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Predator-induced defence in a dinoflagellate generates benefits without direct costs

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  • 1.

    Llewellyn LE. Saxitoxin, a toxic marine natural product that targets a multitude of receptors. Nat Prod Rep. 2006;23:200–18.

    CAS  PubMed  Article  Google Scholar 

  • 2.

    Selander E, Thor P, Toth G, Pavia H. Copepods induce paralytic shellfish toxin production in marine dinoflagellates. Proc R Soc B. 2006;273:1673–80.

    CAS  PubMed  Article  Google Scholar 

  • 3.

    Turner JT, Tester PA. Toxic marine phytoplankton, zooplankton grazers, and pelagic food webs. Limnol Oceanogr. 1997;42:1203–13.

    Article  Google Scholar 

  • 4.

    Smetacek V. A watery arms race. Nature. 2001;441:745.

    Article  Google Scholar 

  • 5.

    Xu J, Kiørboe T. Toxic dinoflagellates produce true grazer deterrents. Ecology. 2018;99:2240–9.

    PubMed  Article  Google Scholar 

  • 6.

    Cusick KD, Widder EA. Bioluminescence and toxicity as driving factors in harmful algal blooms: ecological functions and genetic variability. Harmful Algae. 2020;98:101850.

    CAS  PubMed  Article  Google Scholar 

  • 7.

    Pančić M, Kiørboe T. Phytoplankton defence mechanisms: traits and trade-offs: defensive traits and trade-offs. Biol Rev. 2018;93:1269–303.

    PubMed  Article  Google Scholar 

  • 8.

    John EH, Flynn KJ. Growth dynamics and toxicity of Alexandrium fundyense (Dinophyceae): the effect of changing N:P supply ratios on internal toxin and nutrient levels. Eur J Phycol. 2000;35:11–23.

    Google Scholar 

  • 9.

    Selander E, Cervin G, Pavia H. Effects of nitrate and phosphate on grazer-induced toxin production in Alexandrium minutum. Limnol Oceanogr. 2008;53:523–30.

    CAS  Article  Google Scholar 

  • 10.

    Blossom HE, Markussen B, Daugbjerg N, Krock B, Norlin A, Hansen PJ. The cost of toxicity in microalgae: direct evidence from the dinoflagellate Alexandrium. Front Microbiol. 2019;10:1065.

    PubMed  PubMed Central  Article  Google Scholar 

  • 11.

    Brown ER, Kubanek J. Harmful alga trades off growth and toxicity in response to cues from dead phytoplankton. Limnol Oceanogr. 2020;65:1723–33.

  • 12.

    Windust AJ, Wright JLC, McLachlan JL. The effects of the diarrhetic shellfish poisoning toxins, okadaic acid and dinophysistoxin-1, on the growth of microalgae. Mar Biol. 1996;126:19–25.

    CAS  Article  Google Scholar 

  • 13.

    Legrand C, Rengefors K, Fistarol GO, Granéli E. Allelopathy in phytoplankton—biochemical, ecological and evolutionary aspects. Phycologia. 2003;42:406–19.

    Article  Google Scholar 

  • 14.

    John E, Flynn K. Modelling changes in paralytic shellfish toxin content of dinoflagellates in response to nitrogen and phosphorus supply. Mar Ecol Prog Ser. 2002;225:147–60.

    CAS  Article  Google Scholar 

  • 15.

    Lundholm N, Krock B, John U, Skov J, Cheng J, Pančić M, et al. Induction of domoic acid production in diatoms—types of grazers and diatoms are important. Harmful Algae. 2018;79:64–73.

    CAS  PubMed  Article  Google Scholar 

  • 16.

    Bergkvist J, Selander E, Pavia H. Induction of toxin production in dinoflagellates: the grazer makes a difference. Oecologia. 2008;156:147–54.

    PubMed  Article  Google Scholar 

  • 17.

