Revisiting the burglar-alarm hypothesis: a behavioral cascade mediated by dinoflagellate bioluminescence

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. 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 behavioral 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. 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. 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. The consequent behavioral cascade mediated by
bioluminescence works for small grazers that cause only single cells to
flash, unlike the traditional description of the burglar alarm.