Copepods induce paralytic shellfish toxin production in marine dinoflagellates

Abstract

Among the thousands of unicellular phytoplankton species described in the sea, some frequently occurring and bloom-forming marine dinoflagellates are known to produce the potent neurotoxins causing paralytic shellfish poisoning. The natural function of these toxins is not clear, although they have been hypothesized to act as a chemical defence towards grazers. Here, we show that waterborne cues from the copepod Acartia tonsa induce paralytic shellfish toxin (PST) production in the harmful algal bloom-forming dinoflagellate Alexandrium minutum. Induced A. minutum contained up to 2.5 times more toxins than controls and was more resistant to further copepod grazing. Ingestion of non-toxic alternative prey was not affected by the presence of induced A. minutum. The ability of A. minutum to sense and respond to the presence of grazers by increased PST production and increased resistance to grazing may facilitate the formation of harmful algal blooms in the sea.

Figure 1

Paralytic shellfish toxin (GTX 1, 2 and 4) content (fmol cell⁻¹) in A. minutum that received waterborne cues from different treatments (control, starving copepods, grazing copepods) outside cages in the induction experiment. The GTX 3 content was close to the detection limit in all treatments and is not visible in the figure. Letters above bars indicate significant differences in total PST content among treatments based on the SNK multiple comparisons test (p<0.05). Error bars show +s.e.m. (n=4).

Figure 2

Net growth rate, μ, (d⁻¹) of A. minutum cells (a) exposed to the different treatments (control, starving copepods, grazing copepods) inside cages and (b) that received waterborne cues from the different treatments outside cages. Letters above bars indicate significant differences among treatments based on the SNK multiple comparisons test (p<0.05). Error bars show +s.e.m. (n=4).

Figure 3

Cell specific content of GTX 1, 2 and 4 (fmol cell⁻¹) in A. minutum exposed to direct grazing from the different densities of A. tonsa indicated by the category axis. Letters above bars indicate significant differences among treatments based on the SNK multiple comparisons test (p<0.05). Error bars show +s.e.m. (n=3).

Figure 4

Ingestion of algae (cells copepod⁻¹ h⁻¹) by the copepod A. tonsa offered a simultaneous choice between either control A. minutum and P. micans (black bars) or induced A. minutum and P. micans (white bars) in the feeding preference experiment. Error bars show +s.e.m. (n=12). (NB, the statistical analysis was performed on the proportion of ingested control and induced A. minutum in relation to the ingested P. micans and not on the absolute ingestion of different prey item.)