, Volume 701, Issue 1, pp 25–35 | Cite as

Plankton community dynamics during decay of a cyanobacteria bloom: a mesocosm experiment

  • Jonna Engström-ÖstEmail author
  • Riitta Autio
  • Outi Setälä
  • Sanna Sopanen
  • Sanna Suikkanen
Primary Research Paper


The aim of the work was to study the effects of a decaying cyanobacteria bloom on nutrient dynamics, plankton community development and production rates of bacteria and primary producers. It was hypothesised that the system would turn more heterotrophic following the decay of the bloom. A 10-day outdoors mesocosm experiment was performed in early June in a brackish-water environment. Non-toxic filamentous cyanobacteria Aphanizomenon flos-aquae were added to the treatment, whereas the control lacked cyanobacteria. A. flos-aquae decayed rapidly, and was absent from the units by day 2. Significantly higher bacteria abundances, lower nanoflagellate densities and higher ciliate abundances were found, suggesting a bottom-up regulated process in the treatments bags. N:P ratios were low (6–12), suggesting N-limitation. Bacteria correlated negatively with numbers of heterotrophic nanoflagellates (HNF), suggesting grazing on bacteria by HNF. Primary production correlated positively with irradiance, chlorophyll a and inorganic nutrients in all units. The rapidly decaying A. flos-aquae biomass imposed a significant bottom-up regulation in the treatment mesocosms, and the system turned from autotrophic into more heterotrophic with time. The rapid decay also caused some similarities and parallel changes between the treatment and the control.


Aphanizomenon Bacteria Bottom-up regulation Ciliates Nanoflagellates Production rates 



We thank Prof. K. Sivonen (University of Helsinki) for the Aphanizomenon strain, U. Sjölund for culturing algae, T. Sjölund for help with mesocosm set-up, P. Hakanen for microscopy and E. Salminen & M. Sjöblom for nutrient analyses. A. Brutemark is thanked for valuable discussions and for commenting on the manuscript. Funding was received from the Academy of Finland (nr. 125251, 255566), Maj and Tor Nessling Foundation, and Walter and Andrée de Nottbeck Foundation.


