Estuaries and Coasts

, Volume 37, Issue 3, pp 680–694 | Cite as

Feedback Mechanisms Between Cyanobacterial Blooms, Transient Hypoxia, and Benthic Phosphorus Regeneration in Shallow Coastal Environments

  • Mindaugas Zilius
  • Marco Bartoli
  • Mariano Bresciani
  • Marija Katarzyte
  • Tomas Ruginis
  • Jolita Petkuviene
  • Irma Lubiene
  • Claudia Giardino
  • Paul A. Bukaveckas
  • Rutger de Wit
  • Arturas Razinkovas-Baziukas


We investigated the dissolved oxygen metabolism of the Curonian Lagoon (Baltic Sea) to assess the relative contributions of pelagic and benthic processes to the development of transient hypoxic conditions in shallow water habitats. Metabolism measurements along with the remote sensing-derived estimates of spatial variability in chlorophyll a were used to evaluate the risk of hypoxia at the whole lagoon level. Our data demonstrate that cyanobacterial blooms strongly inhibit light penetration, resulting in net heterotrophic conditions in which pelagic oxygen demand exceeds benthic oxygen demand by an order of magnitude. The combination of bloom conditions and reduced vertical mixing during calm periods resulted in oxygen depletion of bottom waters and greater sediment nutrient release. The peak of reactive P regeneration (nearly 30 μmol m−2 h−1) coincided with oxygen depletion in the water column, and resulted in a marked drop of the inorganic N:P ratio (from >40 to <5, as molar). Our results suggest a strong link between cyanobacterial blooms, pelagic respiration, hypoxia, and P regeneration, which acts as a feedback in sustaining algal blooms through internal nutrient cycling. Meteorological data and satellite-derived maps of chlorophyll a were used to show that nearly 70 % of the lagoon surface (approximately 1,000 km2) is prone to transient hypoxia development when blooms coincide with low wind speed conditions.


Cyanobacterial blooms Respiration Hypoxia Phosphorus release Net ecosystem metabolism 



Mindaugas Zilius was supported by a postdoctoral fellowship funded by the European Union Structural Funds project “Postdoctoral Fellowship Implementation in Lithuania.” Paul Bukaveckas was supported by a Fulbright Fellowship during his residence at Klaipeda University. MERIS data were made available through the ESA project AO-553 (MELINOS). This study was co-funded by CYAN-IS-WAS (Ministero dell’Istruzione dell’Università e della Ricerca, Science and technological cooperation between Italy and the Kingdom of Sweden) and CLAM-PHYM (Italian Space Agency, contract ASI I/015/11/0) projects. We gratefully thank the Lithuanian Hydrometeorological Service of the Ministry of Environment for providing meteorological data. We also gratefully thank three anonymous reviewers for valuable comments which improved the quality of the manuscript.


