, Volume 156, Issue 1, pp 147–154 | Cite as

Induction of toxin production in dinoflagellates: the grazer makes a difference

Plant-Animal Interactions - Original Paper


The dinoflagellate Alexandrium minutum has previously been shown to produce paralytic shellfish toxins (PST) in response to waterborne cues from the copepod Acartia tonsa. In order to investigate if grazer-induced toxin production is a general or grazer-specific response of A. minutum to calanoid copepods, we exposed two strains of A. minutum to waterborne cues from three other species of calanoid copepods, Acartia clausi, Centropages typicus and Pseudocalanus sp. Both A. minutum strains responded to waterborne cues from Centropages and Acartia with significantly increased cell-specific toxicity. Waterborne cues from Centropages caused the strongest response in the A. minutum cells, with 5 to >20 times higher toxin concentrations compared to controls. In contrast, neither of the A. minutum strains responded with significantly increased toxicity to waterborne cues from Pseudocalanus. The absolute increase in PST content was proportional to the intrinsic toxicity of the different A. minutum strains that were used. The results show that grazer-induced PST production is a grazer-specific response in A. minutum, and its potential ecological importance will thus depend on the composition of the zooplankton community, as well as the intrinsic toxin-producing properties of the A. minutum population.


Acartia tonsa Alexandrium minutum Centropages typicus Inducible defense Paralytic shellfish toxin Pseudocalanus sp. 



We thank Maria Grazia Giacobbe for kindly providing the CNR AMIA5 strain of A. minutum. Financial support was provided by the Swedish Research Council Formas through contract 21.0/2003-1122 to HP, by MARICE (Marine Chemical Ecology—an interdisciplinary research platform at the Faculty of Sciences, Göteborg University, Sweden), and by the Wåhlström, Carl Trygger and Colliander Foundations. The study complies with current law.


