar SP et al (2019) Influence of land use and hydrologic variability on seasonal dissolved organic carbon and nitrate export: insights from a multi-year regional analysis for the northeastern USA. Biogeochemistry 146:31–49. https://doi.org/10.1007/s10533-019-00609-x
Smith VH (2003) Eutrophication of freshwater and coastal marine ecosystems a global problem. Environ Sci Pollut R 10:126–139. https://doi.org/10.1065/espr2002.12.142
Smith VH, Tilman GD, Nekola JC (1999) Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environ Pollut 100:179–196. https://doi.org/10.1016/s0269-7491(99)00091-3
USEPA (1993a) Method 353.2, revision 2.0: Determination of nitrate-nitrite nitrogen by automated colorimetry. United States Environmental Protection Agency
USEPA (1993b) Method 350.1, revision 2.0: Determination of ammonia nitrogen by semi-automated colorimetry. United States Environmental Protection Agency
Vaughan MCH, Bowden WB, Shanley JB et al (2017) High-frequency dissolved organic carbon and nitrate measurements reveal differences in storm hysteresis and loading in relation to land cover and seasonality. Water Resour Res 53:5345–5363. https://doi.org/10.1002/2017wr020491
Wehr JD, Sheath RG (2002) Freshwater algae of North America: ecology and classification, 1st edn. Academic Press, San Diego, California
Wenk CB, Zopfi J, Gardner WS et al (2014) Partitioning between benthic and pelagic nitrate reduction in the Lake Lugano south basin. Limnol Oceanogr 59:1421–1433. https://doi.org/10.4319/lo.2014.59.4.1421
Weyhenmeyer GA (2009) Do warmer winters change variability patterns of physical and chemical lake conditions in Sweden? Aquat Ecol 43:653–659. https://doi.org/10.1007/s10452-009-9284-1
Woolway RI, Kraemer BM, Lenters JD et al (2020) Global lake responses to climate change. Nat Rev Earth Environ 1:388–403. https://doi.org/10.1038/s43017-020-0067-5
Yang T, Hei P, Song J et al (2019) Nitrogen variations during the ice-on season in the eutrophic lakes. Environ Pollut 247:1089–1099. https://doi.org/10.1016/j.envpol.2018.12.088
Acknowledgements
This research was made possible through support from the National Science Foundation under grants EPS-1101317, EPS-IIA1330446, OIA1556770, EAR-1561014, and a Vermont EPSCoR Pilot Grant. We thank Brian O’Malley, Trevor Gearhart, Peter Isles, and Yaoyang Xu for assistance with sample collection and Saul Blocher, Hannah Lister, and Elise Mitchell for sample analyses. We also thank two anonymous reviewers that provided suggestions to improve this manuscript.
Funding
This research was made possible through support from the National Science Foundation under Grants EPS-1101317, EPS-IIA1330446, OIA1556770, EAR-1561014, and a Vermont EPSCoR Pilot Grant.
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DWK led the manuscript effort. DJJ, JDS, and AWS contributed to the original comparative study design and conducted the field survey with help from students. DWK, ECA, and AWS came up with the research question. DWK conducted the data analyses. DWK wrote the first draft of the manuscript and all authors provided significant edits to successive drafts.
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Kincaid, D.W., Adair, E.C., Joung, D. et al. Ice cover and thaw events influence nitrogen partitioning and concentration in two shallow eutrophic lakes. Biogeochemistry 157, 15–29 (2022). https://doi.org/10.1007/s10533-021-00872-x
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DOI: https://doi.org/10.1007/s10533-021-00872-x