Marine Biology

, Volume 155, Issue 5, pp 483–491 | Cite as

Nodularin concentrations in Baltic Sea zooplankton and fish during a cyanobacterial bloom

  • Miina KarjalainenEmail author
  • Jari-Pekka Pääkkönen
  • Heikki Peltonen
  • Vesa Sipiä
  • Terhi Valtonen
  • Markku Viitasalo
Original Paper


Toxic cyanobacterial blooms, dominated by Nodularia spumigena, are a recurrent phenomenon in the Baltic Sea during late summer. Nodularin, a potent hepatotoxin, has been previously observed to accumulate on different trophic levels, in zooplankton, mysid shrimps, fish as well as benthic organisms, even in waterfowl. While the largest concentrations of nodularin have been measured from the benthic organisms and the food web originating from them, the concentrations in the pelagic organisms are not negligible. The observations on concentrations in zooplankton and planktivorous fish are sporadic, however. A field study in the Gulf of Finland, northern Baltic Sea, was conducted during cyanobacterial bloom season where zooplankton (copepod Eurytemora affinis, cladoceran Pleopsis polyphemoides) and fish (herring, sprat, three-spined stickleback) samples for toxin analyses were collected from the same sampling areas, concurrently with phytoplankton community samples. N. spumigena was most abundant in the eastern Gulf of Finland. In this same sampling area, cladoceran P. polyphemoides contained more nodularin than in the other areas, suggesting that this species has a low capacity to avoid cyanobacterial exposure when the abundance of cyanobacterial filaments is high. In copepod E. affinis nodularin concentrations were high in all of the sampling areas, irrespective of the N. spumigena cell numbers. Furthermore, nodularin concentrations in herring samples were highest in the eastern Gulf of Finland. Three-spined stickleback contained the highest concentrations of nodularin of all the three fish species included in this study, probably because it prefers upper water layers where also the risk of nodularin accumulation in zooplankton is the highest. No linear relationship was found between N. spumigena abundance and nodularin concentration in zooplankton and fish, but in the eastern area where the most dense surface-floating bloom was observed, the nodularin concentrations in zooplankton were high. The maximum concentrations in zooplankton and fish samples in this study were higher than measured before, suggesting that the temporal variation of nodularin concentrations in pelagic communities can be large, and vary from negligible to potentially harmful.


Fish Sample Cyanobacterial Bloom Planktivorous Fish Zooplankton Sample Toxin Analysis 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Laura Helenius, Eveliina Lindén, Satu Viitasalo, and the whole crew onboard R/V Aranda during TROFIA04 cruise are warmly acknowledged for their help in sample collection. Kaarina Sivonen and Mika Vinni are thanked for all their help and discussions during the manuscript preparation. Two anonymous referees gave valuable comments on the manuscript. This study was financed by the Academy of Finland (project numbers 202437 and 205048), Walter and Andrée de Nottbeck Foundation, and Maj and Tor Nessling Foundation.


