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Consequences for pelagic energy mobilisation of a sudden browning episode without a clear increase in DOC concentration: a case of a boreal pristine lake

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Abstract

In the boreal zone, episodes of heavy rains are among the most conspicuous events disturbing aquatic ecosystems. Due to climate change they are predicted to become more frequent and intense, leading on browning of lakes. We assessed the possible effects of heavy rains to DOC concentration and water colour and resulting impacts on functioning of a headwater lake with naturally high water colour and concentration of allochthonous DOC. The weekly measurements were carried out in summers 2002–2004; the first 2 years had normal and the last year very high summer precipitation. The rains resulted in rapid increase in water colour, but not in DOC. We hypothesised that due to browning, irrespective of whether it stems from an increase in brownish DOC or other coloured substances, photosynthesis decreases, bacterial activity increases, and the lake becomes more heterotrophic. We also anticipated that due to strengthened heterotrophy, the period with apparent net autotrophy and CO2 flux onto the lake would disappear. To test our hypothesis, we measured autotrophic inorganic carbon uptake of photosynthetic organisms as well as dark fixation of inorganic carbon, community respiration and leucine uptake. Finally, we compared the results to CO2 flux measurements with an eddy covariance technique. Our hypotheses were only partly supported since there were no drastic changes in any of the metabolic processes measured. Although the lake ecosystem became slightly more heterotrophic, primary production was still occasionally higher than community respiration and the lake could act as a sink of CO2. Thus regarding metabolic processes, the ecosystem of this pristine lake was not strongly disturbed by the sudden browning episode.

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References

  • Algesten G, Sobek S, Bergström A-K, Ågren A, Tranvik LJ, Jansson M (2003) Role of lakes for organic carbon cycling in the boreal zone. Glob Change Biol 10:141–147

    Article  Google Scholar 

  • Arvola L, Rask M, Ruuhijärvi J, Tulonen T, Vuorenmaa J, Ruoho-Airola T, Tulonen J (2010) Long-term patterns in pH and colour in small acidic boreal lakes of varying hydrological and landscape settings. Biogeochemistry 101:269–279

    Article  Google Scholar 

  • Arvola L, Salonen K, Keskitalo J, Tulonen T, Järvinen M, Huotari J (2014) Plankton metabolism and sedimentation in a small boreal lake—a long-term perspective. Boreal Environ Res 19:83–96

    CAS  Google Scholar 

  • Ask J, Karlsson J, Jansson M (2012) Net ecosystem production in clear-water and brown-water lakes. Global Biochem Cycles. doi:10.1029/2010GB003951

    Google Scholar 

  • Barbiero RP, James WF, Barko JW (1999) The effects of disturbance events on phytoplankton community structure in a small temperate reservoir. Freshw Biol 42:503–512

    Article  Google Scholar 

  • Bertrand G, Danger M, Abbadie L, Lacroix G (2010) Priming effect: bridging the gap between terrestrial and aquatic ecology. Ecology 91:2850–2861

    Article  Google Scholar 

  • Brothers S, Köhler J, Attermeyer K, Grossart HP, Mehner T, Meyer N, Scharnweber K, Hilt S (2014) A feedback loop links brownification and anoxia in a temperate, shallow lake. Limnol Oceanogr 59:1388–1398

    Article  CAS  Google Scholar 

  • Casamayor EO, Garcia-Cantizano J, Pedrós-Alió C (2008) Carbon dioxide fixation in the dark by photosynthetic bacteria in sulfide-rich stratified lakes with oxic-anoxic interfaces. Limnol Oceanogr 53:1193–1203

    Article  CAS  Google Scholar 

  • Catalán N, Kellerman AM, Peter H, Carmona F, Tranvik LJ (2015) Absence of a priming effect on dissolved organic carbon degradation in lake water. Limnol Oceanogr 69:159–168

