Evidence that eye-facing photophores serve as a reference for counterillumination in an order of deep-sea fishes.

Counterillumination, the masking of an animal's silhouette with ventral photophores, is found in a number of mesopelagic taxa but is difficult to employ because it requires that the animal match the intensity of downwelling light without seeing its own ventral photophores. It has been proposed that the myctophid,Tarletonbeania crenularis,uses a photophore directed towards the eye, termed an eye-facing photophore, as a reference standard that it adjusts to match downwelling light. The potential use of this mechanism, however, has not been evaluated in other fishes. Here, we use micro-computed tomography, photography and dissection to evaluate the presence/absence of eye-facing photophores in three families of stomiiform fishes. We found that all sampled species with ventral photophores capable of counterillumination possess an eye-facing photophore that is pigmented on the anterior and lateral sides, thus preventing its use as a laterally directed signal, lure or searchlight. The two species that are incapable of counterillumination,Cyclothone obscuraandSigmops bathyphilus, lack an eye-facing photophore. After determining the phylogenetic distribution of eye-facing photophores, we used histology to examine the morphology of the cranial tissue inArgyropelecus aculeatusand determined that light from the eye-facing photophore passes through a transparent layer of tissue, then the lens, and finally strikes the accessory retina. Additionally, eight of the 14 species for which fresh specimens were available had an aphakic gap that aligned with the path of emitted light from the eye-facing photophore, while the remaining six had no aphakic gap. These findings, combined with records of eye-facing photophores from distantly related taxa, strongly suggest that eye-facing photophores serve as a reference for counterillumination in these fishes.