Grazers and phytoplankton growth in the oceans: an experimental and evolutionary perspective

Background: Phytoplankton responsible for primary production on continental shelves have changed through Earth history. Any understanding of the evolutionary history is complicated by the fact that both the physical and biological components of marine environments have changed through time as well. We carried out experiments in which diverse phytoplankton species were grown in a series of treatments that differed with respect to the presence or absence of grazers as well as seawater chemistry. Results: The presence of grazers altered phytoplankton growth and composition. Some responses were independent of whether the grazer was a protist (Euplotes sp.) or a microarthropod (Acartia tonsa), while some were grazer-specific. Sulfate availability often affected the extent of phytoplankton responses. In the presence of grazers, the green alga Tetraselmis suecica and the diatom Thalassiosira weissflogii enriched their organic composition and had unaltered or higher C:P and N:P ratios; organic composition was unaffected in the cyanobacterium Synechococcus sp. In Tetraselmis and Thalassiosira, the presence of grazers depressed non-photochemical quenching of variable fluorescence at PSII; the opposite was true for Synechococcus. The green alga and the diatom also grew faster in the presence of the ciliate, but the cyanobacterium Synechococcus sp. showed reduced growth or no effect when Euplotes was present. Synechococcus (especially) and Thalassiosira produced toxins effective against the copepod, but ciliate growth was unaffected. Acartia induced a 4-6 fold increase of Si cell quota in the diatom, but Euplotes had no similar effect. Conclusions: The differential growth responses of the eukaryotic algae and cyanobacteria to ciliate grazing may help to explain the apparently coeval radiation of eukaryophagic protists and the rise of eukaryotes to ecological prominence as primary producers in Neoproterozoic oceans. The experimental results suggest that phytoplankton responses to the later radiation of microarthropod grazers were clade-specific, and included changes in growth dynamics, toxin synthesis, encystment, and (in diatoms) enhanced Si uptake.