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Colony formation in marine phytoplankton can be modified by the presence of grazers, but the effect of colony size and shape on the feeding behavior of grazers is still relatively unknown. To explore the defensive role of colony formation, we examined the feeding response of three differently sized grazers (copepodites, copepod nauplii, and two heterotrophic dinoflagellates) feeding on colony-forming phytoplankton, using both direct video observations and bottle incubations. We found a dramatic increase in capture clearance rate with colony size for copepodites, up to 140% higher in the largest diatom chains relative to their solitary cells. This was in part facilitated by a mechanism – described here for the first time – by which copepods efficiently detect and capture colonies using the antennules, thereby increasing their capture radius. Prey handling time by copepodites increased with colony size, but did not limit prey ingestion. Larger chains of diatoms were efficiently handled and consumed by the copepodites, whereas larger spherical colonies of Phaeocystis globosa were rejected subsequent to capture. In contrast, colonial phytoplankton were better protected against the microzooplankton and copepod nauplii examined, since these only managed to consume smaller colonies equivalent of a few cells. We find that the defensive value of colony formation depends on the size and foraging behavior of the grazer and the size and shape of the colony. Thus, the defensive benefit is therefore a function of the composition of the grazer community. We argue that bloom formation in chain-forming diatoms is facilitated by the efficient protection against rapidly responding micro-grazers and the lagged numerical response of efficient copepod grazers.
The diatom frustule provides partial protection against copepod grazing. Whether the defense is due to the cells being de‐selected or handled for so long that the grazers lose time for foraging is unknown. The mechanism has implications for the population dynamics of both defended and co‐occurring, undefended nutrient competitors. We use video‐observations to demonstrate that thick‐shelled diatoms captured by the copepod Temora longicornis were rejected more frequently than thin‐shelled diatoms, irrespective of cell size. The thick‐shelled cells of the larger diatoms were handled for much longer, and the time spent handling these limits the consumption of phytoplankton. This may be why many diatoms, even in the presence of dense grazer populations, reach bloom concentrations, and thus, facilitate aggregation and mass sedimentation. This has implications for both carbon sequestration and for securing a large population of cells at depth ready to colonize the pelagic, when growth conditions again become favorable.
Phytoplankton employ a variety of defence mechanisms against predation, including production of toxins. Domoic acid (DA) production by the diatom Pseudo-nitzschia spp. is induced by the presence of predators and is considered to provide defence benefits, but the evidence is circumstantial. We exposed eight different strains of P. seriata to chemical cues from copepods and examined the costs and the benefits of toxin production. The magnitude of the induced toxin response was highly variable among strains, while the costs in terms of growth reduction per DA cell quota were similar and the trade-off thus consistent. We found two components of the defence in induced cells: (i) a ‘private good’ in terms of elevated rejection of captured cells and (ii) a ‘public good’ facilitated by a reduction in copepod feeding activity. Induced cells were more frequently rejected by copepods and rejections were directly correlated with DA cell quota and independent of access to other food items. By contrast, the public-good effect was diminished by the presence of alternative prey suggesting that it does not play a major role in bloom formation and that its evolution is closely associated with the grazing-deterrent private good.
Phytoplankton induce defensive traits in response to chemical alarm signals from grazing zooplankton. However, these signals are potentially vulnerable to changes in pH and it is not yet known how predator recognition may be affected by ocean acidification. We exposed four species of diatoms and one toxic dinoflagellate to future pCO2 levels, projected by the turn of the century, in factorial combinations with predatory cues from copepods (copepodamides). We measured the change in growth, chain length, silica content, and toxin content. Effects of increased pCO2 were highly species specific. The induction of defensive traits was accompanied by a significant reduction in growth rate in three out of five species. The reduction averaged 39% and we interpret this as an allocation cost associated with defensive traits. Copepodamides induced significant chain length reduction in three of the four diatom species. Under elevated pCO2Skeletonema marinoi reduced silica content by 30% and in Alexandrium minutum the toxin content was reduced by 30%. Using copepodamides to induce defensive traits in the absence of direct grazing provides a straightforward methodology to assess costs of defense in microplankton. We conclude that copepodamide signalling system is likely robust to ocean acidification. Moreover, the variable responses of different taxa to ocean acidification suggest that there will be winners and losers in a high pCO2 world, and that ocean acidification may have structuring effects on phytoplankton communities.
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