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Hydrobiologia

, Volume 778, Issue 1, pp 33–44 | Cite as

Major changes in CO2 efflux when shallow lakes shift from a turbid to a clear water state

  • Erik Jeppesen
  • Dennis Trolle
  • Thomas A. Davidson
  • Rikke Bjerring
  • Martin Søndergaard
  • Liselotte S. Johansson
  • Torben L. Lauridsen
  • Anders Nielsen
  • Søren E. Larsen
  • Mariana Meerhoff
SHALLOW LAKES

Abstract

Lakes can be sources or sinks of carbon, depending on local conditions. Recent studies have shown that the CO2 efflux increases when lakes recover from eutrophication, mainly as a result of a reduction in phytoplankton biomass, leading to less uptake of CO2 by producers. We hypothesised that lake restoration by removal of coarse fish (biomanipulation) or invasion of mussels would have a similar effect. We studied 14–22 year time series of five temperate Danish lakes and found profound effects on the calculated CO2 efflux of major shifts in ecosystem structure. In two lakes, where limited colonisation of submerged macrophytes occurred after biomanipulation or invasion of zebra mussels (Dreissena polymorpha), the efflux increased significantly with decreasing phytoplankton chlorophyll a. In three lakes with major interannual variation in macrophyte abundance, the efflux declined with increasing macrophyte abundance in two of the lakes, while no relation to macrophytes or chlorophyll a was found in the third lake, likely due to high groundwater input to this lake. We conclude that clearing water through invasive mussels or lake restoration by biomanipulation may increase the CO2 efflux from lakes. However, if submerged macrophytes establish and form dense beds, the CO2 efflux may decline again.

Keywords

Air–water CO2 flux Recovery Eutrophication Macrophytes Zebra mussel Lake metabolism 

Notes

Acknowledgments

We are grateful to CRES (Centre for Regional Change in the Earth System), the MARS project (Managing Aquatic ecosystems and water Resources under multiple Stress) funded under the 7th EU Framework Programme, Theme 6 (Environment including Climate Change), Contract No.: 603378 (http://www.mars-project.eu), CLEAR (a Villum Kann Rasmussen Centre of Excellence project on lake restoration) and CIRCE (Centre of Ecoinformatics Research in Complexity in Ecology funded by the AU IDEAS programme) for providing financial support. MM is supported by PEDECIBA, SNI-ANII and the L´Oréal-UNESCO for Women in Science National Award.

Supplementary material

10750_2015_2469_MOESM1_ESM.docx (39 kb)
Supplementary material 1 (DOCX 40kb)

