Skip to main content
SpringerLink
Log in

Denitrification under lake ice

  • Biogeochemistry Letters
  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Many lakes, ponds and reservoirs are subject to long and changing periods of ice cover. However, limited winter research has created key knowledge gaps. How does nitrogen cycling change under ice? And what does changing ice cover duration mean for water quality? Here we present the first measurements of denitrification rates under ice in temperate, polymictic waterbodies. Surprisingly, despite lower winter temperatures, winter and summer rates of denitrification did not differ. Experimental work suggests that denitrification rates are controlled hierarchically, first by nitrate concentrations, then by temperature. As a result, controls on nitrate inputs such as changing hydrology and nitrification, combined with physical controls on delivery of nitrate to sediments, may be more important to nitrate retention via denitrification than the duration of low temperature or ice cover. Nitrous oxide was typically supersaturated under-ice, suggesting an ice-out flux will occur, and this flux may be greatest in systems with elevated nitrate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Allan RJ, Roy M (1980) Lake water nutrient chemistry and chlorophyll a in Pasqua, Echo, Mission, Katepwa, Crooked and Round Lakes on the Qu’Appelle River, Saskatchewan. National Water Research Institute, Inland Waters Directorate. Environment Canada Regina, Saskatchewan. Scientific Series No. 112

  • Barica J (1987) Water quality problems associated with high productivity of prairie lakes in Canada: A Review. Water Qual Bull 107–115:129

    Google Scholar 

  • Baulch HM, Schiff SL, Maranger R, Dillon PJ (2011) Nitrogen enrichment and the emission of nitrous oxide from streams. Global Biogeochem Cycles 25:1–15. https://doi.org/10.1029/2011GB004047

    Article  Google Scholar 

  • Belzile C, Gibson JAE, Vincent WF (2002) Colored dissolved organic matter and dissolved organic carbon exclusion from lake ice: Implications for irradiance transmission and carbon cycling. Limnol Oceanogr 47:1283–1293. https://doi.org/10.4319/lo.2002.47.5.1283

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Breitenbeck GA, Bremner JM (1987) Effects of storing soils at various temperatures on their capacity for denitrification. Soil Biol Biochem 19:377–380

    Article  Google Scholar 

  • Brin LD, Giblin AE, Rich JJ (2017) Similar temperature responses suggest future climate warming will not alter partitioning between denitrification and anammox in temperate marine sediments. Glob Chang Biol 23:331–340. https://doi.org/10.1111/gcb.13370

    Article  Google Scholar 

  • Brown JH, Sibly RM (2012) The metabolic theory of ecology and its central equation. In: Sibly RM, Brown JH, Kodric-Brown A (eds) Metabolic ecology: a scaling approach. Wiley-Blackwell, Oxford, UK, pp 29–30

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Causse J, Baurès E, Mery Y et al (2015) Variability of N export in water: a review. Crit Rev Environ Sci Technol 45:2245–2281. https://doi.org/10.1080/10643389.2015.1010432

    Article  Google Scholar 

  • Ciais P, Sabine C, Bala G et al (2013) Carbon and other biogeochemical cycles. In: Stocker TF, Qin D, Plattner G-K et al (eds) Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, United Kingdom and New York, NY USA, pp 465–570

  • Cole JJ, Caraco NF, Kling GW, Kratz TK (1994) Carbon dioxide supersaturation in the surface waters of lakes. Science 265:1568–1570

    Article  Google Scholar 

  • Costa D, Roste J, Pomeroy J et al (2017) A modelling framework to simulate field-scale nitrate response and transport during snowmelt: the WINTRA model. Hydrol Process 31:4250–4268

    Article  Google Scholar 

  • Firestone MK, Davidson EA (1989) Microbiologial basis of NO and N2O production and consumption in soil. Exch. Trace Gases between Terr. Ecosyst. Atmos. pp 7–21