  1. Asp TN, Larsen S, Aune T (2004) Analysis of PSP toxins in Norwegian mussels by a post-column derivatization HPLC method. Toxicon 43:319–327Google Scholar
  2. Barnard R, et al. (2004) Continuous plankton records: plankton atlas of the North Atlantic Ocean (1958–1999). II. Biogeographical charts. Mar Ecol Prog Ser (Suppl):11–75Google Scholar
  3. Borell EM, Foggo A, Coleman RA (2004) Induced resistance in intertidal macroalgae modifies feeding behaviour of herbivorous snails. Oecologia 140:328–334PubMedCrossRefGoogle Scholar
  4. Calbet A, Garrido S, Saiz E, Alcaraz M, Duarte CM (2001) Annual zooplankton succession in coastal NW Mediterranean waters: the importance of the smaller size fractions. J Plankton Res 23:319–331CrossRefGoogle Scholar
  5. Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator–prey systems: a review and prospectus. Ecoscience 5:338–352Google Scholar
  6. Colin SP, Dam HG (2002) Testing for toxic effects of prey on zooplankton using sole versus mixed diets. Limnol Oceanogr 47:1430–1437CrossRefGoogle Scholar
  7. Cronin G, Hay ME (1996) Induction of seaweed chemical defenses by amphipod grazing. Ecology 77:2287–2301CrossRefGoogle Scholar
  8. Franco JM, Fernandez P, Reguera B (1994) Toxin profiles of natural populations and cultures of Alexandrium minutum Halim from Galician (Spain) coastal waters. J Appl Phycol 6:275–279CrossRefGoogle Scholar
  9. Frost BW (1989) A taxonomy of the marine calanoid copepod genus Pseudocalanus. Can J Zool 67:525–551CrossRefGoogle Scholar
  10. Green TR, Ryan CA (1972) Wound-induced proteinase inhibitorin plant leaves: a possible defense mechanism against insects. Science 175:776–777PubMedCrossRefGoogle Scholar
  11. Guisande C, Frangopulos M, Maneiro I, Vergara AR, Riveiro I (2002) Ecological advantages of toxin production by the dinoflagellate Alexandrium minutum under phosphorus limitation. Mar Ecol Prog Ser 225:169–176CrossRefGoogle Scholar
  12. Ha K, Jang MH, Takamura N (2004) Colony formation in planktonic algae induced by zooplankton culture media filtrate. J Freshwater Ecol 19:9–16Google Scholar
  13. Halsband C, Hirche HJ (2001) Reproductive cycles of dominant calanoid copepods in the North Sea. Mar Ecol Prog Ser 209:219–229CrossRefGoogle Scholar
  14. Hessen DO, Van Donk E (1993) Morphological-changes in Scenedesmus induced by substances released from Daphnia. Arch Hydrobiol 127:129–140Google Scholar
  15. Hillebrand H, Durselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424CrossRefGoogle Scholar
  16. Iyengar EV, Harvell CD (2002) Specificity of cues inducing defensive spines in the bryozoan Membranipora membranacea. Mar Ecol Prog Ser 225:205–218CrossRefGoogle Scholar
  17. Jakobsen HH, Tang KW (2002) Effects of protozoan grazing on colony formation in Phaeocystis globosa (Prymnesiophyceae) and the potential costs and benefits. Aquat Microb Ecol 27:261–273CrossRefGoogle Scholar
  18. Jang MH, Ha K, Joo GJ, Takamura N (2003) Toxin production of cyanobacteria is increased by exposure to zooplankton. Freshwater Biol 48:1540–1550CrossRefGoogle Scholar
  19. John EH, Flynn KJ (2002) Modelling changes in paralytic shellfish toxin content of dinoflagellates in response to nitrogen and phosphorus supply. Mar Ecol Prog Ser 225:147–160CrossRefGoogle Scholar
  20. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, ChicagoGoogle Scholar
  21. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394Google Scholar
  22. Leftley JW, Keller DK, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. J Phycol 23:633–638Google Scholar
  23. Lilly EL, Halanych KM, Anderson DM (2005) Phylogeny, biogeography, and species boundaries within the Alexandrium minutum group. Harmful Algae 4:1004–1020CrossRefGoogle Scholar
  24. Long JD, Smalley GW, Barsby T, Anderson JT, Hay ME (2007) Chemical cues induce consumer-specific defenses in a bloom-forming marine phytoplankton. PNAS 104:10512–10517PubMedCrossRefGoogle Scholar
  25. Lürling M (2003) The effect of substances from different zooplankton species and fish on the induction of defensive morphology in the green alga Scenedesmus obliquus. J Plankton Res 25:979–989CrossRefGoogle Scholar
  26. McGuiness KA (2002) Of rowing boats, ocean liners and tests of the ANOVA homogeneity of variance assumption. Austral Ecol 27:681–688CrossRefGoogle Scholar
  27. Pavia H, Toth GB (2000) Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum. Ecology 81:3212–3225Google Scholar
  28. Rosenberg R, Selander E (2000) Alarm signal response in the brittle star Amphiura filiformis. Mar Biol 136:43–48CrossRefGoogle Scholar
  29. Schnack SB (1981) The structure of the mouth parts of copepods in Kiel Bay Germany. Meeresforschung 29:89–101Google Scholar
  30. Schoeppner NM, Relyea RA (2005) Damage, digestion, and defence: the roles of alarm cues and kairomones for inducing prey defences. Ecol Lett 8:505–512CrossRefGoogle Scholar
  31. Selander E, Thor P, Toth GB, Pavia H (2006) Copepods induce paralytic shellfish toxin production in marine dinoflagellates. Proc R Soc Lond Ser B Biol Sci 273:1673–1680CrossRefGoogle Scholar
  32. Selander E, Cervin G, Pavia H (2008) The effect of nitrate and phosphate on grazer induced paralytic shellfish toxin formation in Alexandrium minutum. Limnol Oceanogr 53:523–530Google Scholar
  33. Tang KW (2003) Grazing and colony size development in Phaeocystis globosa (Prymnesiophyceae): the role of a chemical signal. J Plankton Res 25:831–842CrossRefGoogle Scholar
  34. Teegarden GJ (1999) Copepod grazing selection and particle discrimination on the basis of PSP toxin content. Mar Ecol Prog Ser 181:163–176CrossRefGoogle Scholar
  35. Tollrian R, Harvell CD (1999a) The ecology and evolution of inducible defences. Princeton University Press, PrincetonGoogle Scholar
  36. Tollrian R, Harvell CD (1999b) The evolution of inducible defenses: current ideas. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 306–321Google Scholar
  37. Toth GB, Noren F, Selander E, Pavia H (2004) Marine dinoflagellates show induced life-history shifts to escape parasite infection in response to water-borne signals. Proc R Soc Lond Ser B Biol Sci 271:733–738CrossRefGoogle Scholar
  38. Toth GB, Pavia H (2007) Induced herbivore resistance in seaweeds: a meta-analysis. J Ecol 95:425–434Google Scholar
  39. Traw MB, Dawson TE (2002) Differential induction of trichomes by three herbivores of black mustard. Oecologia 131:526–532CrossRefGoogle Scholar
  40. Van Donk E, Lürling M, Lampert W (1999) Consumer induced changes in phytoplankton: inducibility, costs, benefits, and the impact on grazers. In: Tollrian R, Harvell CD (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 89–103Google Scholar
  41. Yang Z, Kong FX, Shi XL, Cao HS (2006) Morphological response of Microcystis aeruginosa to grazing by different sorts of zooplankton. Hydrobiologia 563:225–230CrossRefGoogle Scholar
  42. Yasumoto K et al (2005) Aliphatic sulfates released from Daphnia induce morphological defense of phytoplankton: isolation and synthesis of kairomones. Tetrahedron Lett 46:4765–4767CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Johanna Bergkvist
    • 1
  • Erik Selander
    • 1
  • Henrik Pavia
    • 1
  1. 1.Department of Marine EcologyGöteborg University, Tjärnö Marine Biological LaboratoryStrömstadSweden

Personalised recommendations