  1. Arrhenius F, Hansson S (1998) Growth of Baltic Sea young-of-the-year herring Clupea harengus is resource limited. Mar Ecol Prog Ser 191:295–299. doi: 10.3354/meps191295 CrossRefGoogle Scholar
  2. Burris JE (1980) Vertical migration of zooplankton in the Gulf of Finland. Am Midl Nat 103:316–322. doi: 10.2307/2424629 CrossRefGoogle Scholar
  3. Bury NR, Newlands AD, Eddy FB, Codd GA (1998) In vivo and in vitro intestinal transport of 3H-microcystin-LR, a cyanobacterial toxin, in rainbow trout (Oncorhyncus mykiss). Aquat Toxicol 42:139–148. doi: 10.1016/S0166-445X(98)00041-1 CrossRefGoogle Scholar
  4. Casini M, Cardinale M, Arrhenius F (2004) Feeding preferences of herring (Clupea harengus) and sprat (Sprattus sprattus) in the southern Baltic Sea. ICES J Mar Sci 61:1267–1277. doi: 10.1016/j.icesjms.2003.12.011 CrossRefGoogle Scholar
  5. De Maagd P, Hendriks AJ, Seinen W, Sijm DTHM (1999) pH-dependent hydrophobicity of the cyanobacteria toxin microcystin-LR. Water Res 33:677–680. doi: 10.1016/S0043-1354(98)00258-9 CrossRefGoogle Scholar
  6. Engström J, Koski M, Viitasalo M, Reinikainen M, Repka S, Sivonen K (2000) Feeding interactions of Eurytemora affinis and Acartia bifilosa with toxic and non-toxic Nodularia sp. J Plankton Res 22:1403–1409. doi: 10.1093/plankt/22.7.1403 CrossRefGoogle Scholar
  7. Flinkman J, Pääkkönen J-P, Saesmaa S, Bruun J (2007) Zooplankton time series 1979–2005 in the Baltic Sea—life in a vice of bottom-up and top-down forces. In: Olsonen R (ed) FIMR monitoring of the Baltic Sea environment—annual report 2006. MERI—Report Series of the Finnish Institute of Marine Research No. 59, pp 73–86Google Scholar
  8. Gasparini S, Castel J (1997) Autotrophic and heterotrophic nanoplankton in the diet of the estuarine copepods Eurytemora affinis and Acartia bifilosa. J Plant Res 19:877–890Google Scholar
  9. HELCOM (2003) The Baltic marine environment 1999–2002. Baltic environment proceedings, p 87. 48Google Scholar
  10. Kahru M, Horstmann U, Rud O (1994) Satellite detection of increased cyanobacteria blooms in the Baltic Sea—natural fluctuation or ecosystem change. Ambio 23:469–472Google Scholar
  11. Kankaanpää HT, Sipiä VO, Kuparinen JS, Ott JL, Carmichael WW (2001) Nodularin analyses and toxicity of a Nodularia spumigena (Nostocales, Cyanobacteria) water-bloom in the western Gulf of Finland, Baltic Sea, in August 1999. Phycologia 40:268–274CrossRefGoogle Scholar
  12. Kankaanpää HT, Turunen A-K, Karlsson K, Bylund G, Meriluoto J, Sipiä V (2005) Heterogeneity of nodularin bioaccumulation in northern Baltic Sea flounders in 2002. Chemosphere 59:1091–1097. doi: 10.1016/j.chemosphere.2004.12.010 CrossRefGoogle Scholar
  13. Karjalainen M, Reinikainen M, Spoof L, Meriluoto J, Sivonen K, Viitasalo M (2005) Trophic transfer of cyanobacterial toxins from zooplankton to planktivores: consequences for pike larvae and mysid shrimps. Environ Toxicol 20:354–362. doi: 10.1002/tox.20112 CrossRefGoogle Scholar
  14. Karjalainen M, Kozlowsky-Suzuki B, Lehtiniemi M, Engström-Öst J, Kankaanpää H, Viitasalo M (2006) Nodularin accumulation during cyanobacterial blooms and experimental depuration in zooplankton. Mar Biol (Berl) 148:683–691. doi: 10.1007/s00227-005-0126-y CrossRefGoogle Scholar
  15. Karlsson KM, Kankaanpää H, Huttunen M, Meriluoto J (2005a) First observation of microcystin-LR in pelagic cyanobacterial blooms in the northern Baltic Sea. Harmful Algae 4:163–166. doi: 10.1016/j.hal.2004.02.002 CrossRefGoogle Scholar