  • 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

    Article  Google Scholar 

  • Gooding R (2015) Denitrification in small reservoirs: understanding nitrogen removal across an agricultural watershed. Thesis, University of Saskatchewan

  • Groffman PM, Holland EA, Myrold DD et al (1999) Denitrification: methods. Stand soil methods long-term. Ecol Res, pp 272–290

  • Groffman PM, Altabet MA, Bohlke JKK et al (2006) Methods for measuring denitrification: diverse approaches to a difficult problem. Ecol Appl 16:2091–2122

    Article  Google Scholar 

  • Hampton SE, Galloway AWE, Powers SM et al (2016) Ecology under lake ice. Ecol Lett 20:98–111. https://doi.org/10.1111/ele.12699

    Article  Google Scholar 

  • Harrison J, Matson P (2003) Patterns and controls of nitrous oxide emissions from waters draining a subtropical agricultural valley. Global Biogeochem Cycles. https://doi.org/10.1029/2002GB001991

    Google Scholar 

  • Harrison JA, Maranger RJ, Alexander RB et al (2009) The regional and global significance of nitrogen removal in lakes and reservoirs. Biogeochemistry 93:143–157. https://doi.org/10.1007/s10533-008-9272-x

    Article  Google Scholar 

  • Hasegawa T, Okino T (2004) Seasonal variation of denitrification rate in Lake Suwa sediment. Limnology 5:33–39. https://doi.org/10.1007/s10201-003-0109-y

    Article  Google Scholar 

  • Kabacoff RI (2011) R in action: data analysis and graphics with R. Manning Publications Co., Shelter Island, NY

    Google Scholar 

  • Knowles R (1982) Denitrification. Microbiol Rev 46:43–70

    Google Scholar 

  • Lemke P, Ren J, Alley RB et al (2007) Observations: changes in snow, ice and frozen ground. In: Solomon S, Qin D, Manning M et al (eds) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, United Kingdom and New York, NY USA, pp 337–383

  • Martin L, Mulholland PJ, Webster J, Valett HM (2001) Denitrification potential in sediments of headwater streams in the southern Appalachian Mountains, USA. J N Am Benthol Soc 20:505–519

    Article  Google Scholar 

  • Myrstener M, Jonsson A, Bergström AK (2016) The effects of temperature and resource availability on denitrification and relative N2O production in boreal lake sediments. J Environ Sci 47:82–90. https://doi.org/10.1016/j.jes.2016.03.003

    Article  Google Scholar 

  • Pawlowicz R (2008) Calculating the conductivity of natural waters. Limnol Oceanogr Methods 6:489–501. https://doi.org/10.4319/lom.2008.6.489

    Article  Google Scholar 

  • Pernica P, North RL, Baulch HM (2017) In the cold light of day: the potential importance of under-ice convective mixed layers to primary producers. Inl Waters 7:138–150

    Article  Google Scholar 

  • Pomeroy JW, Boer D De, Martz LW (2005) Hydrology and water resources of Saskatchewan. Centre for Hydrology, University of Saskatchewan. Saskatoon, Saskatchewan. Centre for Hydrology Report 1

  • Powers SM, Baulch HM, Hampton SE et al (2017a) Nitrification contributes to winter oxygen depletion in seasonally frozen forested lakes. Biogeochemistry 136:1–11. https://doi.org/10.1007/s10533-017-0382-1

    Article  Google Scholar 

  • Powers SM, Labou SG, Baulch HM et al (2017b) Ice duration drives winter nitrate accumulation in north temperate lakes. Limnol Oceanogr Lett. https://doi.org/10.1002/lol2.10048

    Google Scholar 

  • R Core Team (2016) R: a language and environment for statistical computing

  • Ravishankara AR, Daniel JS, Portmann RW (2009) Nitrous oxide (N2O): the dominant ozone-depleting substance emitted in the 21st century. Science 326:123–125