    Article  Google Scholar 

  • Clark JM, Botterell SH, Evans CD, Monteith DT, Bartlett R, Rose R, Newton RJ, Chapman PJ (2010) The importance of the relationship between scale and process in understanding long-term DOC dynamics. Sci Total Environ 408:2768–2775

    Article  CAS  PubMed  Google Scholar 

  • Cole JJ, Pace ML (1995) Bacterial secondary production in oxic and anoxic freshwaters. Limnol Oceanogr 40:1019–1027

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • del Giorgio PA, Cole JJ, Cembleris A (1997) Respiration rates in bacteria exceed phytoplankton production in unproductive aquatic systems. Nature 385:148–151

    Article  Google Scholar 

  • Dhillon GS, Inamdar S (2014) Storm event patterns of particulate organic carbon (POC) for large storms and differences with dissolved organic carbon (DOC). Biogeochemistry 118:61–81

    Article  CAS  Google Scholar 

  • Drakare S, Blomqvist P, Bergström A-K, Jansson M (2002) Primary production and phytoplankton composition in relation to DOC input and bacterioplankton production in humic Lake Örträsket. Freshw Biol 47:41–52

    Article  CAS  Google Scholar 

  • Duarte CM, Prairie YT (2005) Prevalence of heterotrophy and atmospheric CO2 emissions from aquatic ecosystems. Ecosystems 8:862–870

    Article  CAS  Google Scholar 

  • Dyson KE, Billett MF, Dinsmore KJ, Harvey F, Thomson AM, Piirainen S, Kortelainen P (2011) Release of aquatic carbon from two peatland catchments in E. Finland during the spring snowmelt period. Biogeochemistry 103:125–142

    Article  Google Scholar 

  • Felip M, Pace ML, Cole JJ (1996) Regulation of planktonic bacterial growth rates: the effects of temperature and resources. Microb Ecol 31:15–28

    Article  CAS  PubMed  Google Scholar 

  • Flynn KJ, Stoecker DK, Mitra A, Raven JA, Glibert PM, Hansen PJ, Granéli E, Burkholder JM (2013) Misuse of the phytoplankton–zooplankton dichotomy: the need to assign organisms as mixotrophs within plankton functional types. J Plankton Res 35:3–11

    Article  Google Scholar 

  • Forsström L, Roiha T, Rautio M (2013) Responses of microbial food web to increased allochthonous DOM in an oligotrophic subarctic lake. Aquat Microb Ecol 68:171–184

    Article  Google Scholar 

  • Granéli E, Carlsson P, Legrand C (1999) The role of C, N and P in dissolved and particulate organic matter as a nutrient source for phytoplankton growth, including toxic species. Aquat Ecol 33:17–27

    Article  Google Scholar 

  • Guenet B, Danger M, Harrault L, Allard B, Jauset-Alcala M, Bardoux G, Benest D, Lacroix G (2014) Fast mineralization of land-born C in inland waters: first experimental evidences of aquatic priming effect. Hydrobiologia 721:35–44

    Article  CAS  Google Scholar 

  • Hessen D (1992) Dissolved organic carbon in a humic lake: effects on bacterial production and respiration. Hydrobiologia 229:115–123

    Article  CAS  Google Scholar 

  • Hongve D (1997) Cycling of iron, manganese, and phosphate in a meromictic lake. Limnol Oceanogr 42:635–647

    Article  CAS  Google Scholar 

  • Huotari J, Ojala A, Peltomaa E, Nordbo A, Launiainen S, Pumpanen J, Rasilo T, Hari P, Vesala T (2011) Long-term direct CO2 flux measurements over a boreal lake: five years of eddy covariance data. Geophys Res Lett. doi:10.1029/2011GL048753

    Google Scholar 

  • Ilmavirta V (1988) Phytoflagellates and their ecology in Finnish brown-water lakes. Hydrobiologia 161:255–270

    Article  CAS  Google Scholar 

  • Jones RI (1992) The influence of humic substances on lacustrine planktonic food chains. Hydrobiologia 229:73–91

