Skip to main content
SpringerLink
Log in

Nitrous oxide and methane seasonal variability in the epilimnion of a large tropical meromictic lake (Lake Kivu, East-Africa)

  • Research Article
  • Published:
Aquatic Sciences Aims and scope Submit manuscript

Abstract

We report a data-set of monthly vertical profiles obtained from January 2012 to October 2013, from the surface to 70 m depth of nitrous oxide (N2O) and dissolved methane (CH4) in Lake Kivu, a large and deep meromictic tropical lake (East Africa). Vertical variations of N2O were modest, with ranges of 6–9 and 0–16 nmol L−1 in surface and bottom waters, respectively, and occasionally peaks of N2O (up to 58 nmol L−1) were observed at the oxic-anoxic interface. On the contrary, steep vertical gradients of CH4 were observed with values changing several orders of magnitude from surface (19–103 nmol L−1) to 70 m (~113,000–520,000 nmol L−1). Seasonal variations of CH4 were caused by annual cycles of mixing and stratification, during the dry and rainy seasons, respectively. This mixing allowed the establishment of a thick oxic layer (maximum 65 m deep), leading to decreased CH4 concentrations (minimum of 8 nmol L−1), presumably due to bacterial CH4 oxidation. During the stratification period, the oxic mixed layer was thinner (minimum 25 m deep), and an increase of CH4 concentrations in surface waters was observed (maximum of 103 nmol L−1), probably due to a lower integrated CH4 oxidation on the water column. Lake Kivu seasonally alternated between a source and a sink for atmospheric N2O, but on an annual scale was a small source of N2O to the atmosphere (on average 0.43 µmol m−2 day−1), while it was a small source of CH4 to the atmosphere throughout the year (on average 86 µmol m−2 day−1). Vertical and seasonal variations of N2O are discussed in terms of nitrification and denitrification, although from the present data-set it is not possible to unambiguously identify the main drivers of N2O production.

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.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • APHA (1998) Standard methods for the examination of water and wastewater. American Public Health Association, USA

  • Bartlett KB, Crill PM, Bonassi JA, Richey JE, Harriss RC (1990) Methane flux from the Amazon River floodplain: emissions during rising water. J Geophys Res 95:16773–716788

    Article  CAS  Google Scholar 

  • Bastviken D, Cole J, Pace M, Tranvik L (2004) Methane emissions from lakes: dependence of lake characteristics, two regional assessments, and a global estimate. Glob Biogeochem Cy 18:GB4009. doi:10.1029/2004GB002238

    Article  Google Scholar 

  • Bastviken D, Santoro AL, Marotta H, Pinho LQ, Calheiros DF, Crill P, Enrich-Prast A (2010) Methane emissions from pantanal, South America, during the low water season: toward more comprehensive sampling. Environ Sci Technol 44:5450–5455

    Article  CAS  PubMed  Google Scholar 

  • Bastviken D, Tranvik LJ, Downing JA, Crill PM, Enrich-Prast A (2011) Freshwater methane emissions offset the continental carbon sink. Science 331:50

    Article  CAS  PubMed  Google Scholar 

  • Baulch HM, Schiff SL, Maranger R, Dillon PJ (2011) Nitrogen enrichment and the emission of nitrous oxide from streams. Glob Biogeochem Cy 25:GB4013. doi:10.1029/2011GB004047

    Article  Google Scholar 

  • Borges AV, Abril G, Delille B, Descy J-P, Darchambeau F (2011) Diffusive methane emissions to the atmosphere from Lake Kivu (Eastern Africa). J Geophys Res 116:G03032. doi:10.1029/2011JG001673

    Article  Google Scholar 

  • Borges AV, Bouillon S, Abril G, Delille B, Poirier D, Commarieu M-V, Lepoint G, Morana C, Champenois W, Servais P (2012) Variability of carbon dioxide and methane in the epilimnion of Lake Kivu. In: Descy JP, Darchambeau F, Schmid M (eds) Lake Kivu-Limnology and biogeochemistry of a tropical great lake. Springer, New York London, pp 47–66

    Google Scholar 

  • Borges AV, Morana C, Bouillon S, Servais P, Descy J-P, Darchambeau F (2014) Carbon cycling of Lake Kivu (East Africa): net autotrophy in the epilimnion and emission of CO2 to the atmosphere sustained by geogenic inputs. PLoS One 9:e109500

