Chemical cues induce consumer-specific defenses in a bloom-forming marine phytoplankton

Abstract

Blooms of the phytoplankton Phaeocystis can comprise 85% of total production and generate major biogeochemical signals across broad oceanic regions. The success of Phaeocystis may result from its ability to change size by many orders of magnitude when it shifts from small cells of 4-6 microm to large colonies of up to 30,000 microm in diameter. Single cells are consumed by ciliates but not copepods, whereas colonies are consumed by copepods but not ciliates. We demonstrate that chemical cues associated with each of these grazers induce consumer-specific, but opposing, morphological transformations in the bloom-forming species Phaeocystis globosa. Chemical cues from grazing copepods suppress colony formation by a significant 60-90%, a response that should be adaptive because copepods feed four times more on colonies versus solitary cells. In contrast, chemical cues from grazing ciliates enhance colony formation by >25%, a response that should be adaptive because ciliates grow three times faster when fed solitary cells versus colonies. Because size-selective predation fundamentally alters community structure and ecosystem function, this chemically cued shift may redirect energy and nutrients from food webs supporting fisheries to those fueling detrital pathways, thus potentially altering ecosystem-level processes such as productivity, carbon storage, and nutrient release.

Fig. 1.

Percentage of total P. globosa cells within colonies after incubations with chemical cues from grazer-free (open bars) or grazer-containing P. globosa cultures (filled bars). Grazers were either a natural mixture of mesozooplankton (collected in plankton tows in coastal Georgia) (a), the copepod A. tonsa alone (b), or the ciliate Euplotes sp. alone (c). P values designate differences between treatments (ANOVA). Values are means ± 1 SEM.

Fig. 2.

Feeding and performance of grazers on P. globosa solitary cells (open bars) or colonies (filled bars). (a) Fecal pellet production of A. tonsa. (b) Euplotes sp. growth rates. P values designate differences between treatments (ANOVA). Values are means ± 1 SEM.

Fig. 3.

Effects of filtrates from P. globosa cultures with increasing A. tonsa densities on P. globosa. (a) Percentage of total cells within colonies. (b) Colony concentration. (c) Total cell concentration. The shaded region of the graph represents copepod densities far above natural maximal densities. Density-dependent effects on colony formation were analyzed with a curvilinear regression fitted to an exponential decay curve. Percentages were arcsine-transformed before analysis, and reported equations are those using the transformed data. Values are means ± 1 SEM.

Fig. 4.

Effects of organic or aqueous fractions of filtrates on P. globosa colony concentration (a and c) and percentage of total cells within colonies (b and d). Filtrates sources were either P. globosa cultures (open bars) or P. globosa cultures with A. tonsa (filled bars). P values designate differences between filtrate source (ANOVA). Values are means ± 1 SEM.