    Article  CAS  Google Scholar 

  • Jylhä K, Laapas M, Ruosteenoja K, Arvola L, Drebs A, Kersalo J, Saku S, Gregow H, Hannula H-R, Pirinen P (2014) Climate variability and trends in the Valkea-Kotinen region, southern Finland: comparisons between past, current and projected climates. Boreal Environ Res 19(suppl A):4–30

    Google Scholar 

  • Kamjunke N, Tittel J (2008) Utilization of leucine by several phytoplankton species. Limnologica 38:360–366

    Article  Google Scholar 

  • Kankaala P, Lopez Bellido J, Ojala A, Tulonen T, Jones RI (2013) Variable production by different pelagic energy mobilizers in boreal lakes. Ecosystems 16:1152–1164

    Article  CAS  Google Scholar 

  • Keskitalo J, Salonen K (1994) Manual for integrated monitoring. Subprogram Hydrobiology of Lakes. Publications of the Water and Environment Administration—series B 16. National Board of Waters and the Environment, Finland

  • Kirschner AKT, Eiler A, Zechmeister TC, Velimirov B, Herzig A, Mach R, Farnleiter AH (2002) Extremely productive microbial communities in shallow saline pools respond immediately to changing meteorological conditions. Environ Microbiol 4:546–555

    Article  CAS  PubMed  Google Scholar 

  • Köhler SJ, Kothawala D, Futter MN, Liungman O, Tranvik L (2013) In-lake processes offset increased terrestrial inputs of dissolved organic carbon and color to lakes. PLoS ONE. doi:10.1371/journal.pone.007059

    Google Scholar 

  • Kortelainen P (1993) Content of organic carbon in Finnish lakes and its relationship to catchment characteristics. Can J Fish Aquat Sci 50:1477–1483

    Article  CAS  Google Scholar 

  • Kovats RS, Valentini R, Bouwer LM, Georgopoulou E, Jacob D, Martin E, Rounsevell M, Soussana JF (2014) Europe. In: Barros VR, Field CB, Dokken DJ, Mastrandrea MD, Mach KJ, Bili TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Climate change 2014: impacts, adaptation, and vulnerability. Part B: regional aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, pp 1267–1326

  • Kritzberg ES, Ekström SM (2012) Increasing iron concentrations in surface waters—a factor behind brownification? Biogeosciences 9:1465–1478

    Article  CAS  Google Scholar 

  • Lepistö L, Rosenström U (1998) The most typical phytoplankton taxa in four types of boreal lakes. Hydrobiologia 369(370):89–97

    Article  Google Scholar 

  • Lewis TL, Lindberg MS, Schmutz JA, Bertram MR (2014) Multi-trophic resilience of boreal lake ecosystems to forest fires. Ecology 95:1253–1263

    Article  PubMed  Google Scholar 

  • Lopez Bellido J, Peltomaa E, Ojala A (2011) An urban boreal lake basin as a source of CO2 and CH4. Environ Pollut 159:1649–1659

    Article  CAS  PubMed  Google Scholar 

  • Maloney KO, Morris DP, Moses CO, Osburn CL (2005) The role of iron and dissolved organic carbon in the absorption of ultraviolet radiation in humic lake water. Biogeochemistry 75:393–407

    Article  CAS  Google Scholar 

  • Moran MA, Hodson RE (1990) Bacterial production on humic and non humic components of dissolved organic carbon. Limnol Oceanogr 35:1744–1756

    Article  CAS  Google Scholar 

  • Nilsson SI (1985) Budgets of aluminium species, iron and manganese in the Lake Gårdsjön catchment in SW Sweden. Ecol Bull 37:120–132

    Google Scholar 

  • Nordbo A, Launiainen S, Mammarella I, Leppäranta M, Huotari J, Ojala A, Vesala T (2011) Long-term energy flux measurements and energy balance over a small boreal lake using eddy covariance technique. J Geophys Res. doi:10.1029/2010JD014542