    Griffin JE, Park G, Dam HG. Relative importance of nitrogen sources, algal alarm cues and grazer exposure to toxin production of the marine dinoflagellate Alexandrium catenella. Harmful Algae. 2019;84:181–7.

    CAS  PubMed  Article  Google Scholar 

  • 18.

    Selander E, Berglund EC, Engström P, Berggren F, Eklund J, Harðardóttir S, et al. Copepods drive large-scale trait-mediated effects in marine plankton. Sci Adv. 2019;5:eaat5096.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 19.

    Rhoades DF. Evolution of plant chemical defense against herbivores. Herbivores: their interaction with secondary plant metabolites. New York: Academic Press;1979. p 1–55.

  • 20.

    Karban R. The ecology and evolution of induced resistance against herbivores: induced resistance against herbivores. Funct Ecol. 2011;25:339–47.

    Article  Google Scholar 

  • 21.

    Strauss SY, Rudgers JA, Lau JA, Irwin RE. Direct and ecological costs of resistance to herbivory. TREE. 2002;17:278–85.

    Google Scholar 

  • 22.

    Agrawal AA. Current trends in the evolutionary ecology of plant defence. Funct Ecol. 2011;25:420–32.

    Article  Google Scholar 

  • 23.

    Pančić M, Torres RR, Almeda R, Kiørboe T. Silicified cell walls as a defensive trait in diatoms. Proc R Soc B. 2019;286:20190184.

    PubMed  Article  CAS  Google Scholar 

  • 24.

    Grønning J, Kiørboe T. Diatom defence: grazer induction and cost of shell‐thickening. Funct Ecol. 2020;34:1790–1801.

  • 25.

    Kiørboe T, Andersen KH. Nutrient affinity, half-saturation constants and the cost of toxin production in dinoflagellates. Ecol Lett. 2019;22:558–60.

    PubMed  Article  Google Scholar 

  • 26.

    Wang X, Wang Y, Ou L, He X, Chen D. Allocation costs associated with induced defense in Phaeocystis globosa (Prymnesiophyceae): the effects of nutrient availability. Sci Rep. 2015;5:10850.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 27.

    Zhu X, Wang J, Chen Q, Chen G, Huang Y, Yang Z. Costs and trade-offs of grazer-induced defenses in Scenedesmus under deficient resource. Sci Rep. 2016;6:22594.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • 28.

    Redfield AC. The biological control of chemical factors in the environment. Am Sci. 1958;46:205–21.

    CAS  Google Scholar 

  • 29.

    Boyer GL, Sullivan JJ, Andersen RJ, Harrison PJ, Taylor FJR. Effects of nutrient limitation on toxin production and composition in the marine dinoflagellate Protogonyaulax tamarensis. Mar Biol. 1987;96:123–8.

    CAS  Article  Google Scholar 

  • 30.

    Leong SCY, Murata A, Nagashima Y, Taguchi S. Variability in toxicity of the dinoflagellate Alexandrium tamarense in response to different nitrogen sources and concentrations. Toxicon. 2004;43:407–15.

    CAS  PubMed  Article  Google Scholar 

  • 31.

    Chakraborty S, Pančić M, Andersen KH, Kiørboe T. The cost of toxin production in phytoplankton: the case of PST producing dinoflagellates. ISME J. 2019;13:64–75.

    CAS  PubMed  Article  Google Scholar 

  • 32.

    Andersson L. Trends in nutrient and oxygen concentrations in the Skagerrak-Kattegat. J Sea Res. 1996;35:63–71.

    CAS  Article  Google Scholar 

  • 33.

    Tiselius P, Belgrano A, Andersson L, Lindahl O. Primary productivity in a coastal ecosystem: a trophic perspective on a long-term time series. J Plankton Res. 2016;38:1092–102.

    CAS  Article  Google Scholar 

  • 34.

    Kiørboe T, Nielsen TG. Regulation of zooplankton biomass and production in a temperate, coastal ecosystem. 1. Copepods. Limnol Oceanogr. 1994;39:493–507.