  16. Karlsson KM, Spoof LEM, Meriluoto JAO (2005b) Quantitative LC-ESI-MS analyses of microcystins and nodularin-R in animal tissue—matrix effects and method validation. Environ Toxicol 20:381–389. doi: 10.1002/tox.20115 CrossRefGoogle Scholar
  17. Kononen K, Sivonen K, Lehtimäki J (1993) Toxicity of the phytoplankton blooms in the Gulf of Finland and Gulf of Bothnia, Baltic Sea. In: Smayda TJ, Shimizu Y (eds) Toxic phytoplankton blooms in the sea. Elsevier Science, Amsterdam, pp 98–112Google Scholar
  18. Kononen K, Kuparinen J, Mäkelä K, Laanemets J, Pavelson J, Nõmmann S (1996) Initiation of cyanobacterial blooms in a frontal region at the entrance to the Gulf of Finland, Baltic Sea. Limnol Oceanogr 41:98–112CrossRefGoogle Scholar
  19. Kononen K, Hällfors S, Kokkonen M, Kuosa H, Laanemets J, Pavelson J et al (1998) Development of a subsurface chlorophyll maximum at the entrance to the Gulf of Finland, Baltic Sea. Limnol Oceanogr 43:1089–1106CrossRefGoogle Scholar
  20. Koski M, Schmidt K, Engström-Öst J, Viitasalo M, Jónasdóttir S, Repka S et al (2002) Calanoid copepods feed and produce eggs in the presence of toxic cyanobacteria Nodularia spumigena. Limnol Oceanogr 47:878–885CrossRefGoogle Scholar
  21. Kozlowsky-Suzuki B, Karjalainen M, Lehtiniemi M, Engström-Öst J, Koski M, Carlsson P (2003) Feeding, reproduction and toxin accumulation by the copepods Acartia bifilosa and Eurytemora affinis in the presence of the toxic cyanobacterium Nodularia spumigena. Mar Ecol Prog Ser 249:237–249. doi: 10.3354/meps249237 CrossRefGoogle Scholar
  22. Laamanen MJ, Gugger MF, Lehtimäki JM, Haukka K, Sivonen K (2001) Diversity of toxic and non-toxic Nodularia isolates (Cyanobacteria) and filaments from the Baltic Sea. Appl Environ Microbiol 67:4638–4647. doi: 10.1128/AEM.67.10.4638-4647.2001 CrossRefGoogle Scholar
  23. Metcalf JS, Beattie KA, Pflughmacher S, Codd GA (2000) Immuno-crossreactivity and toxicity assessment of conjugation products of the cyanobacterial toxin, microcystin-LR. FEMS Microbiol Lett 189:155–158. doi: 10.1111/j.1574-6968.2000.tb09222.x CrossRefGoogle Scholar
  24. Pääkkönen J-P, Rönkkönen S, Karjalainen M, Viitasalo M (2008) Physiological effects in juvenile three-spined sticklebacks feeding on toxic cyanobacterium Nodularia spumigena-exposed zooplankton. J Fish Biol 72:485–499CrossRefGoogle Scholar
  25. Peltonen H, Vinni M, Lappalainen A, Pönni J (2004) Spatial feeding patterns of herring (Clupea harengus L.), sprat (Sprattus sprattus L.), and the three-spined stickleback (Gasterosteus aculeatus L.) in the Gulf of Finland, Baltic Sea. ICES J Mar Sci 61:966–971. doi: 10.1016/j.icesjms.2004.06.008 CrossRefGoogle Scholar
  26. Peltonen H, Luoto M, Pääkkönen J-P, Karjalainen M, Tuomaala A, Pönni J et al (2007) Pelagic fish abundance in relation to regional environmental variations in the Gulf of Finland, Northern Baltic Sea. ICES J Mar Sci 64:487–495. doi: 10.1093/icesjms/fsl044 CrossRefGoogle Scholar
  27. Poutanen EL, Nikkilä K (2001) Carotenoid pigments as tracers of cyanobacterial blooms in recent and post-glacial sediments of the Baltic Sea. Ambio 30:179–183. doi: 10.1639/0044-7447(2001)030[0179:CPATOC]2.0.CO;2 CrossRefGoogle Scholar
  28. Raid T, Lankov A (1995) Recent changes in the growth and feeding of Baltic herring and sprat in the northeastern Baltic Sea. Proc Est Acad Sci Ecol 5:38–55Google Scholar
