Ecosystem responses to increased organic carbon concentration: comparing results based on long-term monitoring and whole-lake experimentation

ABSTRACT Recent increases in terrestrial dissolved organic carbon (DOC) concentrations in northern inland waters have many ecological consequences. We examined available data on carbon cycles and food webs of 2 boreal headwater lakes in southern Finland. Basic limnology and catchment characteristics of a pristine lake, Valkea-Kotinen (VK), were monitored over the past 25 years while the lake has undergone browning and DOC increased from ∼11 to 13 mg L−1. Pronounced changes in the early 2000s represent a regime shift in DOC concentration and color. Lake Alinen Mustajärvi (AM) was manipulated for 2 years by additions of labile DOC (cane sugar), raising the DOC concentration from ∼10 to 12 mg L−1, but not changing light conditions. The 2 different approaches both revealed increased concentrations and efflux of carbon dioxide (CO2) from the lakes and thus net heterotrophy and changes in the pelagic community structure following an increase in DOC concentration. Long-term monitoring of VK revealed a decline in phytoplankton primary production (PP) along with browning, which was reflected in retarded growth of young (1–2-year-old) perch. In the experimentally manipulated lake (AM), PP was not affected, and the growth of young perch was more variable. The results suggested the importance of a pathway from labile DOC via benthic invertebrates to perch. Although provided with this extra resource, the food chain based on DOC proved inefficient. Long-term monitoring and whole-lake experimentation are complementary approaches for revealing how freshwater ecosystems respond to climate and/or atmospheric deposition-induced changes, such as browning.

[1]  J. Wikner,et al.  BACTERIOPLANKTON GROWTH , 2020 .

[2]  R. Markwald,et al.  Chapter 1 Introduction to COVID-19 , 2022, COVID-19 in the Environment.

[3]  S. Langenheder,et al.  High abundances of the nuisance raphidophyte Gonyostomum semen in brown water lakes are associated with high concentrations of iron , 2018, Scientific Reports.

[4]  N. Grimm,et al.  Global change‐driven effects on dissolved organic matter composition: Implications for food webs of northern lakes , 2018, Global change biology.

[5]  S. Saarnio,et al.  Changes in dissolved organic matter and microbial activity in runoff waters of boreal mires after restoration , 2018, Aquatic Sciences.

[6]  I. Creed,et al.  Recent Synchronous Declines in DIN:TP in Swedish Lakes , 2018 .

[7]  J. Zwart,et al.  A Framework for Understanding Variation in Pelagic Gross Primary Production of Lake Ecosystems , 2018, Ecosystems.

[8]  E. Tipping,et al.  The contribution of algae to freshwater dissolved organic matter: implications for UV spectroscopic analysis , 2018 .

[9]  M. Bek,et al.  Responses of Zooplankton to Long-Term Environmental Changes in the Egyptian Coastal Lakes , 2018 .

[10]  H. Nykänen,et al.  Whole-Lake Sugar Addition Demonstrates Trophic Transfer of Dissolved Organic Carbon to Top Consumers , 2018, Ecosystems.

[11]  H. Grossart,et al.  Benthic carbon is inefficiently transferred in the food webs of two eutrophic shallow lakes , 2017 .

[12]  I. Mammarella,et al.  Methane and carbon dioxide fluxes over a lake: comparison between eddy covariance, floating chambers and boundary layer method , 2017 .

[13]  E. Peltomaa,et al.  Lake eutrophication and brownification downgrade availability and transfer of essential fatty acids for human consumption. , 2016, Environment international.

[14]  S. Larsen,et al.  From greening to browning: Catchment vegetation development and reduced S-deposition promote organic carbon load on decadal time scales in Nordic lakes , 2016, Scientific Reports.

[15]  J. Zwart,et al.  Experimental whole‐lake increase of dissolved organic carbon concentration produces unexpected increase in crustacean zooplankton density , 2016, Global change biology.

[16]  Roger I. Jones,et al.  Accounting for littoral primary production by periphyton shifts a highly humic boreal lake towards net autotrophy , 2016 .