  1. Almroth, E., A. Tengberg, J.H. Andersson, S. Pakhomova, and P.O.J. Hall. 2009. Effects of resuspension on benthic fluxes of oxygen, nutrients, dissolved inorganic carbon, iron, and manganese in the Gulf of Finland, Baltic Sea. Continental Shelf Research 29: 807–818.CrossRefGoogle Scholar
  2. Bailey, S.W., and P.J. Werdell. 2006. A multisensor approach for the on-orbit validation of ocean color satellite data products. Remote Sensing of Environment 102: 12–23.CrossRefGoogle Scholar
  3. Bresciani, M., C. Giardino, D. Stroppiana, R. Pilkaitytė, M. Zilius, M. Bartoli, and A. Razinkovas. 2012. Retrospective analysis of spatial and temporal variability of chlorophyll-a in the Curonian Lagoon. Journal of Coastal Conservation 16: 511–519.CrossRefGoogle Scholar
  4. Caffrey, J.M. 2004. Factors controlling net ecosystem metabolism in US estuaries. Estuaries 27(1): 90–101.CrossRefGoogle Scholar
  5. Candiani, G., D. Floricioiu, C. Giardino, and H. Rott. 2005. Monitoring water quality of the perialpine Italian lake Garda through Multitemporal MERIS data. MERIS/(A)ATSR User Workshop. 26–30, ESA SP-597, CD-ROM.Google Scholar
  6. Carstensen, J., P. Henriksen, and A.-S. Heiskanen. 2007. Summer algal blooms in shallow estuaries: definition, mechanisms, and link to eutrophication. Limnology and Oceanography 52(1): 370–384.CrossRefGoogle Scholar
  7. Chen, C.-C., G.-C. Gong, and F.-K. Shiah. 2007. Hypoxia in the East China Sea: one of the largest coastal low-oxygen areas in the world. Marine Environmental Research 64(4): 399–408.CrossRefGoogle Scholar
  8. Cloern, J.E. 2001. Our evolving conceptual model of the coastal eutrophication problem. Marine Ecology Progress Series 210: 223–253.CrossRefGoogle Scholar
  9. Conley, D.J., and T.C. Malone. 1992. Annual cycle of dissolved silicate in Chesapeake Bay: implications for the production and fate of phytoplankton biomass. Marine Ecology Progress Series 81: 121–128.CrossRefGoogle Scholar
  10. Conley, D.J., H. Kaas, F. Møhlenberg, B. Rasmussen, and J. Windolf. 2000. Characteristics of Danish Estuaries. Estuaries 23(6): 820–837.CrossRefGoogle Scholar
  11. Conley, D.J., J. Carstensen, G. Ærtebjerg, P.B. Christensen, T. Dalsgaard, J.L.S. Hansen, and A.B.. Josefson. 2007. Long-term changes and impacts of hypoxia in Danish coastal waters. Ecological Applications 17(5): 165–184.Google Scholar
  12. Conley, D.J., S. Björck, E. Bonsdorff, J. Carstensen, G. Destouni, B.G. Gustafsson, S. Hietanen, M. Kortekaas, H. Kuosa, M.H.E. Meier, B. Müller-Karulis, K. Nordberg, A. Norko, G. Nürnberg, H. Pitkänen, N.N. Rabalais, R. Rosenberg, O.P. Savchuk, C. Slomp, M. Voss, F. Wulff, and L. Zillén. 2009. Hypoxia-related processes in the Baltic Sea. Environmental Science and Technology 43(10): 3412–3420.CrossRefGoogle Scholar
  13. Conley, D.J., J. Carstensen, J. Aigars, P. Axe, E. Bonsdorff, T. Eremina, B. Haahti, C. Humborg, P. Jonsson, J. Kotta, C. Lannegren, U. Larsson, A. Maximov, M. Medina, E. Lysiak-Pastuszak, N. Remeikaite-Nikiene, J. Walve, S. Wilhelms, and L. Zillén. 2011. Hypoxia is increasing in the coastal zone of the Baltic Sea. Environmental Science and Technology 45: 6777–6783.CrossRefGoogle Scholar
  14. D’Avanzo, C., and J.N. Kremer. 1994. Diel oxygen dynamics and anoxia events in an eutrophic estuary of Waquoit Bay, Massachusetts. Estuaries 17(18): 131–139.CrossRefGoogle Scholar