    Article  PubMed  PubMed Central  Google Scholar 

  • Borges AV, Darchambeau F, Teodoru CR, Marwick TR, Tamooh F, Geeraert N, Omengo FO, Guérin F, Lambert T, Morana C, Okuku E, Bouillon S (2015a) Globally significant greenhouse gas emissions from African inland waters. Nat Geosci 8:637–642

    Article  CAS  Google Scholar 

  • Borges AV, Abril G, Darchambeau F, Teodoru CR, Deborde J, Vidal LO, Lambert T, Bouillon S (2015b) Divergent biophysical controls of aquatic CO2 and CH4 in the World’s two largest rivers. Sci Rep 5

  • Borrel G, Jézéquel D, Biderre-Petit C, Morel-Desrosiers N, Morel J-P, Peyret P, Fonty G, Lehours A-C (2011) Production and consumption of methane in freshwater lake ecosystems. Res Microbiol 162:832–847

    Article  CAS  PubMed  Google Scholar 

  • Cole JJ, Caraco NF (1998) Atmospheric exchange of carbon dioxide in a low-wind oligotrophic lake measured by the addition of SF6. Limnol Oceanogr 43:647–656

    Article  CAS  Google Scholar 

  • Crowe S, Katsev S, Leslie K, Sturm A, Magen C, Nomosatryo S, Pack M, Kessler J, Reeburgh W, Roberts J (2011) The methane cycle in ferruginous Lake Matano. Geobiology 9:61–78

    Article  CAS  PubMed  Google Scholar 

  • Darchambeau F, Sarmento H, Descy JP (2014) Primary production in a tropical large lake: the role of phytoplankton composition. Sci Total Environ 473–474:178–188

    Article  PubMed  Google Scholar 

  • Degens ET, von Herzen RP, Wong H-K, Deuser WG, Jannasch HW (1973) Lake Kivu: structure, chemistry and biology of an East African rift lake. Geol Rundsch 62:245–277

    Article  CAS  Google Scholar 

  • Devol AH, Richey JE, Forsberg BR, Martinelli LA (1990) Seasonal dynamics in methane emissions from the Amazon River floodplain to the troposphere. J Geophys Res 95:16417–416426

    Article  CAS  Google Scholar 

  • Engle D, Melack JM (2000) Methane emissions from an Amazon floodplain lake: enhanced release during episodic mixing and during falling water. Biogeochemistry 51:71–90

    Article  CAS  Google Scholar 

  • Hofmann H (2013) Spatiotemporal distribution patterns of dissolved methane in lakes: how accurate are the current estimations of the diffusive flux path? Geophys Res Lett 40:2779–2784

    Article  CAS  Google Scholar 

  • Holgerson MA, Raymond PA (2016) Large contribution to inland water CO2 and CH4 emissions from very small ponds. Nat Geosci 9:222–226

    Article  CAS  Google Scholar 

  • İnceoğlu Ö, Llirós M, García-Armisen T, Crowe SA, Michiels C, Darchambeau F, Descy J-P, Servais P (2015a) Distribution of bacteria and archaea in meromictic tropical Lake Kivu (Africa). Aquat Microb Ecol 74:215–233

    Article  Google Scholar 

  • İnceoğlu Ö, Llirós M, Crowe S, García-Armisen T, Morana C, Darchambeau F, Borges A, Descy J-P, Servais P (2015b) Vertical distribution of functional potential and active microbial communities in meromictic Lake Kivu. Microb Ecol 70:596–611

    Article  PubMed  Google Scholar 

  • IPCC (2013) Climate change: the physical science basis. Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. United Kingdom, USA

  • Iversen N, Oremland RS, Klug MJ (1987) Big Soda Lake (Nevada). 3. Pelagic methanogenesis and anaerobic methane oxidation. Limnol Oceanogr 32:804–814

    Article  CAS  Google Scholar 

  • Kankaala P, Huotari J, Tulonen T, Ojala A (2013) Lake-size dependent physical forcing drives carbon dioxide and methane effluxes from lakes in a boreal landscape. Limnol Oceanogr 58:1915–1930