    Google Scholar 

  • Ojala A, López Bellido J, Tulonen T, Kankaala P, Huotari J (2011) Carbon gas fluxes from a brown-water and clear-water lake in the boreal zone during a summer with extreme rain events. Limnol Oceanogr 56:61–76

    Article  CAS  Google Scholar 

  • Peltomaa E, Ojala A (2010) Size-related photosynthesis of algae in a strongly stratified humic lake. J Plankton Res 32:341–355

    Article  Google Scholar 

  • Peltomaa E, Ojala A (2012) Meteorological drivers of the dynamics of autotrophic picoplankton. Freshw Biol 57:1005–1016

    Article  Google Scholar 

  • Peltomaa E, Zingel P, Ojala A (2013a) Weak response of the microbial food web of a boreal humic lake to hypolimnetic anoxia. Aquat Microb Ecol 68:91–105

    Article  Google Scholar 

  • Peltomaa E, Ojala A, Holopainen A-L, Salonen K (2013b) Changes in phytoplankton in a boreal lake during a 14-year period. Boreal Environ Res 18:387–400

    CAS  Google Scholar 

  • Puskaric S, Mortain-Bertrand A (2003) Physiology of diatom Skeletonema costatum (Grev.) Cleve photosynthetic extracellular release: evidence for a novel coupling between marine bacteria and phytoplankton. J Plankton Res 25:1227–1235

    Article  CAS  Google Scholar 

  • Rasilo T, Ojala A, Huotari J, Pumpanen J (2012) Rain induced changes in carbon dioxide concentrations in the soil-lake-brook continuum of a boreal forested catchment. Vadose Zone J. doi:10.2136/vzj2011.0039

    Google Scholar 

  • Rasilo T, Ojala A, Huotari J, Starr M, Pumpanen J (2015) Concentrations and quality of DOC along the terrestrial-aquatic continuum in a boreal forested catchment. Freshwat Sci 34:440–455. doi:10.1086/680682

    Article  Google Scholar 

  • Rask M, Arvola L, Forsius M, Vuorenmaa J (2014) Preface to the Special Issue “Integrated monitoring in the Valkea-Kotinen Catchment during 1990–2009: abiotic and biotic responses to changes in air pollution and climate”. Boreal Env Res 19(suppl. A):1–3

    Google Scholar 

  • Sadro S, Melack JJ (2012) The effect of an extreme rain event on the biogeochemistry and ecosystem metabolisms of an oligotrophic high-elevation lake. Art Antarc Alp Res 44:222–231

    Article  Google Scholar 

  • Salonen K (1981) Rapid and precise determination of total inorganic carbon and some gases in aqueous solutions. Water Res 15:403–406

    Article  CAS  Google Scholar 

  • Salonen K, Rosenberg M (2000) Advantages from diel vertical migration can explain the dominance of Gonyostomum semen (Raphidophyceae) in a small, steeply-stratified humic lake. J Plankton Res 22:1841–1853

    Article  Google Scholar 

  • Simon M, Azam F (1989) Protein content and protein synthesis rates of planktonic marine bacteria. Mar Ecol Prog Ser 51:201–213

    Article  CAS  Google Scholar 

  • Staehr PA, Sand-Jensen K (2007) Temporal dynamics and regulation of lake metabolism. Limnol Oceanogr 52:108–120

    Article  CAS  Google Scholar 

  • Tittel J, Wiehle I, Wannicke N, Kampe H, Poerschmann J, Meier J, Kamjunke N (2009) Utilisation of terrestrial carbon by osmotrophic algae. Aquat Sci 71:46–54

    Article  CAS  Google Scholar 

  • Tranvik LJ (1998) Degradation of dissolved organic matter in humic waters by bacteria. In: Hessen DO, Tranvik LJ (eds) Aquatic humic substances, ecology and biochemistry. Spinger, Berlin, pp 259–284