  15. Dalsgaard, T., L.P. Nielsen, V. Brotas, P. Viaroli, G. Underwood, D. Nedwell, K. Sundbäck, S. Rysgaard, A. Miles, M. Bartoli, L. Dong, D.C.O. Thornton, L.D.M. Otossen, G. Castaldelli, and N. Risgaard-Petersen. 2000. Protocol handbook for NICE—Nitrogen Cycling In Estuaries: A project under the EU research program: Marine Science and Technology (MAST III). Silkeborg: National Environmental Research Institute.Google Scholar
  16. Daunys, D. 2001. Patterns of the bottom macrofauna variability and its role in the shallow coastal Lagoon. Summary of Doctoral Dissertation. Klaipėda: Klaipėda University.Google Scholar
  17. Diaz, R.J. 2001. Overview of hypoxia around the world. Journal of Environmental Quality 30: 275–281.CrossRefGoogle Scholar
  18. Diaz, R.J., and R. Rosenberg. 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioral responses of benthic macrofauna. Oceanography and Marine Biology. Annual Review 33: 245–303.Google Scholar
  19. Ferrarin, C., A. Razinkovas, S. Gulbinskas, G. Umgiesser, and L. Bliūdžiutė. 2008. Hydraulic regime-based zonation scheme of the Curonian Lagoon. Hydrobiologia 611(1): 133–146.CrossRefGoogle Scholar
  20. Fomferra, N., and C. Brockmann. 2006. The BEAM Project. Hamburg, Germany: Carsten Brockmann Consult.Google Scholar
  21. Fulweiler, R.W., S.W. Nixon, and B.A. Buckley. 2010. Spatial and temporal variability of benthic oxygen demand and nutrient regeneration in an anthropogenically impacted New England Estuary. Estuaries and Coasts 33: 1377–1390.CrossRefGoogle Scholar
  22. Giardino, C., M. Bresciani, R. Pilkaityte, M. Bartoli, and A. Razinkovas. 2010. In situ measurements and satellite remote sensing of case 2 waters: first results from the Curonian Lagoon. Oceanologia 52(2): 197–210.CrossRefGoogle Scholar
  23. Giordano, J.C.P., M.J. Brush, and I.C. Anderson. 2012. Ecosystem metabolism in shallow coastal lagoons: patterns and partitioning of planktonic, benthic, and integrated community rates. Marine Ecology Progress Series 458: 21–38. doi: 10.3354/meps09719.CrossRefGoogle Scholar
  24. Gitelson, A.A., J.F. Schalles, and C.M. Hladik. 2007. Remote chlorophyll-a retrieval in turbid, productive estuaries: Chesapeake Bay case study. Remote Sensing of Environment 109: 464–472.CrossRefGoogle Scholar
  25. Grasshoff, K., M. Ehrhardt, and K. Kremling. 1983. Methods of Seawater Analysis, 2nd ed. Berlin: Verlag Chemie.Google Scholar
  26. Hagy, J.D., W.R. Boynton, C.W. Keefe, and K.V. Wood. 2004. Hypoxia in Chesapeake Bay, 1950–2001: long-term change in relation to nutrient loading and river flow. Estuaries 27: 634–658.CrossRefGoogle Scholar
  27. Holben, B.N., T.F. Eck, I. Slutsker, D. Tanre, J.P. Buis, A. Setzer, E. Vermote, J.A. Reagan, Y.J. Kaufman, T. Nakajima, F. Lavenu, I. Jankowiak, and A. Smirnov. 1998. AERONET—a federated instrument network and data archive for aerosol characterization. Remote Sensing of Environment 66: 1–16.CrossRefGoogle Scholar
  28. Hopkinson, C.S., and E.M. Smith. 2005. Estuarine respiration: an overview of benthic, pelagic, and whole system respiration. In Respiration in aquatic ecosystems, ed. P.A. del Giorgio and P.J.B. le Williams, 123–147. New York: Oxford Univ. Press.Google Scholar