    Article  CAS  Google Scholar 

  • Kirschke S, Bousquet P, Ciais P, Saunois M, Canadell JG, Dlugokencky EJ, Bergamaschi P, Bergmann D, Blake DR, Bruhwiler L, Cameron-Smith P, Castaldi S, Chevallier F, Feng L, Fraser A, Heimann M, Hodson EL, Houweling S, Josse B, Fraser PJ, Krummel PB, Lamarque JF, Langenfelds RL, Le Quéré C, Naik V, O’Doherty S, Palmer PI, Pison I, Plummer D, Poulter B, Prinn RG, Rigby M, Ringeval B, Santini M, Schmidt M, Shindell DT, Simpson IJ, Spahni R, Steele LP, Strode SA, Sudo K, Szopa S, Van Der Werf GR, Voulgarakis A, Van Weele M, Weiss RF, Williams JE, Zeng G (2013) Three decades of global methane sources and sinks. Nat Geosci 6:813–823

    Article  CAS  Google Scholar 

  • Llirós M, Gich F, Plasencia A, Auguet JC, Darchambeau F, Casamayor EO, Descy JP, Borrego C (2010) Vertical distribution of ammonia-oxidizing crenarchaeota and methanogens in the epipelagic waters of lake kivu (Rwanda-Democratic Republic of the Congo). Appl Environ Microbiol 76:6853–6863

    Article  PubMed  PubMed Central  Google Scholar 

  • Marotta H, Pinho L, Gudasz C, Bastviken D, Tranvik LJ, Enrich-Prast A (2014) Greenhouse gas production in low-latitude lake sediments responds strongly to warming. Nature Clim Change 4:467–470

    Article  CAS  Google Scholar 

  • Melack JM, Hess LL, Gastil M, Forsberg BR, Hamilton SK, Lima IBT, Novo EMLM (2004) Regionalization of methane emissions in the Amazon Basin with microwave remote sensing. Glob Change Biol 10:530–544

    Article  Google Scholar 

  • Mengis M, Gächter R, Wehrli B (1997) Sources and sinks of nitrous oxide (N2O) in deep lakes. Biogeochemistry 38:281–301

    Article  CAS  Google Scholar 

  • Miettinen H, Pumpanen J, Heiskanen JJ, Aaltonen H, Mammarella I, Ojala A, Levula J, Rantakari M (2015) Towards a more comprehensive understanding of lacustrine greenhouse gas dynamics—two-year measurements of concentrations and fluxes of CO2, CH4 and N2O in a typical boreal lake surrounded by managed forests. Boreal Environ Res 20:75–89

    Google Scholar 

  • Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide Biol Chem 5:62–71

    Article  CAS  Google Scholar 

  • Morana C, Sarmento H, Descy JP, Gasol JM, Borges AV, Bouillon S, Darchambeau F (2014) Production of dissolved organic matter by phytoplankton and its uptake by heterotrophic prokaryotes in large tropical lakes. Limnol Oceanogr 59:1364–1375

    Article  CAS  Google Scholar 

  • Morana C, Darchambeau F, Roland FAE, Borges AV, Muvundja FA, Kelemen Z, Masilya P, Descy JP, Bouillon S (2015a) Biogeochemistry of a large and deep tropical lake (Lake Kivu, East Africa): insights from a stable isotope study covering an annual cycle. Biogeosciences 12:4953–4963

    Article  Google Scholar 

  • Morana C, Borges AV, Roland FAE, Darchambeau F, Descy JP, Bouillon S (2015b) Methanotrophy within the water column of a large meromictic tropical lake (Lake Kivu, East Africa). Biogeosciences 12:2077–2088

    Article  CAS  Google Scholar 

  • Natchimuthu S, Sundgren I, Gålfalk M, Klemedtsson L, Crill P, Danielsson Å, Bastviken D (2015) Spatio-temporal variability of lake CH4 fluxes and its influence on annual whole lake emission estimates. Limnol Oceanogr. doi:10.1002/lno.10222

    Google Scholar 

  • Nayar A (2009) Earth science: a lakeful of trouble. Nature News 460:321–323

    Article  CAS  Google Scholar 

  • Pasche N, Dinkel C, Muller B, Schmid M, Wuëst A, Wehrli B (2009) Physical and biogeochemical limits to internal nutrient loading of meromictic lake kivu. Limnol Oceanogr 54:1863–1873