References

  1. Anderson, N. J., H. Bennion & A. F. Lotter, 2014. Lake eutrophication and its implications for organic carbon sequestration in Europe. Global Changes in Biology 20: 2741–2751.CrossRefGoogle Scholar
  2. Bade, D. L. & J. J. Cole, 2006. Impact of chemically enhanced diffusion on dissolved inorganic carbon stable isotopes in a fertilized lake. Journal of Geophysical Research 111. doi: 10.1029/2004JC002684.
  3. Barros, N., J. J. Cole, L. J. Tranvik, Y. T. Prairie, D. Bastviken, V. L. M. Huszar, P. del Giorgio & F. Roland, 2011. Carbon emission from hydroelectric reservoirs linked to reservoir age and latitude. Nature Geoscience 4: 593–596.CrossRefGoogle Scholar
  4. Bastviken, D., J. J. Cole, M. L. Pace & L. Tranvik, 2008. Fates of methane from different lake habitats: connecting whole-lake budgets and CH4 emissions. Journal of Geophysical Research 113: G02024.CrossRefGoogle Scholar
  5. Bjerring, R., L.S. Johansson, M. Søndergaard, E. Jeppesen, T.L. Lauridsen, A. Kjeldgaard, L. Sortkjær, J. Windolf & J. Bøgestrand, 2013. Søer 2013. NOVANA. Aarhus Universitet, DCE – Nationalt Center for Miljø og Energi, 84 s. - Videnskabelig rapport fra DCE - Nationalt Center for Miljø og Energi nr. 76. (in Danish)Google Scholar
  6. Boll, T., L. S. Johansson, T. L. Lauridsen, F. Landkildehus, M. Søndergaard, F. Ø. Andersen & E. Jeppesen, 2012. Changes in benthic macroinvertebrate community and lake isotope (C, N) signals following a shift from clear to turbid water in a shallow lake. Hydrobiologia 686: 135–145.CrossRefGoogle Scholar
  7. Brothers, S. M., S. Hilt, S. Meyer & J. Köhler, 2013. Plant community structure determines primary productivity in shallow, eutrophic lakes. Freshwater Biology 58: 2264–2276.Google Scholar
  8. Carpenter, S. R., 1981. Submersed vegetation: an internal factor in lake ecosystem succession. The American Naturalist 118: 372–383.CrossRefGoogle Scholar
  9. Carpenter, S. R., N. F. Caraco, D. L. Correll, R. W. Howarth, A. N. Sharpley & V. H. Smith, 1998. Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecological Applications 8: 559–568.CrossRefGoogle Scholar
  10. Cole, J. J., 2013. Freshwater ecosystems and the carbon cycle. In Kinne, O. (ed.), Excellence in Ecology. Book 18. International Ecology Institute, Oldendorf/Luhe.Google Scholar
  11. Cole, J. J., N. F. Caraco, G. W. Kling & T. K. Kratz, 1994. Carbon dioxide supersaturation in the surface waters of lakes. Science 265: 1568–1570.CrossRefPubMedGoogle Scholar
  12. Cole, J. J., M. L. Pace, S. R. Carpenter & J. F. Kitchell, 2000. Persistence of net heterotrophy in lakes during nutrient addition and food web manipulations. Limnology and Oceanography 45: 1718–1730.CrossRefGoogle Scholar
  13. Cole, J. J., Y. T. Prairie, N. F. Caraco, W. H. McDowell, L. J. Tranvik, R. G. Striegl, C. M. Duarte, P. Kortelainen, J. A. Downing, J. J. Middelburg & J. Melack, 2007. Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems 10: 171–184.CrossRefGoogle Scholar
  14. Davidson, T. A., J. Audet, J.-C. Svenning, T. L. Lauridsen, M. Søndergaard, F. Landkildehus, S. E. Larsen & E. Jeppesen, 2015. Eutrophication effects on greenhouse gas fluxes from shallow lake mesocosms override those of climate warming. Global Change Biology. doi: 10.1111/gcb.13062.PubMedGoogle Scholar
  15. Dean, W. E. & E. Gorham, 1998. Magnitude and significance of carbon burial in lakes, reservoirs and peatlands. Geology 26: 535–538.CrossRefGoogle Scholar