  29. Huisman, J., J. Sharples, J.M. Stroom, P.M. Visser, W.E.A. Kardinaal, J.M.H. Verspagen, and B. Sommeijer. 2004. Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85: 2960–2970.CrossRefGoogle Scholar
  30. Jakimavičius, D., and J. Kriaučiūnienė. 2013. The climate change impact on the water balance of the Curonian Lagoon. Water Resources 40(2): 120–132.CrossRefGoogle Scholar
  31. Jäntti, H., and S. Hietanen. 2012. The effects of hypoxia on sediment nitrogen cycling in the Baltic Sea. Ambio 41: 161–169. doi: 10.1007/s13280-011-0233-6.CrossRefGoogle Scholar
  32. Jensen, L.M., K. Sand-Jensen, S. Marcher, and M. Hansen. 1990. Plankton community respiration along a nutrient gradient in a shallow Danish estuary. Marine Ecology Progress Series 61: 75–85.CrossRefGoogle Scholar
  33. Jensen, H.S., P.B. Mortensen, F.Ø. Andersen, E. Rasmussen, and A. Jensen. 1995. Phosphorus cycling in coastal marine sediment, Aarhus Bay, Denmark. Limnology and Oceanography 40: 908–917.CrossRefGoogle Scholar
  34. Jöhnk, K.D., J. Huisman, J. Sharples, B. Sommeijer, P.M. Visser, and J.M. Stroom. 2008. Summer heatwaves promote blooms of harmful cyanobacteria. Global Change Biology 14: 495–512. doi: 10.1111/j.1365-2486.2007.01510.x.CrossRefGoogle Scholar
  35. Jonasson, L., Z. Wan, J.H.S. Hansen, and J. She. 2011. The impacts of physical processes on oxygen variations in the North Sea-Baltic Sea transition zone. Ocean Science Discussion 8: 1723–1755. doi: 10.5194/osd-8-1723-2011.CrossRefGoogle Scholar
  36. Jurevičius, R. 1959. Hydrochemical characteristic of the Kuršių Marios Lagoon. In Kuršių marios, ed. Institute of Biology, 69–108. Vilnius: Academy of Sciences. [In Russian with German summary]Google Scholar
  37. Kahru, M., U. Horstmann, and O. Rud. 1994. Increased cyanobacterial blooming in the Baltic Sea detected by satellites: natural fluctuation or ecosystem change? Ambio 23: 469–472.Google Scholar
  38. Kanoshina, I., U. Lips, and J.M. Leppänen. 2003. The influence of weather conditions (temperature and wind) on cyanobacterial bloom development in the Gulf of Finland (Baltic Sea). Harmful Algae 2: 29–41.CrossRefGoogle Scholar
  39. Kemp, W.M., P.A. Sampou, J. Garber, J. Tuttle, and W.R. Boynton. 1992. Seasonal depletion of oxygen from bottom waters of Chesapeake Bay: relative roles of benthic and planktonic respiration and physical exchange processes. Marine Ecology Progress Series 85: 137–152.CrossRefGoogle Scholar
  40. Kemp, W.M., J.M. Testa, D.J. Conley, D. Gilbert, and J.D. Hagy. 2009. Temporal responses of coastal hypoxia to nutrient loading and physical controls. Biogeosciences 6: 2985–3008. 10.5194/bg-6-2985-2009.Google Scholar
  41. Kotchenova, S.Y., E.F. Vermote, R. Matarrese, and F.J. Klemm Jr. 2006. Validation of a vector version of the 6S radiative transfer code for atmospheric correction of satellite data. Part I: Path radiance. Applied Optics 45: 6762–6774. doi: 10.1364/AO.45.006762.CrossRefGoogle Scholar
  42. Lorenzen, C.J. 1967. Determination of chlorophyll and pheopigments: spectrophotometric equations. Limnology and Oceanography 12: 343–346.CrossRefGoogle Scholar
