Chemical defense in the microplankton I: Feeding and growth rates of heterotrophic protists on the DMS‐producing phytoplankter Emiliania huxleyi

Abstract

In this study, the hypothesis that Emiliania huxleyi, a cosmopolitan, bloom‐forming coccolithophorid, produces chemical defenses against protist grazers was tested using four axenic strains of the alga. The putative chemical defense involves the cleavage of dimethylsulfoniopropionate (DMSP) by the enzyme DMSP lyase to yield dimethylsulfide (DMS) and acrylate. Out of six tested protist grazer species, five (including ciliates and heterotrophic dinoflagellates) showed lower feeding rates on E. huxleyi strains with high DMPS lyase activity than on low‐lyase strains. Reductions in population growth rate were consistent with feeding reductions. These results suggest that high levels of DMSP lyase activity somehow promote reduced palatability, although covariation of E. huxleyi protein and carbohydrate content with DMSP lyase activity meant that prey “nutritional quality” could not be ruled out as a contributing factor. Additional experiments with the heterotrophic dinoflagellate Amphidinium longum demonstrated that (1) individuals need not ingest E. huxleyi cells to receive the “don't eat me” cue and (2) exposure to high‐lyase E. huxleyi cells confers no harmful consequences in terms of the ability to feed and grow on alternate phytoplankton prey. Thus, factors promoting reduced grazing on high‐lyase E. huxleyi are hypothesized to constitute signals rather than acute toxins. Furthermore, although cell surface carbohydrates (as assayed by lectin binding) showed few differences among strains, results of feeding studies indicate that the deterrent signal resides on the cell surface or in the near‐cell dissolved phase. Behavior responses to such cues might play an important role in the outcome of encounters between protist grazers and their prey, with profound consequences for planktonic community structure.