  1. Acinas, S. G., T. H. A. Haverkamp, J. Huisman & L. J. Stal, 2009. Phenotypic and genetic diversification of Pseudanabaena spp. (cyanobacteria). The ISME Journal 3: 31–46.PubMedCrossRefGoogle Scholar
  2. Andersson, A., S. Hajdu, P. Haecky, J. Kuparinen & J. Wikner, 1996. Succession and growth limitation of phytoplankton in the Gulf of Bothnia (Baltic Sea). Marine Biology 126: 791–801.CrossRefGoogle Scholar
  3. Autio, R., 1992. Temperature regulation of brackish water bacterioplankton. Archiv für Hydrobiologie – Beiheft Ergebnisse der Limnologie 37: 253–263.Google Scholar
  4. Autio, R., 1998. Response of seasonally cold-water bacterioplankton to temperature and substrate treatments. Estuarine Coastal and Shelf Science 46: 465–474.CrossRefGoogle Scholar
  5. Branco, P., M. Stomp, M. Egas & J. Huisman, 2010. Evolution of nutrient uptake reveals a trade-off in the ecological stoichiometry of plant-herbivore interactions. American Naturalist 176: 162–176.CrossRefGoogle Scholar
  6. Deng, L. & P. K. Hayes, 2008. Evidence for cyanophages active against bloom-forming freshwater cyanobacteria. Freshwater Biology 53: 1240–1252.CrossRefGoogle Scholar
  7. Devercelli, M. & V. Williner, 2006. Diatom grazing by Aegla uruguayana (Decapoda: Anomura: Aeglidae): digestibility and cell viability after gut passage. International Journal of Limnology 42: 73–77.CrossRefGoogle Scholar
  8. Engström-Öst, J., M. Koski, K. Schmidt, M. Viitasalo, S. H. Jónasdóttir, M. Kokkonen, S. Repka & K. Sivonen, 2002. Effects of toxic cyanobacteria on a plankton assemblage: community development during decay of Nodularia spumigena. Marine Ecology Progress Series 232: 1–14.CrossRefGoogle Scholar
  9. Faithfull, C. L., A.-K. Bergström & T. Vrede, 2011. Effects of nutrients and physical lake characteristics on bacterial and phytoplankton production: a meta-analysis. Limnology and Oceanography 56: 1703–1713.Google Scholar
  10. Goldman, J. C., 1980. Physiological processes, nutrient availability, and the concept of relative growth rate in marine plankton ecology. In Falkowski, P. G. (ed.), Primary Productivity in the Sea. Plenum Press, New York: 179–194.CrossRefGoogle Scholar
  11. Gugger, M., C. Lyra, I. Suominen, I. Tsitko, J. F. Humbert, M. S. Salkinoja-Salonen & K. Sivonen, 2002. Cellular fatty acids as chemotaxonomic markers of the genera Anabaena, Aphanizomenon, Microcystis, Nostoc and Planktothrix (cyanobacteria). International Journal of Systematic and Evolutionary Microbiology 52: 1007–1015.PubMedCrossRefGoogle Scholar
  12. Hairston, N. G. Jr., C. L. Holtmeier, W. Lampert, L. J. Weider, D. M. Post, J. M. Fisher, C. E. Cáceres, J. A. Fox & U. Gaedke, 2001. Natural selection for grazing resistance to toxic cyanobacteria: evolution of phenotypic plasticity? Evolution 55: 2203–2214.PubMedCrossRefGoogle Scholar
  13. Halinen, K., D. P. Fewer, L. M. Sihvonen, C. Lyra, E. Eronen & K. Sivonen, 2008. Genetic diversity in strains of the genus Anabaena isolated from planktonic and benthic habitats of the Gulf of Finland (Baltic Sea). FEMS Microbiology and Ecology 64: 199–208.CrossRefGoogle Scholar
  14. Haney, J. F., J. J. Sasner & M. Ikawa, 1995. Effects of products released by Aphanizomenon flos-aquae and purified saxitoxin on the movements of Daphnia carinata feeding appendages. Limnology and Oceanography 40: 263–272.CrossRefGoogle Scholar
  15. Heinänen, A., K. Kononen, H. Kuosa, J. Kuparinen & K. Mäkelä, 1995. Bacterioplankton growth associated with physical fronts during a cyanobacterial bloom. Marine Ecology Progress Series 16: 233–245.CrossRefGoogle Scholar
  16. Hobbie, J. E., R. J. Daley & S. Jasper, 1977. Use of nuclepore filters for counting bacteria by fluorescence microscopy. Applied Environmental Microbiology 33: 1225–1228.Google Scholar
  17. Ikawa, M., J. J. Sasner & J. F. Haney, 1994. Lipids of cyanobacterium Aphanizomenon flos-aquae and inhibition of Chlorella growth. Journal of Chemical Ecology 20: 2429–2436.CrossRefGoogle Scholar
  18. Iriarte, A., A. Sarobe & E. Orive, 2008. Seasonal variability in bacterial abundance, production and protistan bacterivory in the lower Urdaibai estuary, Bay of Biscay. Aquatic Microbial Ecology 52: 273–282.CrossRefGoogle Scholar
  19. Jespersen, A. M. & K. Christoffersen, 1987. Measurements of chlorophyll a from phytoplankton using ethanol as extraction solvent. Archive für Hydrobiologie 109: 445–454.Google Scholar
  20. Karjalainen, M., B. Kozlowsky-Suzuki, M. Lehtiniemi, J. Engström-Öst, H. Kankaanpää & M. Viitasalo, 2006. Nodularin accumulation during cyanobacterial blooms and experimental depuration in zooplankton. Marine Biology 148: 683–691.CrossRefGoogle Scholar
