Grazer-induced bioluminescence gives dinoflagellates a competitive edge.

Bioluminescent dinoflagellates grow at one third the rate of their competitors of equivalent size, such as diatoms [1]. Despite this disadvantage, dinoflagellates successfully persist within phytoplankton communities and even form large blooms during favourable conditions. One explanation for this paradox is that bioluminescence acts as a defence that reduces losses to zooplankton grazers, such as copepods [2,3]. Lindström et al.[4] found that the dinoflagellate Lingulodinium polyedra (F.Stein) J.D.Dodge increase their bioluminescence in response to copepodamides [5], polar lipids exuded by copepod grazers, allowing for a brighter flash when bioluminescent capacity is stimulated. Here, we show that copepodamide-induced bioluminescence in L. polyedra causes a marked shift in the grazing preference of the copepod Acartia tonsa Dana. L. polyedra goes from being the preferred prey when non-bioluminescent to near complete rejection when pre-treated with copepodamides to induce a higher bioluminescent capacity. High-speed and low-light-sensitive videos show how L. polyedra cells flash upon contact with the copepod and are subsequently rejected, seemingly unharmed (Videos S1 and S2). Instead, A. tonsa shows compensatory feeding on the alternative prey.

Effects of predator lipids on dinoflagellate defence mechanisms - increased bioluminescence capacity.

Short flashes of blue light (bioluminescence) from dinoflagellates can reduce copepod grazing of light-emitting cells. Other protective strategies against grazing are toxicity, reduced cell chain length and altered swimming patterns in different phytoplankton. Both toxicity and bioluminescence capacity in dinoflagellates decrease in copepod-free cultures, but toxin production can be restored in response to chemical alarm signals from copepods, copepodamides. Here we show that strains of the dinoflagellates Lingulodinium polyedra and Alexandrium tamarense, kept in culture for 14 and 9 years respectively, are capable of increasing their total bioluminescence capacity in response to copepodamides. The luminescence response to mechanical stimulation with air bubbles also increases significantly in L. polyedra after exposure to copepodamides. Effects on size, swimming speed and rate of change of direction in L. polyedra and A. tamarense were not detected, suggesting that post-encounter mechanisms such as bioluminescence and toxin production may constitute the dominating line of defence in these taxa. To our knowledge, this study provides the first evidence of changes in bioluminescence physiology as a response to chemical cues from natural enemies and emphasizes the importance of bioluminescence as an anti-grazing strategy.