  16. Declerck, S., J. Vandekerkhove, L. S. Johansson, K. Muylaert, J. M. Conde-Porcuna, K. van der Gucht, T. Lauridsen, K. Schwenk, G. Zwart, W. Rommens & J. Lopez-Ramos, 2005. Multi-group biodiversity in shallow lakes along gradients of phosphorus and water plant cover. Ecology 86: 1905–1915.CrossRefGoogle Scholar
  17. de Kluijver, A., J. Ning, Z. Liu, E. Jeppesen & J. J. Middelburg, 2015. Macrophyte and periphyton carbon subsidies to bacterioplankton and zooplankton in a shallow, eutrophic lake in tropical China. Limnology and Oceanography 60: 375–385.CrossRefGoogle Scholar
  18. Downing, J. A., Y. T. Prairie, J. J. Cole, M. Duarte, L. J. Tranvik, R. G. Striegl, W. H. McDowell, P. Kortelainen, N. F. Caraco, J. M. Melack & J. J. Middelburg, 2006. The global abundance and size distribution of lakes, ponds, and impoundments. Limnology and Oceanography 51: 2388–2397.CrossRefGoogle Scholar
  19. Dudgeon, D., A. H. Arthington, M. O. Gessner, Z.-I. Kawabata, D. J. Knowler, C. Lévêque, R. J. Naiman, A.-H. Prieur-Richard, D. Soto, M. L. J. Stiassny & C. A. Sullivan, 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews 81: 163–182.CrossRefPubMedGoogle Scholar
  20. Gao, J., Z. Liu & E. Jeppesen, 2014. Fish trophic structures but not biomass changed after lake restoration by biomanipulation in a tropical eutrophic lake. Hydrobiologia 724: 127–140.CrossRefGoogle Scholar
  21. Genkai-Kato, M., Y. Vadeboncoeur, L. Liboriussen & E. Jeppesen, 2012. Benthic-pelagic coupling, regime shifts and whole-lake primary production in shallow lakes. Ecology 93: 619–631.CrossRefPubMedGoogle Scholar
  22. Higgins, S. N. & M. J. Vander Zanden, 2010. What a difference a species makes: a meta-analysis of dreissenid mussel impacts on freshwater ecosystems. Ecological Monographs 80: 179–196.CrossRefGoogle Scholar
  23. Huttunen, J. T., S. Juutinen, J. Alm, T. Larmola, T. Hammar, J. Silvola & P. J. Martikainen, 2003. Fluxes of methane, carbon dioxide and nitrous oxide in boreal lakes and potential anthropogenic effects on the aquatic greenhouse gas emissions. Chemosphere 52: 609–621.CrossRefPubMedGoogle Scholar
  24. Idrisi, N., E. L. Mills, L. G. Rudstam & D. J. Stewart, 2001. Impact of zebra mussels (Dreissena polymorpha) on the pelagic lower trophic levels of Oneida Lake, New York. Candian Journal of Fisheries and Aquatic Sciences 58: 1430–1441.CrossRefGoogle Scholar
  25. Jeppesen, E., J. P. Jensen, M. Søndergaard, T. Lauridsen, F. P. Møller & K. Sandby, 1998. Changes in nitrogen retention in shallow eutrophic lakes following a decline in density of cyprinids. Archiv für Hydrobiologie 142: 129–151.CrossRefGoogle Scholar
  26. Jeppesen, E., J. P. Jensen, M. Søndergaard, T. Lauridsen & F. Landkildehus, 2000. Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient. Freshwater Biology 45: 201–213.CrossRefGoogle Scholar
  27. Jeppesen, E., M. Søndergaard, T. L. Lauridsen, T. A. Davidson, Z. Liu & N. Mazzeo, 2012. Biomanipulation as a restoration tool to combat eutrophication: recent advances and future challenges. Advances in Ecological Research 47: 411–487.CrossRefGoogle Scholar
  28. Jones, J. I., 2005. The metabolic cost of bicarbonate use in the submerged plant Elodea nuttallii. Aquatic Botany 83: 71–81.CrossRefGoogle Scholar
  29. Jones, J. I., K. Hardwick & J. W. Eaton, 1996. Diurnal carbon restrictions on the photosynthesis of dense stands of Elodea nuttallii (Planch.) St. John. Hydrobiologia 340: 11–16.CrossRefGoogle Scholar
  30. Jones, J. I., J. W. Eaton & K. Hardwick, 2000. The effect of changing environmental variables in the surrounding water on the physiology of Elodea nuttallii. Aquatic Botany 66: 115–129.CrossRefGoogle Scholar