  21. Kirchman, D. L., E. K’Nees & R. Hodson, 1985. Leucine incorporation and its potential as a measure of protein synthesis by bacteria in natural aquatic systems. Applied Environmental Microbiology 49: 599–607.Google Scholar
  22. Kivi, K. & O. Setälä, 1995. Simultaneous measurement of food particle selection and clearance rates of planktonic oligotrich ciliates (Ciliophora: Oligotrichina). Marine Ecology Progress Series 119: 125–137.CrossRefGoogle Scholar
  23. Kivi, K., S. Kaitala, H. Kuosa, J. Kuparinen, E. Leskinen, R. Lignell, B. Marcussen & T. Tamminen, 1993. Nutrient limitation and grazing control of the Baltic plankton community during annual succession. Limnology and Oceanography 38: 893–905.CrossRefGoogle Scholar
  24. Kononen, K., 1988. Phytoplankton summer assemblages in relation to environmental factors at the entrance to the Gulf of Finland during 1972–1985. Kieler Meeresforschungen Sonderheft 6: 281–294.Google Scholar
  25. Koroleff, F., 1979. Meriveden yleisimmät kemialliset analyysimenetelmät. Meri 7: 1–60. (in Finnish).Google Scholar
  26. Kotai, J., 1972. Instructions for preparation of modified nutrient solution Z8 for algae. Norwegian Institute of Water Research Oslo B-11/69: 1–5.Google Scholar
  27. Kuparinen, J., 1988. Development of bacterioplankton during winter and early spring at the entrance to the Gulf of Finland, Baltic Sea. Verhandlungen des Internationalen Verein Limnologie 23: 1869–1878.Google Scholar
  28. Kuuppo, P., 1994. Heterotrophic nanoflagellates in the microbial food web of the SW coast of Finland, Baltic Sea. PhD thesis, University of Helsinki, Finland.Google Scholar
  29. Kuuppo, P., K. Samuelsson, R. Lignell, J. Seppälä, T. Tamminen & A. Andersson, 2003. Fate of increased production in late-summer plankton communities due to nutrient enrichment of the Baltic Proper. Aquatic Microbial Ecology 32: 47–60.CrossRefGoogle Scholar
  30. Kuuppo-Leinikki, P., 1990. Protozoan grazing on planktonic bacteria and its impact on bacterial population. Marine Ecology Progress Series 63: 227–238.CrossRefGoogle Scholar
  31. Laamanen, M., L. Forsström & K. Sivonen, 2002. Diversity of Aphanizomenon flos-aquae (cyanobacteria) populations along a Baltic Sea salinity gradient. Applied and Environmental Microbiology 68: 5296–5303.PubMedCrossRefGoogle Scholar
  32. Lignell, R., S. Kaitala & H. Kuosa, 1992. Factors controlling phyto and bacterioplankton in late spring on a salinity gradient in the northern Baltic. Marine Ecology Progress Series 86: 273–281.CrossRefGoogle Scholar
  33. Lignell, R., J. Seppälä, P. Kuuppo, T. Tamminen, T. Andersen & I. Gismervik, 2003. Beyond bulk properties: responses of coastal summer plankton communities to nutrient enrichment in the northern Baltic Sea. Limnology Oceanography 48: 189–209.CrossRefGoogle Scholar
  34. Menden-Deuer, S. & E. J. Lessard, 2000. Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnology and Oceanography 45: 569–579.CrossRefGoogle Scholar
  35. Murrell, M. C., 2003. Bacterioplankton dynamics in a subtropical estuary: evidence for substrate limitation. Aquatic Microbial Ecology 32: 239–250.CrossRefGoogle Scholar
  36. Niemi, Å., J. Kuparinen, A. Uusi-Rauva & K. Korhonen, 1983. Preparation of 14C-labeled algal samples for liquid scintillation counting. Hydrobiologia 106: 149–156.CrossRefGoogle Scholar
  37. Niemistö, L., I. Rinne, T. Melvasalo & Å. Niemi, 1989. Blue-green algae and their nitrogen fixation in the Baltic Sea in 1980, 1982 and 1984. Meri 17: 1–59.Google Scholar
  38. Olrik, K., P. Blomqvist, P. Brettum, G. Cronberg & P. Eloranta, 1998. Methods for quantitative assessment of phytoplankton in freshwaters. Naturvårdsverket, Stockholm.Google Scholar
  39. Østensvik, Ø., O. M. Skulberg, B. Underdal & V. Hormazabal, 1998. Antibacterial properties of extracts from selected planktonic freshwater cyanobacteria – a comparative study of bacterial bioassays. Journal of Applied Microbiology 84: 1117–1124.PubMedCrossRefGoogle Scholar
  40. Paerl, H. W. & J. Huisman, 2008. Blooms like it hot. Science 320: 57–58.PubMedCrossRefGoogle Scholar
  41. Paerl, H. W. & J. Huisman, 2009. Climate change: a catalyst for global expansion of harmful cyanobacterial blooms. Environmental Microbiology Reports 1: 27–37.CrossRefGoogle Scholar
  42. Ptacnik, R., T. Andersen & T. Tamminen, 2010. Performance of the Redfield ratio and a family of nutrient limitation indicators as thresholds for phytoplankton N vs. P limitation. Ecosystems 13: 1201–1214.CrossRefGoogle Scholar
  43. Putt, M. & D. K. Stoecker, 1989. An experimentally determined carbon: volume ratio for marine “oligotrichous” ciliates from estuarine and coastal waters. Limnology and Oceanography 34: 1097–1103.CrossRefGoogle Scholar