[17]  S. Carpenter,et al.  Response of plankton to nutrients, planktivory and terrestrial organic matter: a model analysis of whole-lake experiments. , 2016, Ecology letters.

[18]  A. Ojala,et al.  Consequences for pelagic energy mobilisation of a sudden browning episode without a clear increase in DOC concentration: a case of a boreal pristine lake , 2016, Aquatic Sciences.

[19]  Lesley B. Knoll,et al.  Ecological consequences of long-term browning in lakes , 2015, Scientific Reports.

[20]  C. Hein,et al.  Terrestrial organic matter input suppresses biomass production in lake ecosystems. , 2015, Ecology.

[21]  J. Lapierre,et al.  The influence of dissolved organic carbon on primary production in northern lakes , 2015 .

[22]  J. Lennon,et al.  A test of the subsidy–stability hypothesis: the effects of terrestrial carbon in aquatic ecosystems , 2015 .

[23]  J. Pumpanen,et al.  Concentrations and quality of DOC along the terrestrial–aquatic continuum in a boreal forested catchment , 2015, Freshwater Science.

[24]  J. Read,et al.  Ecosystem Consequences of Changing Inputs of Terrestrial Dissolved Organic Matter to Lakes: Current Knowledge and Future Challenges , 2015, Ecosystems.

[25]  P. Hari,et al.  Precipitation and net ecosystem exchange are the most important drivers of DOC flux in upland boreal catchments , 2014 .

[26]  M. Vanni,et al.  Whole-lake experiments reveal the fate of terrestrial particulate organic carbon in benthic food webs of shallow lakes. , 2014, Ecology.

[27]  Tom Andersen,et al.  The Absorption of Light in Lakes: Negative Impact of Dissolved Organic Carbon on Primary Productivity , 2014, Ecosystems.

[28]  A. Lepistö,et al.  Almost 50 years of monitoring shows that climate, not forestry, controls long‐term organic carbon fluxes in a large boreal watershed , 2014, Global change biology.

[29]  L. Arvola,et al.  Plankton metabolism and sedimentation in a small boreal lake - a long-term perspective , 2014 .

[30]  L. Arvola,et al.  Water quality of a small headwater lake reflects long-term variations in deposition, climate and in-lake processes , 2014 .

[31]  L. Arvola,et al.  Responses of zooplankton to long-term environmental changes in a small boreal lake , 2014 .

[32]  Chris J. Hulatt,et al.  Bioavailability and radiocarbon age of fluvial dissolved organic matter (DOM) from a northern peatland-dominated catchment: effect of land-use change , 2014, Aquatic Sciences.

[33]  Lars J. Tranvik,et al.  Browning of Boreal Freshwaters Coupled to Carbon-Iron Interactions along the Aquatic Continuum , 2014, PloS one.

[34]  T. Ruoho-Airola,et al.  Temporal trends in the bulk deposition and atmospheric concentration of acidifying compounds and trace elements in the Finnish Integrated Monitoring catchment Valkea-Kotinen during 1988–2011 , 2014 .

[35]  A. Eiler,et al.  Enhanced greenhouse gas emissions and changes in plankton communities following an experimental increase in organic carbon loading to a humic lake , 2014, Biogeochemistry.

[36]  Anne Ojala,et al.  Lake‐size dependent physical forcing drives carbon dioxide and methane effluxes from lakes in a boreal landscape , 2013 .

[37]  A. Ojala,et al.  Changes in phytoplankton in a boreal lake during a 14-year period , 2013 .

[38]  L. Tranvik,et al.  In-Lake Processes Offset Increased Terrestrial Inputs of Dissolved Organic Carbon and Color to Lakes , 2013, PloS one.

[39]  K. Dinsmore,et al.  Contrasting CO2 concentration discharge dynamics in headwater streams: A multi‐catchment comparison , 2013 .

[40]  D. Bastviken,et al.  Determination of the piston velocity for water‐air interfaces using flux chambers, acoustic Doppler velocimetry, and IR imaging of the water surface , 2013 .

[41]  E. Peltomaa Phytoplanktonic life in boreal humic lakes : special emphasis on autotrophic picoplankton and microbial food webs , 2013 .