  31. Karatayev, A. Y., D. K. Padilla, D. Minchin, D. Boltovskoy & L. E. Burlakova, 2007. Changes in global economies and trade: the potential spread of exotic freshwater bivalves. Biological Invasions 9: 161–180.CrossRefGoogle Scholar
  32. Kidmose, J., B. Nilsson, P. Engesgaard, M. Frandsen, S. Karan, F. Landkildehus, M. Søndergaard & E. Jeppesen, 2013. Focused groundwater discharge of phosphorus to a eutrophic seepage lake (Lake Væng, Denmark): implications for lake ecological state and restoration. Hydrogeology Journal 2: 1787–1802.CrossRefGoogle Scholar
  33. Kling, G. W., G. W. Kipphut & M. C. Miller, 1992. The flux of CO2 and CH4 from lakes and rivers in arctic Alaska. Hydrobiologia 240: 23–36.CrossRefGoogle Scholar
  34. Kosten, S., F. Roland, D. M. L. Da Motta Marques, E. H. Van Nes, N. Mazzeo, L. D. S. L. Sternberg, M. Scheffer & J. J. Cole, 2010. Climate-dependent CO2 emissions from lakes. Global Biogeochemical Cycles 24: GB2007.CrossRefGoogle Scholar
  35. Kronvang, B., G. Ærtebjerg, R. Grant, P. Kristensen, M. Hovmand & J. Kirkegaard, 1993. Nation-wide Danish monitoring programme – state of the aquatic environment. Ambio 22: 176–187.Google Scholar
  36. Lauridsen, T., E. Jeppesen & F. Ø. Andersen, 1993. Colonization of sub­merged macrophytes in shallow fish manipulated lake Væng: Impact of sediment compo­si­tion and birds grazing. Aquatic Botany 46: 1–15.Google Scholar
  37. Lauridsen, T. L., E. Jeppesen & M. Søndergaard, 1994. Colonization and succession of submerged macrophytes in shallow Lake Væng during the first five years following fish manipulation. Hydrobiologia 275(276): 233–242.CrossRefGoogle Scholar
  38. Lauridsen, T. L., J. P. Jensen, E. Jeppesen & M. Søndergaard, 2003. Response of submerged macrophytes in Danish lakes to nutrient loading reductions and biomanipulation. Hydrobiologia 506–509: 641–649.Google Scholar
  39. Liboriussen, L. & E. Jeppesen, 2003. Temporal dynamics in epipelic, pelagic and epiphytic algal production in a clear and a turbid shallow lake. Freshwater Biology 48: 418–431.CrossRefGoogle Scholar
  40. Liboriussen, L., M. Søndergaard & E. Jeppesen (red.), 2007. Sørestaurering i Danmark. Faglig rapport fra DMU 636: del I 86 s + del II 312 s. (in Danish)Google Scholar
  41. Liboriussen, L., T. L. Lauridsen, M. Søndergaard, F. Landkildehus, M. Søndergaard & E. Jeppesen, 2011. Climate warming effect on the seasonal dynamics in sediment respiration in shallow lakes: an outdoor mesocosms experiment. Freshwater Biology 56: 437–447.CrossRefGoogle Scholar
  42. Marklund, O., H. Sandsten, L.-A. Hansson & I. Blindow, 2002. Effects of waterfowl and fish on submerged vegetation and macroinvertebrates. Freshwater Biology 47: 2049–2059.CrossRefGoogle Scholar
  43. Mayer, C. M., R. A. Keats, L. G. Rudstam & E. L. Mill, 2002. Scale-dependent effects of zebra mussels on benthic invertebrates in a large eutrophic lake. Journal of the North American Benthological Society 21: 616–633.CrossRefGoogle Scholar
  44. Moss, B., 1990. Engineering and biological approaches to the restoration from eutrophication of shallow lakes in which aquatic plant communities are important components. Hydrobiologia 200(201): 367–377.CrossRefGoogle Scholar
  45. Moss, B., J. Madgwick & G. L. Phillips, 1996. A Guide to the Restoration of Nutrient-Enriched Shallow Lakes. Broads Authority & Environment Agency, Norwich.Google Scholar
  46. Moss, B., S. Kosten, M. Meerhoff, R. W. Battarbee, E. Jeppesen, N. Mazzeo, K. Havens, G. Lacerot, Z. Liu, L. De Meester, H. Paerl & M. Scheffer, 2011. Allied attack: climate change and nutrient pollution. Inland Waters 1: 101–105.CrossRefGoogle Scholar
