Fear of predation may influence food webs more than actual predation. However, the mechanisms and magnitude of nonconsumptive predator effects are largely unknown in unicellular-dominated food webs such as marine plankton. We report a general mechanism of chemically induced predator effects in marine plankton. Copepods, the most abundant zooplankton in the oceans, imprint seawater with unique polar lipids—copepodamides—which trigger toxin production and bioluminescence in harmful dinoflagellates. We show that copepodamides also elicit defensive traits in other phytoplankton, inducing the harmful algal bloom-forming diatom Pseudo-nitzschia seriata to produce 10 times more toxins, and colony-forming diatoms to decrease colony size by half. A 1-year study in the northeast Atlantic revealed that natural copepodamide concentrations are high enough to induce harmful algal toxins and size reduction in dominant primary producers when copepods are abundant. We conclude that copepodamides will structure marine plankton toward smaller, more defended life forms on basin-wide scales.

Diatoms of the genus Pseudo-nitzschia produce domoic acid (DA), a toxin that is vectored in the marine food web, thus causing serious problems for marine organisms and humans. In spite of this, knowledge of interactions between grazing zooplankton and diatoms is restricted. In this study, we examined the interactions between Calanus copepodites and toxin producing Pseudo-nitzschia. The copepodites were fed with different concentrations of toxic P. seriata and a strain of P. obtusa that previously was tested to be non-toxic. The ingestion rates did not differ among the diets (P. seriata, P. obtusa, a mixture of both species), and they accumulated 6%–16% of ingested DA (up to 420 µg per dry weight copepodite). When P. seriata was exposed to the copepodites, either through physical contact with the grazers or separated by a membrane, the toxicity of P. seriata increased (up to 3300%) suggesting the response to be chemically mediated. The induced response was also triggered when copepodites grazed on another diatom, supporting the hypothesis that the cues originate from the copepodite. Neither pH nor nutrient concentrations explained the induced DA production. Unexpectedly, P. obtusa also produced DA when exposed to grazing copepodites, thus representing the second reported toxic polar diatom.

A major cause of phytoplankton mortality is predation by zooplankton. Strategies to avoid grazers have probably played a major role in the evolution of phytoplankton and impacted bloom dynamics and trophic energy transport. Certain species of the genus Pseudo-nitzschia produce the neurotoxin, domoic acid (DA), as a response to the presence of copepod grazers, suggesting that DA is a defense compound. The biosynthesis of DA comprises fusion of two precursors, a C10 isoprenoid geranyl pyrophosphate and l-glutamate. Geranyl pyrophosphate (GPP) may derive from the mevalonate isoprenoid (MEV) pathway in the cytosol or from the methyl-erythritol phosphate (MEP) pathway in the plastid. l-glutamate is suggested to derive from the citric acid cycle. Fragilariopsis, a phylogenetically related but nontoxic genus of diatoms, does not appear to possess a similar defense mechanism. We acquired information on genes involved in biosynthesis, precursor pathways and regulatory functions for DA production in the toxigenic Pseudo-nitzschia seriata, as well as genes involved in responses to grazers to resolve common responses for defense strategies in diatoms. Several genes are expressed in cells of Pseudo-nitzschia when these are exposed to predator cues. No genes are expressed in Fragilariopsis when treated similarly, indicating that the two taxa have evolved different strategies to avoid predation. Genes involved in signal transduction indicate that Pseudo-nitzschia cells receive signals from copepods that transduce cascading molecular precursors leading to the formation of DA. Five out of seven genes in the MEP pathway for synthesis of GPP are upregulated, but none in the conventional MEV pathway. Five genes with known or suggested functions in later steps of DA formation are upregulated. We conclude that no gene regulation supports that l-glutamate derives from the citric acid cycle, and we suggest the proline metabolism to be a downstream precursor. Pseudo-nitzschia cells, but not Fragilariopsis, receive and respond to copepod cues. The cellular route for the C10 isoprenoid product for biosynthesis of DA arises from the MEP metabolic pathway and we suggest proline metabolism to be a downstream precursor for l-glutamate. We suggest 13 genes with unknown function to be involved in diatom responses to grazers.

Marine zooplankton release chemical cues, which trigger defenses in unicellular phytoplankton, such as increased toxin production and changes of colony sizes. Here, we identify the structure of two novel alarm cues belonging to the group of copepodamides. Similar to the known copepodamides, one of the compounds described is shown to trigger both amnesic and paralytic shellfish toxin production and chain length shortening in Skeletonema marinoi. In addition, we report the putative structures of another 21 copepodamides, which constitute 28% of the total copepodamides extractable from whole animals, suggesting that the copepodamide concentrations have been underestimated in earlier studies. We introduce a structure‐based nomenclature to handle the increasing number of copepodamides. Analysis of 12 copepod species showed that marine calanoid and freshwater cyclopoid copepods contain copepodamides. The only harpacticoid included in the analysis, Tigriopus californicus, did not appear to produce detectable amounts of copepodamides. Feeding experiments revealed that copepodamide compositions depend on both diet and species‐specific properties. Copepodamides induce both morphological and biochemical defensive traits in phytoplankton and may drive large‐scale trait–mediated effects in marine food webs. The more comprehensive list of copepodamides reported here makes it possible to explore the role of the copepodamide signaling system in the pelagic ecosystem in greater detail.