    Article  Google Scholar 

  • 35.

    Selander E, Kubanek J, Hamberg M, Andersson MX, Cervin G, Pavia H. Predator lipids induce paralytic shellfish toxins in bloom-forming algae. Proc Natl Acad Sci USA. 2015;112:6395–400.

    CAS  PubMed  Article  Google Scholar 

  • 36.

    Hansen PJ. The red tide dinoflagellate Alexandrium tamarense: effects on behaviour and growth of a tintinnid ciliate. Mar Ecol Prog Ser. 1989;53:105–16.

    Article  Google Scholar 

  • 37.

    Berdalet E, Peters F, Koumandou VL, Roldán C, Guadayol Ò, Estrada M. Species-specific physiological response of dinoflagellates to quantified small-scale turbulence 1. J Phycol. 2007;43:965–77.

    Article  Google Scholar 

  • 38.

    Fischer R, Andersen T, Hillebrand H, Ptacnik R. The exponentially fed batch culture as a reliable alternative to conventional chemostats. Limnol Oceanogr Meth. 2014;12:432–40.

    Article  Google Scholar 

  • 39.

    Flynn K, Jones KJ, Flynn KJ. Comparisons among species of Alexandrium (Dinophyceae) grown in nitrogen- or phosphorus-limiting batch culture. Mar Biol. 1996;126:9–18.

    CAS  Article  Google Scholar 

  • 40.

    Brandenburg KM, Wohlrab S, John U, Kremp A, Jerney J, Krock B, et al. Intraspecific trait variation and trade-offs within and across populations of a toxic dinoflagellate. Ecol Lett. 2018;21:1561–71.

    PubMed  Article  Google Scholar 

  • 41.

    Hillebrand H, Dürselen C-D, Kirschtel D, Pollingher U, Zohary T. Biovolume calculation for pelagic and benthic microalgae. J Phycol. 1999;35:403–24.

    Article  Google Scholar 

  • 42.

    Schnetger B, Lehners C. Determination of nitrate plus nitrite in small volume marine water samples using vanadium(III)chloride as a reduction agent. Mar Chem. 2014;160:91–8.

    CAS  Article  Google Scholar 

  • 43.

    Asp TN, Larsen S, Aune T. Analysis of PSP toxins in Norwegian mussels by a post-column derivatization HPLC method. Toxicon. 2004;43:319–27.

    CAS  PubMed  Article  Google Scholar 

  • 44.

    Turner A, Tölgyesi L. Determination of Paralytic Shellfish Toxins and Tetrodotoxin in Shellfish using HILIC/MS/MS. Application Note No. 5994-0967EN. [Internet]. 2019. Available from: https://www.agilent.com/en/solutions/food-testing-agriculture/seafood-testing.

  • 45.

    Franco JM, Fernández P, Reguera B. Toxin profiles of natural populations and cultures of Alexandrium minutum Halim from Galician (Spain) coastal waters. J Appl Phycol. 1994;6:275–9.

    CAS  Article  Google Scholar 

  • 46.

    Xu J, Hansen PJ, Nielsen LT, Krock B, Tillmann U, Kiørboe T. Distinctly different behavioral responses of a copepod, Temora longicornis, to different strains of toxic dinoflagellates, Alexandrium spp. Harmful Algae. 2017;62:1–9.

    PubMed  Article  Google Scholar 

  • 47.

    Wood S, Scheipl F. gamm4: Generalized additive mixed models using mgcv and lme4. R package version 0.2-6. [Internet]. 2020. Available from: https://cran.r-project.org/.

  • 48.

    Kuznetsova A, Brockhoff PB, Christensen RHB. lmerTest package: tests in linear mixed effects models. J Stat Soft 2017;82:1–26.

  • 49.

    Wohlrab S, Selander E, John U. Predator cues reduce intraspecific trait variability in a marine dinoflagellate. BMC Ecol. 2017;17:8.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • 50.

