Synchronous and asynchronous counterillumination by three types of photophores in the firefly squid, Watasenia scintillans

Abstract

Countershading--animal body coloration that is darker on the dorsum than the ventrum--is a form of crypsis achieved through a gradient in skin pigmentation. Counterillumination is somewhat similar, achieving crypsis in midwater marine organisms by emitting downward-directed bioluminescence. Although mesopelagic squids are assumed to use counterillumination, high-resolution spatiotemporal changes in illumination, particularly for each photophore type, have not been elucidated. Watasenia scintillans has three types of photophores on its ventral surfaces: blue- and green-emitting ventral photophores and ocular photophores. It is demonstrated here that all three types of photophores are synchronously, reversibly, and repeatedly involved in counterillumination in response to changes in dim overhead lighting. Furthermore, the green-emitting photophores maintained luminescence in darkness, and their on/off switching is precisely regulated within the ambient temperature range. The photoreceptors responsible for counterillumination are extraocular photosensitive vesicles (EOPs) rather than eyes. Exposure of EOPs to visible light (blue, green, and yellow) elicited counterillumination in proportion to light intensity. No color shifts (such as from green to blue) were observed in any of the photophores. While synchronous illumination seems to support the crypsis hypothesis, the ability to independently control each photophore type could also support a previous hypothesis of conspecific signaling. Significance StatementBioluminescence is widespread among deep-sea organisms, yet the specific functions of individual light-producing organs distributed across the body surface remain underexplored. In this study, three types of ventral photophores in the firefly squid, Watasenia scintillans, were video-recorded, revealing their synchronous involvement in counterillumination--a mechanism that obscures the body silhouette when viewed from below against blue downwelling surface light. Notably, green-emitting photophores remained illuminated for extended periods in darkness, indicating a potential role in visual communication among conspecifics. The video-based techniques employed to quantify individual photophore activity provide new opportunities to investigate photo-signaling in animals inhabiting the mesopelagic zone.