  47. Muylaert, K., C. Pérez-Martínez, P. Sánchez-Castillo, T. L. Lauridsen, M. Vanderstukken, S. A. J. Declerck, K. Van der Gucht, J. M. Conde-Porcuna, E. Jeppesen, L. De Meester & W. Vyverman, 2010. Influence of nutrients, submerged macrophytes and zooplankton grazing on phytoplankton biomass and diversity along a latitudinal gradient in Europe. Hydrobiologia 653: 79–90.CrossRefGoogle Scholar
  48. Nielsen, A., D. Trolle, R. Bjerring, M. Søndergaard, J. E. Olesen & E. Jeppesen, 2014. Effects of climate and nutrient load on the water quality of shallow lakes assessed through ensemble runs by PCLake. Ecological Applications 24: 1926–1944.CrossRefGoogle Scholar
  49. Peterson, B. J. & B. Fry, 1987. Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18: 293–320.CrossRefGoogle Scholar
  50. Prejs, A., 1984. Herbivory by temperate freshwater fishes and its consequences. Environmental Biology of Fishes 10: 281–296.CrossRefGoogle Scholar
  51. Provoost, P., S. van Heuven, K. Soetaert, R. Laane & J. J. Middelburg, 2010. Long-term record of pH in the Dutch coastal zone: a major role for eutrophication-induced changes. Biogeosciences Discussions 7: 4127–4152.CrossRefGoogle Scholar
  52. Raymond, P. A., J. Hartmann, R. Lauerwald, S. Sobek, C. McDonald, M. Hoover, D. Butman, R. Striegl, E. Mayorga, C. Humborg, P. Kortelainen, H. Durr, M. Meybeck, P. Ciais & P. Guth, 2013. Global carbon dioxide emissions from inland waters. Nature 503: 355–359.CrossRefPubMedGoogle Scholar
  53. Rodríguez-Gallego, L., N. Mazzeo, J. Gorga, M. Meerhoff, J. Clemente, C. Kruk, F. Scasso, G. Lacerot, J. García & F. Quintans, 2004. Effects of an artificial wetland with free-floating plants on the restoration of a hypertrophic subtropical lake. Lake and Reservoir Management 9: 203–215.CrossRefGoogle Scholar
  54. Sandby, K. S. & J. Hansen, 2007. Lake Arreskov. In: Liboriussen, L., M. Søndergaard, E. Jeppesen (eds) Sørestaurering i Danmark. Report from NERI no. 636 (in Danish).Google Scholar
  55. Scheffer, M., S. H. Hosper, M. L. Meijer, B. Moss & E. Jeppesen, 1993. Alternative equilibria in shallow lakes. Trends in Ecology and Evolution 8: 275–279.CrossRefPubMedGoogle Scholar
  56. Stallard, R. F., 1998. Terrestrial sedimentation and the carbon cycle: coupling weathering and erosion to carbon burial. Global Biogeochemical Cycles 12: 231–257.CrossRefGoogle Scholar
  57. Stewart, T. W., J. G. Miner & R. L. Lowe, 1998. Quantifying mechanisms for zebra mussel effects on benthic macroinvertebrates: organic matter production and shell-generated habitat. Journal of the North American Benthological Society 17: 81–94.CrossRefGoogle Scholar
  58. Stumm, W. & J. J. Morgan, 1996. Aquatic Chemistry. John Wiley, New York.Google Scholar
  59. Strand, J. A. & S. E. B. Weisner, 2001. Dynamics of submerged macrophyte populations in response to biomanipulation. Freshwater Biology 46: 1397–1408.CrossRefGoogle Scholar
  60. Strayer, D. L., N. F. Caraco, J. J. Cole, S. Findlay & M. L. Pace, 1999. Transformation of freshwater ecosystems by bivalves – a case study of zebra mussels in the Hudson River. Bioscience 49: 19–27.CrossRefGoogle Scholar
  61. Søndergaard, M., E. Jeppesen, E. Mortensen, E. Dall, P. Kristensen & O. Sortkjær, 1990. Phytoplankton biomass reduction after planktivorous fish reduction in a shallow, eutrophic lake: a combined effect of reduced internal P-loading and increased zooplankton grazing. Hydrobiologia 200(201): 229–240.CrossRefGoogle Scholar
