Fear of grazing rivals the toxin induction effect of nitrogen enrichment in marine harmful algae— a meta-analysis

One of the major subfields of chemical ecology is the study of toxins and how they mediate interactions between organisms. Toxins produced by harmful algae, phycotoxins, impact a wide variety of organisms connected to the marine food web. Significant research efforts have thus aimed to identify the ecological and evolutionary drivers behind harmful algal blooms (HABs) to facilitate their forecasting, mitigation, and management. Nutrient availability is a key factor controlling growth and toxin production. Additionally, recent evidence has shown that harmful algae can sense the presence of zooplankton grazers, primarily copepods, and respond by dramatically increasing toxin production. Phycotoxin production is consequently controlled by a combination of bottom-up and top-down drivers, but the relative importance of the two is not understood. Here we conducted a meta-analysis of 113 control-treatment contrasts from 37 peer-reviewed experimental studies, comparing the effects of relative nitrogen enrichment (increased nitrogen:phosphorus ratio) and elevated grazing risk on phycotoxin induction in the two most studied marine HAB-forming genera, Alexandrium dinoflagellates and Pseudo-nitzschia diatoms. We show that phycotoxins are induced in response to both nitrogen enrichment and elevated grazing risk. Although both genera responded similarly to nitrogen enrichment, Pseudo-nitzschi a toxins increased four times more in response to grazers than to nitrogen enrichment, and ten times more than Alexandrium toxins did in response to grazers. Grazing risk thus appears to rival, perhaps even supersede, the well-established phycotoxin-inducing effect of nitrogen enrichment in marine harmful algae. Although this analysis is limited to the two most studied marine HAB genera, we conclude that future attempts to understand the evolution and variable production of phycotoxins require integration of bottom-up nutrient availability and top-down selective pressures to fully elucidate phycotoxin dynamics in marine HAB-forming species.