[42]  M. Brett,et al.  The influence of bacteria-dominated diets on Daphnia magna somatic growth, reproduction, and lipid composition. , 2012, FEMS microbiology ecology.

[43]  Craig R. Allen,et al.  Insight on Invasions and Resilience Derived from Spatiotemporal Discontinuities of Biomass at Local and Regional Scales , 2012 .

[44]  J. Pumpanen,et al.  Rain Induced Changes in Carbon Dioxide Concentrations in the Soil–Lake–Brook Continuum of a Boreal Forested Catchment , 2012 .

[45]  David P. Hamilton,et al.  Lake‐size dependency of wind shear and convection as controls on gas exchange , 2012 .

[46]  J. Karlsson,et al.  Transfer of bacterial production based on labile carbon to higher trophic levels in an oligotrophic pelagic system , 2012 .

[47]  C. Gagnon,et al.  Increases of dissolved organic carbon in temperate and boreal lakes in Quebec, Canada , 2012, Environmental Science and Pollution Research.

[48]  FaithfullCarolyn,et al.  Transfer of bacterial production based on labile carbon to higher trophic levels in an oligotrophic pelagic system , 2011 .

[49]  E. Kritzberg,et al.  Increasing iron concentrations in surface waters – a factor behind brownification? , 2011 .

[50]  P. Hari,et al.  Long‐term direct CO2 flux measurements over a boreal lake: Five years of eddy covariance data , 2011 .

[51]  D. Martin‐Creuzburg,et al.  Food quality of heterotrophic bacteria for Daphnia magna: evidence for a limitation by sterols. , 2011, FEMS microbiology ecology.

[52]  V. Kitunen,et al.  Properties of dissolved organic matter derived from silver birch and Norway spruce stands: Degradability combined with chemical characteristics , 2011 .

[53]  H. Nykänen,et al.  Impacts of added dissolved organic carbon on boreal freshwater pelagic metabolism and food webs in mesocosm experiments. , 2010 .

[54]  L. Nurminen,et al.  Diet shifts and food selection of perch Perca fluviatilis and roach Rutilus rutilus in humic lakes of varying water colour. , 2010, Journal of fish biology.

[55]  L. Arvola,et al.  Long-term patterns in pH and colour in small acidic boreal lakes of varying hydrological and landscape settings , 2010 .

[56]  P. Chapman,et al.  The importance of the relationship between scale and process in understanding long-term DOC dynamics. , 2010, The Science of the total environment.

[57]  H. Laudon,et al.  Efficient aquatic bacterial metabolism of dissolved low-molecular-weight compounds from terrestrial sources , 2010, The ISME Journal.

[58]  J. Vuorenmaa,et al.  Re-establishment of perch in three lakes recovering from acidification : rapid growth associated with abundant food resources , 2010 .

[59]  P. Ask,et al.  Terrestrial organic matter and light penetration: Effects on bacterial and primary production in lakes , 2009 .

[60]  Per Ask,et al.  Light limitation of nutrient-poor lake ecosystems , 2009, Nature.

[61]  Lauri Arvola,et al.  Impacts of Climate on the Flux of Dissolved Organic Carbon from Catchments , 2009 .

[62]  L. Tranvik,et al.  Sedimentation in Boreal Lakes—The Role of Flocculation of Allochthonous Dissolved Organic Matter in the Water Column , 2008, Ecosystems.

[63]  J. Stoddard,et al.  Dissolved organic carbon trends resulting from changes in atmospheric deposition chemistry , 2007, Nature.

[64]  L. Tranvik,et al.  Terrestrial carbon and intraspecific size-variation shape lake ecosystems. , 2007, Trends in ecology & evolution.

[65]  L. Ström,et al.  Composition and variations in the occurrence of dissolved free simple organic compounds of an unproductive lake ecosystem in northern Sweden , 2007 .

[66]  P. Kortelainen,et al.  Controls on the export of C, N, P and Fe from undisturbed boreal catchments, Finland , 2006, Aquatic Sciences.

[67]  M. Forsius,et al.  Increasing trends of total organic carbon concentrations in small forest lakes in Finland from 1987 to 2003. , 2006, The Science of the total environment.

