Toxic dinoflagellates produce true grazer deterrents

Abstract

Many phytoplankton species produce toxic substances, but their functional role is unclear. Specifically, it remains uncertain whether these compounds have a toxic or deterrent effect on grazers; only, the latter is consistent with toxins as defensive tools. Here, we show that 10 of 12 species or strains of toxic dinoflagellates were consumed at lower rates than a similarly sized nontoxic dinoflagellate by a copepod. Through video observations of individual prey-grazer interactions, we further demonstrate that the dominating mechanism is through capture, examination, and subsequent rejection of vital cells, that is, a true deterrent effect that offers a straightforward explanation to its evolution. We argue that the diversity of grazer responses to toxic phytoplankton reported in the literature, including toxic effects, and the high diversity of toxin profiles between strains of the same phytoplankton species reflect different stages of an ever-ongoing evolutionary arms race, facilitated by rapid adaptation of grazers to toxic substances. We further argue that defensive toxicity requires a chemical signal exterior to the cell that informs the grazer about the toxicity of the cell. The signal can be the toxin itself or just an aposematic signal of toxicity. In the former case, allelochemical effects may emerge at high cell concentrations as a nonadaptive side effect of a predator defenses.

Trophic interactions, toxicokinetics, and detoxification processes in a domoic acid‐producing diatom and two copepod species

“…By contrast evidence of dinoflagellate toxins reveal that C. finmarchicus reduced grazing rates on toxic Alexandrium dinoflagellates and preferred a nontoxic diatom (Turriff et al ), and A. clausi and Oithona similis suffered reduced escape response and increased mortality after feeding on Alexandrium (Wohlrab et al ; Turner ). Xu and Kiørboe () demonstrated that several species or strains of toxic dinoflagellates were consumed at lower rates than nontoxic dinoflagellates by the copepod O. similis . For Pseudo‐nitzschia , it has recently been shown that long exposure time to a toxic diet might be the cause of mortality in the copepod A. tonsa (Lundholm et al ), and two Calanus species seemed to suffer reduced escape response after exposure to a toxic Pseudo‐nitzschia diet (Harðardóttir et al ).…”

On biological evolution and environmental solutions

“…Harmful algal blooms are characterised by an array of defense traits that are favored by natural selection. Some algae produce compounds that are toxic to grazers, such as the neurotoxins, saxitoxins and domoic acid produced by dinoflagellates, cyanobacteria, and diatoms, respectively (Pančić and Kiørboe, 2018;Xu and Kiørboe, 2018). Remarkably, toxin production varies widely both within and among populations.…”

Costs and benefits of toxin production in a dinoflagellate

“…The efficiency of the defence was not as high as that reported for other strains and species of Alexandrium spp. Thus, Xu & Kiørboe (2018) found that more than 90% of the cells of some toxic Alexandrium species/strains were rejected by a copepod, but also that other strains containing toxins were readably consumed by the copepod. Neither Xu et al (2017) nor Teegarden et al (2008) were consequently able to relate the efficiency of the defence to the composition and concentration of specific toxins in the cells of Alexandrium spp.…”

“…Dinoflagellates of the genus Alexandrium produce paralytic shellfish toxins (PSTs), intracellular secondary metabolites that may have defensive capabilities (Selander et al 2006;Xu & Kiørboe 2018). Indeed, toxicity as a defence mechanism against grazers is the favoured explanation for the evolution of algal toxins (Turner & Tester 1997;Smetacek 2001;Xu & Kiørboe 2018).…”