    Driscoll WW, Hackett JD, Ferrière R. Eco-evolutionary feedbacks between private and public goods: evidence from toxic algal blooms. Ecol Lett. 2016;19:81–97.

    PubMed  Article  Google Scholar 

  • 51.

    Flynn K, Franco J, Fernandez P, Reguera B, Zapata M, Wood G, et al. Changes in toxin content, biomass and pigments of the dinoflagellate Alexandrium minutum during nitrogen refeeding and growth into nitrogen or phosphorus stress. Mar Ecol Prog Ser. 1994;111:99–109.

    CAS  Article  Google Scholar 

  • 52.

    Tillmann U, John U. Toxic effects of Alexandrium spp. on heterotrophic dinoflagellates: an allelochemical defence mechanism independent of PSP-toxin content. Mar Ecol Prog Ser. 2002;230:47–58.

    CAS  Article  Google Scholar 

  • 53.

    Tillmann U, Hansen PJ. Allelopathic effects of Alexandrium tamarense on other algae: evidence from mixed growth experiments. Aquat Micro Ecol. 2009;57:101–12.

    Article  Google Scholar 

  • 54.

    Teegarden GJ, Campbell RG, Anson DT, Ouellett A, Westman BA, Durbin EG. Copepod feeding response to varying Alexandrium spp. cellular toxicity and cell concentration among natural plankton samples. Harmful Algae. 2008;7:33–44.

    Article  Google Scholar 

  • 55.

    Peter KH, Sommer U. Interactive effect of warming, nitrogen and phosphorus limitation on phytoplankton cell size. Ecol Evol. 2015;5:1011–24.

    PubMed  PubMed Central  Article  Google Scholar 

  • 56.

    Garcia NS, Bonachela JA, Martiny AC. Interactions between growth-dependent changes in cell size, nutrient supply and cellular elemental stoichiometry of marine. Synechococcus ISME J. 2016;10:2715–24.

    CAS  PubMed  Article  Google Scholar 

  • 57.

    Kiørboe T. Turbulence, phytoplankton cell size, and the structure of pelagic food webs. Adv Mar Biol. 1993;29:1–72.

    Article  Google Scholar 

  • 58.

    Lindemann C, Fiksen Ø, Andersen KH, Aksnes DL. Scaling laws in phytoplankton nutrient uptake affinity. Front Microbiol. 2016;3:1–6.

    Google Scholar 

  • 59.

    Edwards KF, Thomas MK, Klausmeier CA, Litchman E. Allometric scaling and taxonomic variation in nutrient utilization traits and maximum growth rate of phytoplankton. Limnol Oceanogr. 2012;57:554–66.

    Article  Google Scholar 

  • 60.

    Lürling M, Van Donk E. Grazer-induced colony formation in Scenedesmus: are there costs to being colonial? Oikos. 2000;88:111–8.

    Article  Google Scholar 

  • 61.

    Selander E, Jakobsen HH, Lombard F, Kiorboe T. Grazer cues induce stealth behavior in marine dinoflagellates. Proc Natl Acad Sci USA. 2011;108:4030–4.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 62.

    Kiørboe T. A mechanistic approach to plankton ecology. Princeton, NJ: Princeton University Press; 2008. pp. 128–129.

  • 63.

    Tollrian R, Harvell CD. The ecology and evolution of inducible defenses. Princeton, NJ: Princeton University Press; 1999. pp. 1–383.

  • 64.

    Leao T, Castelão G, Korobeynikov A, Monroe EA, Podell S, Glukhov E, et al. Comparative genomics uncovers the prolific and distinctive metabolic potential of the cyanobacterial genus Moorea. Proc Natl Acad Sci USA. 2017;114:3198–203.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • 65.

    Züst T, Agrawal AA. Trade-Offs Between Plant Growth and Defense Against Insect Herbivory: An Emerging Mechanistic Synthesis. Annu Rev Plant Biol. 2017;68:513–34.

    PubMed  Article  CAS  PubMed Central  Google Scholar 


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