Influence of predator-prey evolutionary history, chemical alarm-cues, and feeding selection on induction of toxin production in a marine dinoflagellate

Abstract

The dinoflagellate, Alexandrium fundyense, produces paralytic shellfish toxins and co‐occurs with populations of the copepod, Acartia hudsonica, from Maine, but not New Jersey. The hypothesis that history of co‐occurrence between predator and prey effects the ability of prey to recognize and respond to predators with increased toxin production was tested for this copepod‐alga interaction. When A. fundyense was exposed to waterborne cues released by copepods from Maine (indirect exposure) that were either starved or fed toxic cells, cell toxin quota increased by 35% compared to unexposed controls. The induced response was significantly less for cells exposed to waterborne cues of copepods from New Jersey, and induction (20%) was only elicited by this population when fed toxic cells. These results suggest that A. fundyense responded to a kairomone from copepods from Maine, but required a feeding cue from copepods from New Jersey. An increase of approximately 300% in cell toxin quota, however, occurred when cells were directly exposed to grazing, and was independent of copepod population. Evolutionary history, therefore, had no apparent effect when induction was underlain by feeding cues. In assays with a mixture of toxic and nontoxic cells, selection for the latter was evident, and also independent of copepod population. Selectivity for nontoxic cells, however, could not account for changes in cell toxin content in the mixture experiments. When A. fundyense was exposed to extracts of toxic or nontoxic Alexandrium, toxin production increased significantly (23%), suggesting modest induction by an alga‐to‐alga alarm signal.

A multi-phylum study of grazer-induced paralytic shellfish toxin production in the dinoflagellate Alexandrium fundyense: A new perspective on control of algal toxicity

“…Also included in this comparison were data of indirectly enhanced toxin production previously reported (Senft-Batoh et al, 2015) for populations of the copepod, Acartia hudsonica, from Maine (fed and starved) and New Jersey (fed). Differences in percent enhancement among the treatments were significant (p < 0.0001), and differences among the mean values of treatments are shown in Fig.…”

“…During this time, the copepods were starved to ensure complete gut evacuation prior to assays (Dam and Peterson, 1988). Results of induction assays involving two populations (Maine and New Jersey) of the copepod Acartia hudsonica, were obtained previously (Senft-Batoh et al, 2015), and have been reanalyzed with the present results. The A. hudsonica were reared and prepared for experiments in similar conditions to those of Eurytemora herdmani.…”

“…Incubation conditions of treatments and controls were 18 8C under a 12 h:12 h light-dark photoperiod. To circumvent any nutrient-dependent effects upon toxin content of dinoflagellate cells, all treatments and controls were conducted in nutrientreplete, F/4 medium (Guillard, 1975) (F/2 medium was used for previously conducted assays with Acartia hudsonica [Senft-Batoh et al, 2015] reanalyzed with the present results). During incubation, cages were lifted, gently, twice a day (12 h apart) to ensure exchange of cues between compartments.…”

“…It has already been demonstrated that grazing activities of copepods increase production of PST in the dinoflagellate genus Alexandrium (Selander et al, 2006(Selander et al, , 2012Senft-Batoh et al, 2015). Because induced toxin production is purported to defend prey, an induced response to all grazers may be expected.…”

“…The grazer species represent the phyla Dinoflagellata and Ciliophora (protists), Mollusca, Chordata (ascidians), and Arthropoda. Induced PST production was previously measured when A. fundyense was exposed to two populations of the copepod Acartia hudsonica (Senft-Batoh et al, 2015) and those results are also assessed with the present study.…”