Bioluminescent flashes drive nighttime schooling behavior and synchronized swimming dynamics in flashlight fish

Schooling fishes, like flocking birds and swarming insects, display remarkable behavioral coordination. While over 25% of fish species exhibit schooling behavior, nighttime schooling has rarely been observed or reported. This is due to vision being the primary modality for schooling, which is corroborated by the fact that most fish schools disperse at critically low light levels. Here we report on a large aggregation of the bioluminescent flashlight fish Anomalops katoptron that exhibited nighttime schooling behavior during multiple moon phases, including the new moon. Data were recorded with a suite of low-light imaging devices, including a high-speed, high-resolution scientific complementary metal-oxide-semiconductor (sCMOS) camera. Image analysis revealed nighttime schooling using synchronized bioluminescent flashing displays, and demonstrated that school motion synchrony exhibits correlation with relative swim speed. A computer model of flashlight fish schooling behavior shows that only a small percentage of individuals need to exhibit bioluminescence in order for school cohesion to be maintained. Flashlight fish schooling is unique among fishes, in that bioluminescence enables schooling in conditions of no ambient light. In addition, some members can still partake in the school while not actively exhibiting their bioluminescence. Image analysis of our field data and model demonstrate that if a small percentage of fish become motivated to change direction, the rest of the school follows. The use of bioluminescence by flashlight fish to enable schooling in shallow water adds an additional ecological application to bioluminescence and suggests that schooling behavior in mesopelagic bioluminescent fishes may be also mediated by luminescent displays.集群鱼类（schooling fish）与集群鸟类、群居昆虫类似，均展现出卓越的行为协同能力。尽管已有超过25%的鱼类物种展现出集群行为，但夜间集群现象却极少被观测或报道。这是因为视觉是集群行为的主要感知模态，多数鱼群会在临界低光照条件下解散的现象，也佐证了这一结论。本研究报道了一大群生物发光（bioluminescent）的发光器鱼类（flashlight fish，Anomalops katoptron），它们在包括新月在内的多个月相周期中均展现出夜间集群行为。研究数据通过一套低光成像设备采集，其中包含高速高分辨率的科学互补金属氧化物半导体（sCMOS）相机。图像分析结果显示，该鱼群通过同步的生物发光闪光信号实现夜间集群，并证实鱼群运动的同步性与相对游速存在相关性。针对发光器鱼类集群行为构建的计算机模型显示，仅需少量个体展现生物发光行为，即可维持整个鱼群的凝聚力。发光器鱼类的集群行为在鱼类中独树一帜，其可借助生物发光在完全无光的环境中实现集群；此外，部分个体即便未主动展现生物发光行为，仍可加入鱼群集群。对野外采集数据与模型的图像分析表明，只要有少量个体产生转向动机，整个鱼群便会随之行动。发光器鱼类借助生物发光在浅水环境中实现集群的现象，为生物发光增添了一项新的生态应用场景，同时也暗示中层浮游（mesopelagic）生物发光鱼类的集群行为，或许同样是通过发光信号介导完成的。