Abstract
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.
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References
Asp TN, Larsen S, Aune T (2004) Analysis of PSP toxins in Norwegian mussels by a post-column derivatization HPLC method. Toxicon 43:319–327
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):11–75
Borell EM, Foggo A, Coleman RA (2004) Induced resistance in intertidal macroalgae modifies feeding behaviour of herbivorous snails. Oecologia 140:328–334
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 23:319–331
Chivers DP, Smith RJF (1998) Chemical alarm signalling in aquatic predator–prey systems: a review and prospectus. Ecoscience 5:338–352
Colin SP, Dam HG (2002) Testing for toxic effects of prey on zooplankton using sole versus mixed diets. Limnol Oceanogr 47:1430–1437
Cronin G, Hay ME (1996) Induction of seaweed chemical defenses by amphipod grazing. Ecology 77:2287–2301
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 6:275–279
Frost BW (1989) A taxonomy of the marine calanoid copepod genus Pseudocalanus. Can J Zool 67:525–551
Green TR, Ryan CA (1972) Wound-induced proteinase inhibitorin plant leaves: a possible defense mechanism against insects. Science 175:776–777
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 225:169–176
Ha K, Jang MH, Takamura N (2004) Colony formation in planktonic algae induced by zooplankton culture media filtrate. J Freshwater Ecol 19:9–16
Halsband C, Hirche HJ (2001) Reproductive cycles of dominant calanoid copepods in the North Sea. Mar Ecol Prog Ser 209:219–229
Hessen DO, Van Donk E (1993) Morphological-changes in Scenedesmus induced by substances released from Daphnia. Arch Hydrobiol 127:129–140
Hillebrand H, Durselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424
Iyengar EV, Harvell CD (2002) Specificity of cues inducing defensive spines in the bryozoan Membranipora membranacea. Mar Ecol Prog Ser 225:205–218
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 27:261–273
Jang MH, Ha K, Joo GJ, Takamura N (2003) Toxin production of cyanobacteria is increased by exposure to zooplankton. Freshwater Biol 48:1540–1550
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 225:147–160
Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago
Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394
Leftley JW, Keller DK, Selvin RC, Claus W, Guillard RRL (1987) Media for the culture of oceanic ultraphytoplankton. J Phycol 23:633–638
Lilly EL, Halanych KM, Anderson DM (2005) Phylogeny, biogeography, and species boundaries within the Alexandrium minutum group. Harmful Algae 4:1004–1020
Long JD, Smalley GW, Barsby T, Anderson JT, Hay ME (2007) Chemical cues induce consumer-specific defenses in a bloom-forming marine phytoplankton. PNAS 104:10512–10517
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 25:979–989
McGuiness KA (2002) Of rowing boats, ocean liners and tests of the ANOVA homogeneity of variance assumption. Austral Ecol 27:681–688
Pavia H, Toth GB (2000) Inducible chemical resistance to herbivory in the brown seaweed Ascophyllum nodosum. Ecology 81:3212–3225
Rosenberg R, Selander E (2000) Alarm signal response in the brittle star Amphiura filiformis. Mar Biol 136:43–48
Schnack SB (1981) The structure of the mouth parts of copepods in Kiel Bay Germany. Meeresforschung 29:89–101
Schoeppner NM, Relyea RA (2005) Damage, digestion, and defence: the roles of alarm cues and kairomones for inducing prey defences. Ecol Lett 8:505–512
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 273:1673–1680
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 53:523–530
Tang KW (2003) Grazing and colony size development in Phaeocystis globosa (Prymnesiophyceae): the role of a chemical signal. J Plankton Res 25:831–842
Teegarden GJ (1999) Copepod grazing selection and particle discrimination on the basis of PSP toxin content. Mar Ecol Prog Ser 181:163–176
Tollrian R, Harvell CD (1999a) The ecology and evolution of inducible defences. Princeton University Press, Princeton
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 306–321
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 271:733–738
Toth GB, Pavia H (2007) Induced herbivore resistance in seaweeds: a meta-analysis. J Ecol 95:425–434
Traw MB, Dawson TE (2002) Differential induction of trichomes by three herbivores of black mustard. Oecologia 131:526–532
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 89–103
Yang Z, Kong FX, Shi XL, Cao HS (2006) Morphological response of Microcystis aeruginosa to grazing by different sorts of zooplankton. Hydrobiologia 563:225–230
Yasumoto K et al (2005) Aliphatic sulfates released from Daphnia induce morphological defense of phytoplankton: isolation and synthesis of kairomones. Tetrahedron Lett 46:4765–4767
Acknowledgements
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.
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Communicated by Dag Olav Hessen.
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Bergkvist, J., Selander, E. & Pavia, H. Induction of toxin production in dinoflagellates: the grazer makes a difference. Oecologia 156, 147–154 (2008). https://doi.org/10.1007/s00442-008-0981-6
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DOI: https://doi.org/10.1007/s00442-008-0981-6