Revisiting the burglar alarm hypothesis: A behavioural cascade mediated by dinoflagellate bioluminescence

1. Bioluminescence is widespread among marine organisms and has evolved independently multiple times. While its specific adaptive value is diverse, bioluminescence in most cases mediates fundamental interactions between individuals (predator, prey, mates) and thus impacts ecosystem processes. One hypothesized value of bioluminescence in dinoflagellates is through the ‘burglar alarm’: Grazers of phytoplankton will make the ambient water ‘glow’ as they swim, thereby attracting visual predators of the grazer, thus indirectly protecting the dinoflagellates.
2. However, the most important grazers of dinoflagellates, copepods, are generally too small to elicit dinoflagellates to glow. Only individual cells captured by a copepod will flash, which in turn elicits a powerful escape response in the copepod. Here, we test a variant of this hypothesis that may work for copepods. The behavioural response of the grazer to the flashing of a captured dinoflagellate, rather than the flashing itself, attracts the attention of the grazer's flow-sensing predators.
3. We demonstrate that bioluminescence in three dinoflagellates reduces the clearance and ingestion rate of nauplii of the copepod Temora longicornis. The presence of bioluminescent cells also elicited an increased frequency of high-speed jumps of the grazers.
4. The increased jump frequency elevated the detectability of the grazers to a flow-sensing predator, the copepod Centropages typicus, consequently leading to increased predation mortality of T. longicornis nauplii.
5. The consequent behavioural cascade mediated by bioluminescence works for small grazers that cause only single cells to flash, unlike the traditional description of the burglar alarm. The significance of such behavioural mediated indirect interactions in shaping food webs is becoming increasingly recognized, although rarely demonstrated in pelagic food webs.
6. We argue that the burglar alarm is a secondary adaptation, while the defence of individual cells is the primary adaptive value of bioluminescence in dinoflagellates.