  44. Redfield, A. C., B. H. Ketchum & F. A. Richards, 1963. The influence of organisms on the composition of sea-water. In Hill, M. N. (ed.), The Sea, Vol. 2. Wiley, New York: 26–77.Google Scholar
  45. Repka, S., M. Meyerhöfer, K. von Bröckel & K. Sivonen, 2004. Associations of cyanobacterial toxin, nodularin, with environmental factors and zooplankton in the Baltic Sea. Microbial Ecology 47: 350–358.PubMedCrossRefGoogle Scholar
  46. Riemann, L., G. F. Steward & F. Azam, 2000. Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Applied Environmental Microbiology 66: 578–587.CrossRefGoogle Scholar
  47. Sellner, K., 1997. Physiology, ecology, and toxic properties of marine cyanobacterial blooms. Limnology and Oceanography 42: 1089–1104.CrossRefGoogle Scholar
  48. Serôdio, J., S. Vieira & S. Cruz, 2008. Photosynthetic activity, photoprotection and photoinhibition in intertidal microphytobenthos as studied in situ using variable chlorophyll fluorescence. Continental Shelf Research 28: 1363–1375.CrossRefGoogle Scholar
  49. Sivonen, K., K. Kononen, A.-L. Esala & S.-I. Niemelä, 1989. Toxicity and isolation of the cyanobacterium Nodularia spumigena from the southern Baltic Sea in 1986. Hydrobiologia 185: 3–8.CrossRefGoogle Scholar
  50. Sokal, R. R. & F. J. Rohlf, 1995. Biometry. WH Freeman, New York.Google Scholar
  51. Sopanen, S., P. Uronen, P. Kuuppo, C. Svensen, A. Rühl, T. Tamminen, E. Granéli & C. Legrand, 2009. Transfer of nodularin to the copepod Eurytemora affinis through the microbial food web. Aquatic Microbial Ecology 55: 115–130.CrossRefGoogle Scholar
  52. Suikkanen, S., G. O. Fistarol & E. Granéli, 2004. Allelopathic effects of the Baltic cyanobacteria Nodularia spumigena, Aphanizomenon flos-aquae and Anabaena lemmermannii on algal monocultures. Journal of Experimental Marine Biology and Ecology 308: 85–101.CrossRefGoogle Scholar
  53. Suikkanen, S., G. O. Fistarol & E. Granéli, 2005. Effects of cyanobacterial allelochemicals on a natural plankton community. Marine Ecology Progress Series 287: 1–9.CrossRefGoogle Scholar
  54. Suikkanen, S., M. Laamanen & M. Huttunen, 2007. Long-term changes in summer phytoplankton communities of the open northern Baltic Sea. Estuarine Coastal and Shelf Science 71: 580–592.CrossRefGoogle Scholar
  55. Tamminen, T., J. Kuparinen & R. Lignell, 1984. Diurnal cycles of phytoplankton exudation and bacterial uptake of organic substrates. Ergebnisse der Limnologie 19: 267–279.Google Scholar
  56. Thingstad, T. F., R. G. J. Bellerby, G. Bratbak, K. Y. Børsheim, J. K. Egge, M. Heldal, A. Larsen, C. Neill, J. Nejstgaard, S. Norland, R.-A. Sandaa, E. F. Skjoldal, T. Tanaka, R. Thyrhaug & B. Töpper, 2008. Counterintuitive carbon-to-nutrient coupling in an Arctic pelagic ecosystem. Nature 455: 387–390.PubMedCrossRefGoogle Scholar
  57. Tulonen, T., 1993. Bacterial production in a mesohumic lake estimated from [14C]leucine incorporation rate. Microbial Ecology 26: 201–217.CrossRefGoogle Scholar
  58. Utermöhl, H., 1958. Zur Vervollkommnung der quantitative Phytoplankton-Methodik. Mitteilungen. Internationale Vereiningung für Theoretische und Angewandte Limnologie 29: 117–126. (in German).Google Scholar
  59. Viherluoto, M. & M. Viitasalo, 2000. Temporal variability in functional responses and prey selectivity of the pelagic mysid, Mysis mixta, in natural prey assemblages. Marine Biology 138: 575–583.CrossRefGoogle Scholar
  60. Walve, J. & U. Larsson, 2007. Blooms of Baltic Sea Aphanizomenon sp. (Cyanobacteria) collapse after internal phosphorus depletion. Aquatic Microbial Ecology 49: 57–69.CrossRefGoogle Scholar
  61. Walve, J. & U. Larsson, 2010. Seasonal changes in Baltic Sea seston stoichiometry: the influence of diazotrophic cyanobacteria. Marine Ecology Progress Series 407: 13–25.CrossRefGoogle Scholar
  62. Zöllner, E., H.-G. Hoppe, U. Sommer & K. Jürgens, 2009. Effect of zooplankton-mediated trophic cascades on marine microbial food web components (bacteria, nanoflagellates, ciliates). Limnology and Oceanography 54: 262–275.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Jonna Engström-Öst
    • 1
    Email author
  • Riitta Autio
    • 2
    • 3
  • Outi Setälä
    • 2
    • 3
  • Sanna Sopanen
    • 4
  • Sanna Suikkanen
    • 2
    • 3
  1. 1.Aronia Coastal Zone Research TeamYrkeshögskolan Novia & Åbo AkademiEkenäsFinland
  2. 2.Finnish Environment Institute, Marine Research CentreHelsinkiFinland
  3. 3.Tvärminne Zoological StationHankoFinland
  4. 4.RambollEspooFinland

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