Aquatic Sciences

, Volume 79, Issue 2, pp 209–218 | Cite as

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

  • Fleur A. E. Roland
  • François Darchambeau
  • Cédric Morana
  • Alberto V. Borges
Research Article

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.

Keywords

Nitrous oxide Methane Tropical lake Lake Kivu 

Notes

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).

Supplementary material

27_2016_491_MOESM1_ESM.docx (235 kb)
Supplementary material 1 (DOCX 234 kb)

References

  1. APHA (1998) Standard methods for the examination of water and wastewater. American Public Health Association, USAGoogle Scholar
  2. 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 95:16773–716788CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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 44:5450–5455CrossRefPubMedGoogle Scholar
  5. Bastviken D, Tranvik LJ, Downing JA, Crill PM, Enrich-Prast A (2011) Freshwater methane emissions offset the continental carbon sink. Science 331:50CrossRefPubMedGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. 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 CrossRefGoogle Scholar
  8. 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 47–66Google Scholar
  9. 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:e109500CrossRefPubMedPubMedCentralGoogle Scholar
  10. 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 8:637–642CrossRefGoogle Scholar
  11. 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 5Google Scholar
  12. 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 162:832–847CrossRefPubMedGoogle Scholar
  13. Cole JJ, Caraco NF (1998) Atmospheric exchange of carbon dioxide in a low-wind oligotrophic lake measured by the addition of SF6. Limnol Oceanogr 43:647–656CrossRefGoogle Scholar
  14. 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 9:61–78CrossRefPubMedGoogle Scholar
  15. Darchambeau F, Sarmento H, Descy JP (2014) Primary production in a tropical large lake: the role of phytoplankton composition. Sci Total Environ 473–474:178–188CrossRefPubMedGoogle Scholar
  16. 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 62:245–277CrossRefGoogle Scholar
  17. 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 95:16417–416426CrossRefGoogle Scholar
  18. Engle D, Melack JM (2000) Methane emissions from an Amazon floodplain lake: enhanced release during episodic mixing and during falling water. Biogeochemistry 51:71–90CrossRefGoogle Scholar
  19. 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 40:2779–2784CrossRefGoogle Scholar
  20. Holgerson MA, Raymond PA (2016) Large contribution to inland water CO2 and CH4 emissions from very small ponds. Nat Geosci 9:222–226CrossRefGoogle Scholar
  21. 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 74:215–233CrossRefGoogle Scholar
  22. 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 70:596–611CrossRefPubMedGoogle Scholar
  23. 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, USAGoogle Scholar
  24. Iversen N, Oremland RS, Klug MJ (1987) Big Soda Lake (Nevada). 3. Pelagic methanogenesis and anaerobic methane oxidation. Limnol Oceanogr 32:804–814CrossRefGoogle Scholar
  25. 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 58:1915–1930CrossRefGoogle Scholar
  26. 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 6:813–823CrossRefGoogle Scholar
  27. 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 76:6853–6863CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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 4:467–470CrossRefGoogle Scholar
  29. 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 10:530–544CrossRefGoogle Scholar
  30. Mengis M, Gächter R, Wehrli B (1997) Sources and sinks of nitrous oxide (N2O) in deep lakes. Biogeochemistry 38:281–301CrossRefGoogle Scholar
  31. 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 20:75–89Google Scholar
  32. Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide Biol Chem 5:62–71CrossRefGoogle Scholar
  33. 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 59:1364–1375CrossRefGoogle Scholar
  34. 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 12:4953–4963CrossRefGoogle Scholar
  35. 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 12:2077–2088CrossRefGoogle Scholar
  36. 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
  37. Nayar A (2009) Earth science: a lakeful of trouble. Nature News 460:321–323CrossRefGoogle Scholar
  38. 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 54:1863–1873CrossRefGoogle Scholar
  39. 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 CrossRefGoogle Scholar
  40. Podgrajsek E, Sahlée E, Rutgersson A (2014) Diurnal cycle of lake methane flux. J Geophys Res Biogeosci 119:236–248CrossRefGoogle Scholar
  41. 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 40:1734–1740CrossRefGoogle Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 56:265–274CrossRefGoogle Scholar
  44. Saad OALO, Conrad R (1993) Temperature dependence of nitrification, denitrification, and turnover of nitric oxide in different soils. Biol Fertil Soils 15:21–27CrossRefGoogle Scholar
  45. 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 20:2829–2840CrossRefGoogle Scholar
  46. 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 40:5752–5756CrossRefGoogle Scholar
  47. 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, LondonGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. Schmidt W (1928) Über die Temperatur- und Stabilitätsverhältnisse von Seen. Geogr Ann 10:145–177Google Scholar
  50. 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 72:455–466CrossRefGoogle Scholar
  51. 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 16:2064–2090CrossRefPubMedGoogle Scholar
  52. Smith LK, Lewis WM Jr (1992) Seasonality of methane emissions from five lakes and associated wetlands of the Colorado Rockies. Glob Biogeochem Cy 6:323–338CrossRefGoogle Scholar
  53. Stahl DA, De La Torre JR (2012) Physiology and diversity of ammonia-oxidizing archaea. Annu Rev Microbiol 66:83–101CrossRefPubMedGoogle Scholar
  54. 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 8:1135–1146CrossRefPubMedPubMedCentralGoogle Scholar
  55. 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 CrossRefGoogle Scholar
  56. 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 7:317–337CrossRefGoogle Scholar
  57. 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 19:611–616CrossRefGoogle Scholar
  58. Weiss RF, Price BA (1980) Nitrous oxide solubility in water and seawater. Mar Chem 8:347–359CrossRefGoogle Scholar
  59. Westwood D (1981) Ammonia in waters (ed) Methods for the examination of waters and associated materials. HMSO, LondonGoogle Scholar
  60. Winfrey M, Zeikus J (1979) Microbial methanogenesis and acetate metabolism in a meromictic lake. Appl Environ Microbiol 37:213–221PubMedPubMedCentralGoogle Scholar
  61. 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 48:14490–14498CrossRefPubMedGoogle Scholar
  62. Yamamoto S, Alcauskas JB, Crozier TE (1976) Solubility of methane in distilled water and seawater. J Chem Eng Data 21:78–80CrossRefGoogle Scholar
  63. 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 507:488–491CrossRefPubMedGoogle Scholar
  64. 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 7:3505–3516CrossRefGoogle Scholar

Copyright information

© Springer International Publishing 2016

Authors and Affiliations

  • Fleur A. E. Roland
    • 1
  • François Darchambeau
    • 1
  • Cédric Morana
    • 2
  • Alberto V. Borges
    • 1
  1. 1.Chemical Oceanography UnitUniversity of LiègeLiègeBelgium
  2. 2.Department of Earth and Environmental SciencesKU LeuvenLouvainBelgium

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