    Chapter  Google Scholar 

  • Tsai J-W, Kratz TK, Hanson PC, Kimura N, Liu W-C, Lin F-P, Chou H-M, Wu J-T, Chiu C-Y (2011) Metabolic changes and the resistance and resilience of a subtropical heterotrophic lake to typhoon disturbance. Can J Fish Aquat Sci 68:768–780

    Article  Google Scholar 

  • Tulonen T (1993) Bacterial production in a mesohumic lake estimated from [14C] leucine incorporation rate. Microb Ecol 3:201–217

    Google Scholar 

  • Vähätalo AV, Salkinoja-Salonen M, Taalas P, Salonen K (2000) Spectrum of the quantum yield for photochemical mineralization of dissolved organic carbon in a humic lake. Limnol Oceanogr 45:664–676

    Article  Google Scholar 

  • Vesala T, Huotari J, Rannik Ü, Suni T, Smolander S, Sogachev A, Launiainen S, Ojala A (2006) Eddy covariance measurements of carbon exchange and latent and sensible heat fluxes over a boreal lake for a full open-water period. J Geophys Res 111:D11101. doi:10.1029/2005JD006365

    Article  Google Scholar 

  • Vesala T, Eugster W, Ojala A (2012) Eddy covariance measurements over lakes. In: Aubinet M, Papale D, Vesala T (eds) Eddy covariance: a practical guide to measurement and data analysis. Springer Atmospheric Sciences. doi:10.1007/1978-94-007-2351-1_15

  • Vidon P, Carleton W, Mitchell MJ (2014) Spatial and temporal variability in stream dissolved organic carbon quantity and quality in an Adirondack forested catchment. Appl Geochem 46:10–18

    Article  CAS  Google Scholar 

  • von Einem J, Granélli W (2010) Effects of fetch and dissolved organic carbon on epilimnion depth and light climate in small forest lakes in southern Sweden. Limnol Oceanogr 55:920–930

    Article  Google Scholar 

  • Vuorenmaa J, Forsius M, Mannio J (2006) Increasing trends of total organic carbon concentrations in small forest lakes in Finland from 1987 to 2003. Sci Total Environ 365:47–65

    Article  CAS  PubMed  Google Scholar 

  • Vuorenmaa J, Salonen K, Arvola L, Mannio J, Rask M, Horppila P (2014) Water quality of a small headwater lake reflects long-term variations in deposition, climate and in-lake processes. Boreal Environ Res 19:47–65

    CAS  Google Scholar 

  • Weyhenmeyer GA, Prairie YT, Tranvik L (2014) Browning of boreal freshwaters coupled to carbon–iron interactions along the aquatic continuum. PLoS ONE. doi:10.1371/journal.pone.0088104

    PubMed  PubMed Central  Google Scholar 

  • Yannarell A, Triplett EW (2004) Within- and between-lake variability in the composition of bacterioplankton communities; investigations using multiple spatial scales. Appl Environ Microb 70:214–223

    Article  CAS  Google Scholar 

  • Znachor P, Zapomĕlova E, Řeháková K, Nedoma J, Šimek K (2008) The effect of extreme rainfall on summer succession and vertical distribution of phytoplankton in a lacustrine part of a eutrophic reservoir. Aquat Sci 70:77–86

    Article  Google Scholar 

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Acknowledgments

This research was funded by the Helsinki University Research Centre (HERC; project REBECCA). Lammi Biological Station (University of Helsinki) provided the working facilities, and the Finnish Meteorological Institute the precipitation data. We would like to thank Ms Mirka Autio, Ms Riitta Ilola and Mr Jaakko Vainionpää (Lammi Biological Station) for their contribution in sampling and laboratory analyses.

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Peltomaa, E., Ojala, A. Consequences for pelagic energy mobilisation of a sudden browning episode without a clear increase in DOC concentration: a case of a boreal pristine lake. Aquat Sci 78, 627–639 (2016). https://doi.org/10.1007/s00027-015-0452-1

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