[68]  M. Jansson,et al.  Bacterioplankton Growth and Nutrient Use Efficiencies Under Variable Organic Carbon and Inorganic Phosphorus Ratios , 2006, Microbial Ecology.

[69]  Marti J. Anderson,et al.  Distance‐Based Tests for Homogeneity of Multivariate Dispersions , 2006, Biometrics.

[70]  M. Starr,et al.  Proton budgets for a monitoring network of European forested catchments: impacts of nitrogen and sulphur deposition , 2005 .

[71]  L. Tranvik Availability of dissolved organic carbon for planktonic bacteria in oligotrophic lakes of differing humic content , 1988, Microbial Ecology.

[72]  S. Rodionov A sequential algorithm for testing climate regime shifts , 2004 .

[73]  Y. Prairie,et al.  Bacterial metabolism and growth efficiency in lakes: The importance of phosphorus availability , 2004 .

[74]  Ulla Rosenström,et al.  The most typical phytoplankton taxa in four types of boreal lakes , 1998, Hydrobiologia.

[75]  L. Arvola,et al.  Effects of different molecular weight fractions of dissolved organic matter on the growth of bacteria, algae and protozoa from a highly humic lake , 1992, Hydrobiologia.

[76]  G. Cronberg,et al.  Mass development of the flagellate Gonyostomum semen (Raphidophyta) in Swedish forest lakes - an effect of acidification? , 1988, Hydrobiologia.

[77]  Roger I. Jones,et al.  The influence of humic substances on lacustrine planktonic food chains , 2004, Hydrobiologia.

[78]  U. Münster Concentrations and fluxes of organic carbon substrates in the aquatic environment , 2004, Antonie van Leeuwenhoek.

[79]  S. Carpenter,et al.  Lake metabolism: Relationships with dissolved organic carbon and phosphorus , 2003 .

[80]  L. Tranvik,et al.  The catchment and climate regulation of pCO2 in boreal lakes , 2003 .

[81]  M. Jansson,et al.  Primary production and phytoplankton composition in relation to DOC input and bacterioplankton production in humic Lake Ortrasket , 2002 .

[82]  M. Jansson,et al.  Effects of Additions of DOC on Pelagic Biota in a Clearwater System: Results from a Whole Lake Experiment in Northern Sweden , 2001, Microbial Ecology.

[83]  N. H. Borch,et al.  Dynamics of biodegradable DOC produced by freshwater plankton communities , 2000 .

[84]  K. Salonen,et al.  Advantages from diel vertical migration can explain the dominance of Gonyostomum semen (Raphidophyceae) in a small, steeply-stratified humic lake , 2000 .

[85]  Roger I. Jones,et al.  Mixotrophy in planktonic protists: an overview , 2000 .

[86]  Jonathan J. Cole,et al.  Atmospheric exchange of carbon dioxide in a low‐wind oligotrophic lake measured by the addition of SF6 , 1998 .

[87]  L. Tranvik DEGRADATION OF DISSOLVED ORGANIC MATTER IN HUMIC WATERS BY BACTERIA , 1998 .

[88]  C. Curtis,et al.  NORTHERN EUROPEAN LAKE SURVEY, 1995 , 1998 .

[89]  L. Arvola,et al.  Effects of phosphorus and allochthonous humic matter enrichment on metabolic processes and community structure of plankton in a boreal lake (Lake Pääjärvi) , 1996 .

[90]  R. Peters,et al.  Patterns in planktonic P:R ratios in lakes: Influence of lake trophy and dissolved organic carbon , 1994 .

[91]  J. Raitaniemi,et al.  The growth of perch, Perca fluviatilis L., in recently acidified lakes of Southern Finland ― a comparison with unaffected waters , 1988 .

[92]  L. Arvola,et al.  The biomass and production of pike perch and whitefish in two small lakes in southern Finland , 1985 .

[93]  R. Koschel,et al.  Primary Production , 2021, Tropical Marine Ecology.

[94]  L. Arvola,et al.  Hypolimnetic phosphorus retrieval by diel vertical migrations of lake phytoplankton , 1984 .