    Article  Google Scholar 

  • Schindler DW, Donahue WF (2006) An impending water crisis in Canada’s western prairie provinces. Proc Natl Acad Sci USA 103:7210–7216. https://doi.org/10.1073/pnas.0601568103

    Article  Google Scholar 

  • Seitzinger SP, Nielsen LP, Caffrey J, Christensen PB (1993) Denitrification measurements in aquatic sediments: a comparison of three methods. Biogeochemistry 23:147–167

    Article  Google Scholar 

  • Seitzinger S, Harrison JA, Böhlke JK et al (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16:2064–2090

    Article  Google Scholar 

  • Small GE, Bullerjahn GS, Sterner RW et al (2013) Rates and controls of nitrification in a large oligotrophic lake. Limnol Oceanogr 58:276–286. https://doi.org/10.4319/lo.2013.58.1.0276

    Article  Google Scholar 

  • Smith M, Firestone M, Tiedje J (1978) The acetylene inhibition method for short-term measurement of soil denitrification and its evaluation using nitrogen-13. Soil Sci Soc Am J 42:611–615

    Article  Google Scholar 

  • Soued C, del Giorgio PA, Maranger R (2015) Nitrous oxide sinks and emissions in boreal aquatic networks in Québec. Nat Geosci 9:116–120. https://doi.org/10.1038/NGEO2611

    Article  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern Applied Statistics with S. Springer, New York, NY

    Book  Google Scholar 

  • Ward BB, Granger J, Maldonado MT et al (2005) Denitrification in the hypolimnion of permanently ice-covered Lake Bonney, Antarctica. Aquat Microb Ecol 38:295–307. https://doi.org/10.3354/ame038295

    Article  Google Scholar 

  • Weiss RF, Price BA (1980) Nitrous oxide solubility in water and seawater. Mar Chem 8:347–359

    Article  Google Scholar 

  • Wheeler B, Torchiano M (2016) lmPerm: permutation tests for linear models. R package version 2.1.0

  • Wu QT, Knowles R, Niven DF (1995) Effect of ionophores on denitrification in Flexibacter canadensis. Can J Microbiol 41:227–234

    Article  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge support of NSERC (Discovery Grant), the Global Institute for Water Security, and the University of Saskatchewan, School of Environment and Sustainability and the Teacher Scholar Doctoral Fellowship for funding this project. For their support and advice, we would like to thank Drs. Rebecca North, Angela Bedard-Haughn, John-Mark Davies, Karl-Erich Lindenschmidt and Cherie Westbrook. Further, we would like to acknowledge the following individuals for their extensive technical assistance, particularly those that aided in field work that took place in the extreme cold of Saskatchewan winters: Bruce Johnson, Dell Bayne, Jay Bauer, Britni Brenna, Cameron Hoggarth, Erin Hillis, Victor Sit, Kim Gilmour, Navjot Kaur, Rosa Brannen, Heather Wilson, Dr. Michael Kehoe, Alyse Kambeitz, Dr. Lorne Doig, Katya Dobrovolskkava, Katy Nugent, Beau Schlageter, Hayden Yip, Jeremy Kiss, Dr. Colin Whitfield, Sherry Olauson, Kate Wilson, Michelle Martel-Andre, Raea Gooding, Noel Galuschik, Zachary Keesey and all members of the Saskwatche (Saskatchewan Water Chemistry and Ecology) Lab.

Author information

Authors and Affiliations

  1. School of Environment and Sustainability, Global Institute for Water Security, University of Saskatchewan, 11 Innovation Boulevard, Saskatoon, SK, S7N3H5, Canada

    E. Cavaliere & H. M. Baulch

Authors
  1. E. Cavaliere
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H. M. Baulch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Cavaliere.

Additional information

Responsible Editor: Stuart Grandy.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 42 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cavaliere, E., Baulch, H.M. Denitrification under lake ice. Biogeochemistry 137, 285–295 (2018). https://doi.org/10.1007/s10533-018-0419-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-018-0419-0

Keywords

Search

Navigation