  29. Rajaniemi P, Hrouzek P, Kaštovská K, Willame R, Rautala A, Hoffmann L et al (2005) Phylogenetic and morphological evaluation of the genera Anabaena, Aphanizomenon, Trichormus and Nostoc (Nostocales, Cyanobacteria). Int J Syst Evol Microbiol 55:11–26. doi: 10.1099/ijs.0.63276-0 CrossRefGoogle Scholar
  30. Sipiä VO, Kankaanpää H, Flinkman J, Lahti K, Meriluoto JAO (2001a) Time-dependent accumulation of cyanobacterial hepatotoxins in flounders (Platichtys flesus) and mussels (Mytilus edulis) from the northern Baltic Sea. Environ Toxicol 16:330–336. doi: 10.1002/tox.1040 CrossRefGoogle Scholar
  31. Sipiä V, Kankaanpää H, Lahti K, Carmichael WW, Meriluoto J (2001b) Detection of nodularin in flounders and cod from the Baltic Sea. Environ Toxicol 16:121–126. doi: 10.1002/tox.1015 CrossRefGoogle Scholar
  32. Sipiä VO, Kankaanpää HT, Pflugmacher S, Flinkman J, Furey A, James KJ (2002a) Bioaccumulation and detoxication of nodularin in tissues of flounder (Platichthys flesus), mussels (Mytilus edulis, Dreissena polymorpha), and clams (Macoma balthica) from the northern Baltic Sea. Ecotoxicol Environ Saf 53:305–311. doi: 10.1006/eesa.2002.2222 CrossRefGoogle Scholar
  33. Sipiä VO, Lahti K, Kankaanpää HT, Vuorinen PJ, Meriluoto JAO (2002b) Screening for cyanobacterial hepatotoxins in herring and salmon from the Baltic Sea. Aquat Ecosyst Health Manage 5:451–456. doi: 10.1080/14634980290001959 CrossRefGoogle Scholar
  34. Sipiä VO, Sjövall O, Valtonen T, Barnaby DL, Codd GA, Metcalf JS et al (2006) Analysis of nodularin-R in eider (Somateria mollissima), roach (Rutilus rutilus L.), and flounder (Platichtys flesus L.) liver and muscle samples from the western Gulf of Finland, northern Baltic Sea. Environ Toxicol Chem 25:2834–2839. doi: 10.1897/06-185R.1 CrossRefGoogle Scholar
  35. Sipiä V, Kankaanpää H, Peltonen H, Vinni M, Meriluoto J (2007) Transfer of nodularin to three-spined stickleback (Gasterosteus aculeatus L.), herring, (Clupea harengus L.), and salmon (Salmo salar L.) in the northern Baltic Sea. Ecotoxicol Environ Saf 66:421–425. doi: 10.1016/j.ecoenv.2006.02.006 CrossRefGoogle Scholar
  36. Sivonen K, Kononen K, Carmichael WW, Dahlem AM, Rinehart K, Kiviranta J et al (1989) Occurrence of the hepatotoxic cyanobacterium Nodularia spumigena in the Baltic Sea and the structure of the toxin. Appl Environ Microbiol 55:1990–1995PubMedPubMedCentralGoogle Scholar
  37. Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplanktonmethodik. Mitt Int Verein Theor Angew Limnol 29:117–126Google Scholar
  38. Williams DE, Dawe S, Kent M, Andersen R, Graig M, Holmes C (1997) Bioaccumulation and clearance of microcystins from salt water mussels, Mytilus edulis, and in vivo evidence for covalently bound microcystins in mussel tissues. Toxicon 35:1617–1627. doi: 10.1016/S0041-0101(97)00039-1 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Miina Karjalainen
    • 1
    • 4
    Email author
  • Jari-Pekka Pääkkönen
    • 2
  • Heikki Peltonen
    • 3
  • Vesa Sipiä
    • 1
  • Terhi Valtonen
    • 1
  • Markku Viitasalo
    • 1
  1. 1.Finnish Institute of Marine ResearchHelsinkiFinland
  2. 2.City of Helsinki Environment Centre HelsinkiFinland
  3. 3.Finnish Environment InstituteHelsinkiFinland
  4. 4.Kotka Maritime Research CentreKotkaFinland

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