    Article  CAS  Google Scholar 

  • Pasche N, Schmid M, Vazquez F, Schubert CJ, Wüest A, Kessler JD, Pack MA, Reeburgh WS, Bürgmann H (2011) Methane sources and sinks in Lake Kivu. J Geophys Res 116:G03006. doi:10.1029/2011JG001690

    Article  Google Scholar 

  • Podgrajsek E, Sahlée E, Rutgersson A (2014) Diurnal cycle of lake methane flux. J Geophys Res Biogeosci 119:236–248

    Article  CAS  Google Scholar 

  • Polsenaere P, Deborde J, Detandt G, Vidal LO, Pérez MA, Marieu V, Abril G (2013) Thermal enhancement of gas transfer velocity of CO2 in an Amazon floodplain lake revealed by eddy covariance measurements. Geophys Res Lett 40:1734–1740

    Article  CAS  Google Scholar 

  • Read JS, Hamilton DP, Desai AR, Rose KC, MacIntyre S, Lenters JD, Smyth RL, Hanson PC, Cole JJ, Staehr PA (2012) Lake‐size dependency of wind shear and convection as controls on gas exchange. Geophys Res Lett 39:L09405. doi:10.1029/2012GL051886

    Article  Google Scholar 

  • Riera JL, Schindler JE, Kratz TK (1999) Seasonal dynamics of carbon dioxide and methane in two clear-water lakes and two bog lakes in northern Wisconsin, USA. Can J Fish Aquat Sci 56:265–274

    Article  Google Scholar 

  • Saad OALO, Conrad R (1993) Temperature dependence of nitrification, denitrification, and turnover of nitric oxide in different soils. Biol Fertil Soils 15:21–27

    Article  CAS  Google Scholar 

  • Sawakuchi HO, Bastviken D, Sawakuchi AO, Krusche AV, Ballester MV, Richey JE (2014) Methane emissions from Amazonian Rivers and their contribution to the global methane budget. Glob Change Biol 20:2829–2840

    Article  Google Scholar 

  • Schilder J, Bastviken D, Hardenbroek M, Kankaala P, Rinta P, Stötter T, Heiri O (2013) Spatial heterogeneity and lake morphology affect diffusive greenhouse gas emission estimates of lakes. Geophys Res Lett 40:5752–5756

    Article  CAS  Google Scholar 

  • Schmid M, Wüest A (2012) Stratification, mixing and transport processes in Lake Kivu. In: Descy JP, Darchambeau F, Schmid M (eds) Lake Kivu: limnology and biogeochemistry of a tropical great lake. Springer, New York, London

    Google Scholar 

  • Schmid M, Halbwachs M, Wehrli B, Wüest A (2005) Weak mixing in Lake Kivu: New insights indicate increasing risk of uncontrolled gas eruption. Geochem Geophys Geosyst 6:Q07009. doi:10.1029/2004GC000892

    Article  Google Scholar 

  • Schmidt W (1928) Über die Temperatur- und Stabilitätsverhältnisse von Seen. Geogr Ann 10:145–177

    Google Scholar 

  • Schubert CJ, Lucas F, Durisch-Kaiser E, Stierli R, Diem T, Scheidegger O, Vazquez F, Müller B (2010) Oxidation and emission of methane in a monomictic lake (Rotsee, Switzerland). Aquat Sci 72:455–466

    Article  CAS  Google Scholar 

  • Seitzinger S, Harrison JA, Böhlke JK, Bouwman AF, Lowrance R, Peterson B, Tobias C, Van Drecht G (2006) Denitrification across landscapes and waterscapes: a synthesis. Ecol Appl 16:2064–2090

    Article  CAS  PubMed  Google Scholar 

  • Smith LK, Lewis WM Jr (1992) Seasonality of methane emissions from five lakes and associated wetlands of the Colorado Rockies. Glob Biogeochem Cy 6:323–338

    Article  CAS  Google Scholar 

  • Stahl DA, De La Torre JR (2012) Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol 66:83–101

