Cues and consequences: Copepodamides as mediators of defence induction in marine phytoplankton

Abstract

Marine phytoplankton account for less than one percent of Earth’s primary-producer biomass, yet they sustain almost half of global primary production. These unicellular organisms face more intense predation pressure than terrestrial plants, primarily from microzooplankton but also from copepods, which are among the most abundant animals on Earth. Consequently, phytoplankton have evolved a suite of defence traits to reduce grazing losses. Because plankton generally lack complex visual and auditory senses, they rely mainly on chemical and hydromechanical signals and cues in their environment to navigate the main Darwinian missions of life. Marine copepods exude a group of polar lipids, copepodamides, that have been co-opted by taxonomically diverse prey organisms, mainly diatoms and dinoflagellates, to act as general alarm cues that copepods are nearby. This leads prey to induce morphological, behavioural, and biochemical defences that help them evade and reduce predation. Examples of these defence traits include colony-size reduction, which lowers encounter rates with predators, and elevated toxin production or bioluminescence, which increase rejection by copepods and redirects grazing towards less-defended prey.

This thesis investigates how widespread copepodamides are among copepods, which organisms can detect and respond to them, and the consequences of those responses at individual, population, and ecosystem levels. Analysing individual copepods and bulk zooplankton samples, I show for the first time that freshwater copepods contain copepodamides in amounts comparable to marine copepods, that the composition differs markedly between the two groups, and that freshwater copepods putatively possess four unique copepodamide congeners. By using purified copepodamides to simulate copepod presence in controlled exposure experiments I corroborate previous evidence that the commonly occurring chain-forming diatom Skeletonema marinoi reduces chain length in response to copepodamides, that three species not previously tested do not respond similarly, and that chain-suppression should thus not be assumed to be a general anti-copepod defence strategy. I also expand the catalogue of dinoflagellate species associated with harmful algal blooms (HABs) that respond to copepodamides: Gymnodinium catenatum, Alexandrium catenella, and Dinophysis sacculus increase phycotoxin production, while Alexandrium catenella and Protoceratium reticulatum increase bioluminescence intensity. Cue-mediated induction of such traits, combined with selective grazing by copepods on less-defended cells, may facilitate HAB-formation and should be incorporated into conceptual models of HAB drivers and HAB forecasting efforts.

Finally, research into the drivers of phycotoxin induction in marine HAB species has long been focused on bottom-up, nutrient availability effects. Accumulating evidence over the last 25 years, however, shows that top-down grazer-induced effects are also important. However, bottom-up and top-down drivers have rarely been directly compared in primary studies. Using a meta-analytical framework, I synthesise and statistically compare published experimental studies on toxin induction caused by relative nitrogen enrichment (nitrogen enrichment or phosphorus limitation) or by exposure to grazers or their chemical cues for the two most-studied marine HAB genera, Alexandrium and Pseudo-nitzschia. I find that grazer-induced increases in phycotoxins rival—and may even exceed—nutrient-driven effects. I discuss these findings in the context of well-developed frameworks of plant-defences in terrestrial plants, and suggest a path towards adopting a unified framework.

Copepodamides constitute a powerful experimental tool: by simulating grazer presence without direct predation, we can isolate non-consumptive inducible defences and test their mechanisms under controlled, repeatable conditions. The use of copepodamides is improving our understanding of phytoplankton–zooplankton interactions and offers new leverage to test broader ideas in predator–prey ecology and the evolution of anti-grazer defences. The detection of copepodamides in freshwater copepods, in particular, opens an exciting new research frontier that warrants thorough investigation.