  43. Minghelli-Roman, A., T. Laugier, L. Polidori, S. Mathieu, L. Loubersac, and P. Gouton. 2011. Satellite survey of seasonal trophic status and occasional anoxic ‘malaïgue’ crises in the Thau lagoon using MERIS images. International Journal of Remote Sensing 32(4): 909–923.CrossRefGoogle Scholar
  44. MRC, 1996. Annual report of scientific work. Center of Marine research. Environmental Protection Ministry, p 94.Google Scholar
  45. Murrell, M.C., J.G. Campbell, J.D. Hagy III, and J.M. Caffrey. 2009. Effects of irradiance on benthic and water column processes in a Gulf of Mexico estuary: Pensacola Bay, Florida, USA. Estuarine, Coastal and Shelf Science 81: 501–512.CrossRefGoogle Scholar
  46. Olenina, I. 1998. Long-term changes in the Kuršių Marios lagoon: eutrophication and phytoplankton response. Ekologija 1: 56–65.Google Scholar
  47. Paldaviciene, A., H. Mazur-Marzec, and A. Razinkovas. 2009. Toxic cyanobacteria blooms in the Lithuanian part of the Curonian Lagoon. Oceanologia 51(2): 203–216.CrossRefGoogle Scholar
  48. Park, K., Ch.-K. Kim, and W.W. Schroeder. 2007. Temporal variability in summertime bottom hypoxia in shallow areas of Mobile Bay, Alabama. Estuaries and Coasts 30(1): 54–65.Google Scholar
  49. Patt, F.S., 2002. Navigation algorithms for the SeaWiFS mission. NASA Technical Memorandum, vol. 206892. Greenbelt, MD: National Aeronautics and Space Administration, Goddard Space Flight Center.Google Scholar
  50. Pilkaitytė, R. 2003. Phytoplankton seasonal succession and abundance in the eutrophic estuarine lagoons. Summary of Doctoral Disertation. Klaipėda: Klaipėda University.Google Scholar
  51. Pilkaitytė, R., and A. Razinkovas. 2006. Factors controlling phytoplankton blooms in a temperate estuary: nutrient limitation and physical forcing. Hydrobiologia 555(1): 41–48.CrossRefGoogle Scholar
  52. Pilkaitytė, R., and A. Razinkovas. 2007. Seasonal changes in phytoplankton composition and nutrient limitation in a shallow Baltic lagoon. Boreal Environmental Research 12(5): 551–559.Google Scholar
  53. Post, A.F., R. De Wit, and L.R. Mur. 1985. Interactions between temperature and light intensity on growth and photosynthesis of the cyanobacterium Oscillatoria agardhii. Journal of Plankton Research 7: 487–495.CrossRefGoogle Scholar
  54. Rabalais, N.N., R.E. Turner, and W.J. Wiseman Jr. 2002. Gulf of Mexico hypoxia, A.K.A. “The Dead Zone”. Annual Review of Ecology and Systematics 33: 235–263. doi: 10.1146/annurev.ecolsys.33.010802.150513.CrossRefGoogle Scholar
  55. Razinkovas, A., I. Dailidienė and R. Pilkaitytė. 2008. Reduction of the Land-Based Discharges to the Curonian Lagoon in a View of a Climate Change Perspective. In Sustainable Use and Development of Watersheds. NATO Science for Peace and Security Series C: Environmental Security, ed. E. Gönenç,, A. Vadineanu, J. P. Wolflin, and R. C. Russo. Berlin: 403–413.Google Scholar
  56. Santer, R., and C. Schmechtig. 2000. Adjacency effects on water surfaces: primary scattering approximation and sensitivity study. Applied Optics 39: 361–375.CrossRefGoogle Scholar
  57. Souchu, P., A. Gasc, A. Vaquer, Y. Collos, H. Tournier, and J.M. Deslous-Paoli. 1998. Biogeochemical aspects of bottom anoxia in a Mediterranean lagoon. Marine Ecology Progress Series 164: 135–146.CrossRefGoogle Scholar
  58. Stanley, D.W., and S.W. Nixon. 1992. Stratification and bottom-water hypoxia in the Pamlico River Estuary. Estuaries 15: 270–281.CrossRefGoogle Scholar