    Article  CAS  PubMed  Google Scholar 

  • Stieglmeier M, Mooshammer M, Kitzler B, Wanek W, Zechmeister-Boltenstern S, Richter A, Schleper C (2014) Aerobic nitrous oxide production through N-nitrosating hybrid formation in ammonia-oxidizing archaea. ISME J 8:1135–1146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tassi F, Vaselli O, Tedesco D, Montegrossi G, Darrah T, Cuoco E, Mapendano MY, Poreda R, Delgado Huertas A (2009) Water and gas chemistry at Lake Kivu (DRC): geochemical evidence of vertical and horizontal heterogeneities in a multibasin structure. Geochem Geophys Geosyst 10:Q02005. doi:10.1029/2008GC002191

    Article  Google Scholar 

  • Thiery W, Martynov A, Darchambeau F, Descy JP, Plisnier PD, Sushama L, van Lipzig NPM (2014) Understanding the performance of the FLake model over two African Great Lakes. Geosci Model Dev 7:317–337

    Article  Google Scholar 

  • Weiss RF (1981) Determinations of carbon dioxide and methane by dual catalyst flame ionization chromatography and nitrous oxide by electron capture chromatography. J Chromatogr Sci 19:611–616

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Westwood D (1981) Ammonia in waters (ed) Methods for the examination of waters and associated materials. HMSO, London

  • Winfrey M, Zeikus J (1979) Microbial methanogenesis and acetate metabolism in a meromictic lake. Appl Environ Microbiol 37:213–221

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xiao W, Liu S, Li H, Xiao Q, Wang W, Hu Z, Hu C, Gao Y, Shen J, Zhao X, Zhang M, Lee X (2014) A flux-gradient system for simultaneous measurement of the CH4, CO2, and H2O fluxes at a lake-air interface. Environ Sci Technol 48:14490–14498

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto S, Alcauskas JB, Crozier TE (1976) Solubility of methane in distilled water and seawater. J Chem Eng Data 21:78–80

    Article  CAS  Google Scholar 

  • Yvon-Durocher G, Allen AP, Bastviken D, Conrad R, Gudasz C, St-Pierre A, Thanh-Duc N, del Giorgio PA (2014) Methane fluxes show consistent temperature dependence across microbial to ecosystem scales. Nature 507:488–491

    Article  CAS  PubMed  Google Scholar 

  • Zhang GL, Zhang J, Liu SM, Ren JL, Zhao YC (2010) Nitrous oxide in the Changjiang (Yangtze River) Estuary and its adjacent marine area: riverine input, sediment release and atmospheric fluxes. Biogeosciences 7:3505–3516

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Boniface Kaningini, Pascal Isumbisho, Georges Alunga, Fabrice Muvundja and Pascal Masilya (Institut Supérieur Pédagogique, Bukavu, DRC) for logistic support for the monitoring, and providing the meteorological data, Professor Jean-Pierre Thomé (University of Liège, ULg) for access to the multi-plate reader, and Marc-Vincent Commarieu (ULg) for help in analyses. This study was funded by the Belgian Federal Science Policy Office (BELSPO, Belgium) under the EAGLES (East African Great lake Ecosystem Sensitivity to Changes, SD/AR/02A) project, by the Fonds National de la Recherche Scientifique (FNRS) under the MICKI (Microbial diversity and processes in Lake Kivu, 1715859) project, and contributes to the European Research Council (ERC) starting grant AFRIVAL (African river basins: Catchment-scale carbon fluxes and transformations, 240002). A.V.B is a senior research associated to the FNRS. F.A.E.R received a PhD grant from FNRS (Fonds pour la Formation à la Recherche dans l’Industrie et dans l’Agriculture).

Author information

Authors and Affiliations

  1. Chemical Oceanography Unit, University of Liège, Liège, Belgium

    Fleur A. E. Roland, François Darchambeau & Alberto V. Borges

  2. Department of Earth and Environmental Sciences, KU Leuven, Louvain, Belgium

    Cédric Morana

Authors
  1. Fleur A. E. Roland
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. François Darchambeau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cédric Morana
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alberto V. Borges
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Fleur A. E. Roland.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 234 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Roland, F.A.E., Darchambeau, F., Morana, C. et al. Nitrous oxide and methane seasonal variability in the epilimnion of a large tropical meromictic lake (Lake Kivu, East-Africa). Aquat Sci 79, 209–218 (2017). https://doi.org/10.1007/s00027-016-0491-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00027-016-0491-2

Keywords

Search

Navigation