  62. Søndergaard, M., L. Olufsen, T. Lauridsen, E. Jeppesen & T. Vindbæk Madsen, 1996. The impact of grazing waterfowl on submerged macrophytes: in situ experiments in a shallow eutrophic lake. Aquatic Botany 53: 73–84.CrossRefGoogle Scholar
  63. Søndergaard, M., T. L. Lauridsen, E. Jeppesen & L. Bruun, 1998. Macrophyte-Waterfowl Interactions: Tracking a Variable Resource and the Impact of Herbivory on Plant Growth. In Jeppesen, E., M. Søndergaard, M. Søndergaard & K. Christoffersen (eds.), The Structuring Role of Submerged Macrophytes in Lakes, Vol. 131., Ecological Studies Series Springer, New York: 298–306.CrossRefGoogle Scholar
  64. Talling, J. F., 1976. The depletion of carbon dioxide from lake water by phytoplankton. Journal of Ecology 64: 79–121.CrossRefGoogle Scholar
  65. Tranvik, L. J., J. A. Downing, J. B. Cotner, S. A. Loiselle, R. G. Striegl, T. J. Ballatore, P. Dillon, L. B. Knoll, T. Kutser, S. Larsen, I. Laurion, D. M. Leech, S. L. McAllister, D. M. McKnight, J. Melack, E. Overholt, J. A. Porter, Y. T. Prairie, W. H. Renwick, F. Roland, B. S. Sherman, D. W. Schindler, S. Sobek, A. Tremblay, M. J. Vanni, A. M. Verschoor, E. von Wachenfeldt & G. Weyhenmeyer, 2009. Lakes and reservoirs as regulators of carbon cycling and climate. Limnology and Oceanography 54: 2298–2314.CrossRefGoogle Scholar
  66. Trolle, D., P. A. Staehr, T. A. Davidson, R. Bjerring, T. L. Lauridsen, M. Søndergaard & E. Jeppesen, 2012. Seasonal dynamics of CO2 flux across the surface of shallow temperate lakes of contrasting trophic status, and the response to nutrient load reduction. Ecosystems 15: 336–347.CrossRefGoogle Scholar
  67. Vadeboncoeur, Y., E. Jeppesen, M. J. Vander Zanden, H. H. Schierup, K. Christoffersen & D. Lodge, 2003. From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes. Limnology and Oceanography 48: 1408–1418.CrossRefGoogle Scholar
  68. Vadeboncoeur, Y., G. Peterson, M. J. Vander Zanden & J. Kalff, 2008. Benthic algal productivity across lake size gradients: interactions among morphometry, nutrients, and light. Ecology 89: 2542–2552.CrossRefPubMedGoogle Scholar
  69. Verpoorter, C., T. Kutser, D. A. Seekell & L. J. Tranvik, 2014. A global inventory of lakes based on high-resolution satellite imagery. Geophysical Research Letters 41: 6396–6402.CrossRefGoogle Scholar
  70. Vörösmarty, C. J., P. B. McIntyre, M. O. Gessner, D. Dudgeon, A. Prusevich, P. Green, S. Glidden, S. E. Bunn, C. A. Sullivan, C. Reidy Liermann & P. M. Davies, 2010. Global threats to human water security and river biodiversity. Nature 467: 555–561.CrossRefPubMedGoogle Scholar
  71. Wetzel, R. G., 2001. Limnology: Lake and River Ecosystems. Academic Press, San Diego.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Erik Jeppesen
    • 1
    • 3
  • Dennis Trolle
    • 1
    • 3
  • Thomas A. Davidson
    • 1
  • Rikke Bjerring
    • 1
  • Martin Søndergaard
    • 1
  • Liselotte S. Johansson
    • 1
  • Torben L. Lauridsen
    • 1
    • 3
  • Anders Nielsen
    • 1
  • Søren E. Larsen
    • 2
    • 3
    • 4
  • Mariana Meerhoff
    • 1
    • 4
  1. 1.Lake Ecology Section, Department of Bioscience and the Arctic Research CentreAarhus UniversityAarhusDenmark
  2. 2.Catchment Science and Environmental Management Section, Department of BioscienceAarhus UniversityAarhusDenmark
  3. 3.Sino-Danish Centre for Education and Research (SDC)BeijingChina
  4. 4.Departamento de Ecología Teórica y Aplicada, Centro Universitario de la Región Este-Facultad de CienciasUniversidad de la RepúblicaMaldonadoUruguay

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