  59. Steckbauer, A., C.M. Duarte, J. Carstensen, R. Vaquer-Sunyer, and D.J. Conley. 2011. Ecosystem impacts of hypoxia: thresholds of hypoxia and pathways to recovery. Environmental Research Letters 6(2): 1–12. doi: 10.1088/1748-9326/6/2/025003.CrossRefGoogle Scholar
  60. Tyler, R.M., D.C. Brady, and T. Targett. 2009. Temporal and spatial dynamics of diel-cycling hypoxia in estuarine tributaries. Estuaries and Coasts 32: 123–145.CrossRefGoogle Scholar
  61. Vahtera, E., D.J. Conley, B.G. Gustafsson, H. Kuosa, H. Pitkänen, O.P. Savchuk, T. Tamminen, M. Viitasalo, M. Voss, N. Wasmund, and F. Wulff. 2007. Internal ecosystem feedbacks enhance nitrogen-fixing cyanobacteria blooms and complicate management in the Baltic Sea. Ambio 36: 186–194.CrossRefGoogle Scholar
  62. Vermote, E.F., D. Tanrè, J.L. Deizè, M. Herman, and J.J. Morcrette. 1997. Second simulation of the satellite signal in the solar spectrum, 6S: an overview. Transactions on Geoscience and Remote Sensing 35: 675–686. doi: 10.1109/36.581987.CrossRefGoogle Scholar
  63. Vos, R.J., J.H.M. Hakvoort, R.W.J. Jordans, and B.W. Ibelings. 2003. Multiplatform optical monitoring of eutrophication in temporally and spatially variable lakes. The Science of the Total Environment 312: 221–243.CrossRefGoogle Scholar
  64. Walsby, A.E., P.K. Hayes, R. Boje, and L.J. Stal. 2001. The selective advantage of buoyancy provided by gas vesicles for planktonic cyanobacteria in the Baltic Sea. New Phytologist 136: 407–417.CrossRefGoogle Scholar
  65. Wynne, T.T., R.P. Stumpf, M.C. Tomlinson, and J. Dybleb. 2010. Characterizing a cyanobacterial bloom in western Lake Erie using satellite imagery and meteorological data. Limnology and Oceanography 55(5): 2025–2036.CrossRefGoogle Scholar
  66. Zilius, M., M. Bartoli, D.D. Daunys, R. Pilkaityte, and A. Razinkovas. 2012a. Patterns of benthic oxygen uptake in a hypertrophic lagoon: spatial variability and controlling factors. Hydrobiologia 699: 85–98.CrossRefGoogle Scholar
  67. Zilius, M., D. Daunys, J. Petkuviene, and M. Bartoli. 2012b. Sediment-water oxygen, ammonium and soluble reactive phosphorus fluxes in a turbid freshwater estuary (Curonian lagoon, Lithuania): evidences of benthic microalgal activity. Journal of Limnology 71(2): 309–319.CrossRefGoogle Scholar

Copyright information

© Coastal and Estuarine Research Federation 2013

Authors and Affiliations

  • Mindaugas Zilius
    • 1
  • Marco Bartoli
    • 2
  • Mariano Bresciani
    • 2
    • 3
  • Marija Katarzyte
    • 1
  • Tomas Ruginis
    • 1
  • Jolita Petkuviene
    • 1
  • Irma Lubiene
    • 1
  • Claudia Giardino
    • 3
  • Paul A. Bukaveckas
    • 4
  • Rutger de Wit
    • 1
    • 5
  • Arturas Razinkovas-Baziukas
    • 1
  1. 1.Coastal Research and Planning InstituteKlaipeda UniversityKlaipedaLithuania
  2. 2.Department of Environmental SciencesParma UniversityParmaItaly
  3. 3.Optical Remote Sensing GroupCNR-IREAMilanItaly
  4. 4.Department of Biology, Center for Environmental StudiesVirginia Commonwealth UniversityRichmondUSA
  5. 5.Ecologie des Systèmes marins côtiers (Ecosym), UMR 5119Université Montpellier 2, CNRS, IRD, Ifremer, Université Montpellier 1MontpellierFrance

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