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Cases where animals use controlled illumination to improve vision are rare and thus far limited to chemiluminescence, which only functions in darkness. This constraint was recently relaxed by studies onTripterygion delaisi, a small triplefin that redirects sunlight instead. By reflecting light sideways with its iris, it has been suggested to induce and detect eyeshine in nearby micro-prey. Here, we test whether ‘diurnal active photolocation’ also improvesT. delaisi's ability to detect the cryptobenthic sit-and-wait predatorScorpaena porcus,a scorpionfish with strong daytime retroreflective eyeshine. Three independent experiments revealed that triplefins in which light redirection was artificially suppressed approached scorpionfish significantly closer than two control treatments before moving away to a safer distance. Visual modelling confirmed that ocular light redirection by a triplefin is sufficiently strong to generate a luminance increase in scorpionfish eyeshine that can be perceived by the triplefin over 6–8 cm under average conditions. These distances coincide well with the closest approaches observed. We conclude that light redirection by small, diurnal fish significantly contributes to their ability to visually detect cryptic predators, strongly widening the conditions under which active sensing with light is feasible. We discuss the consequences for fish eye evolution.

Active sensing by means of light is rare. In vertebrates, it is known only from chemiluminescent fish with light organs below their pupils, an anatomical arrangement that is ideal to generate eyeshine in the pupils of nearby organisms. Here, we test whether diurnal fish can achieve the same by redirecting sunlight through reflection instead. We recently showed that small (< 5 cm), benthic, marine triplefin fish actively redirect downwelling light using their iris. We hypothesized that this mechanism allows triplefins to improve detection of a cryptic organism by generating eyeshine in its pupil. Here, we tested this by attaching small dark hats to triplefins to shade their iris from downwelling light. Two controls consisted of triplefins with a clear or no hat. These treatments test the prediction that light redirection increases the visual detection ability of triplefins. To this end, we placed treated fish in a tank with a display compartment containing either a stone as the control stimulus, or a scorpionfish, i.e. a cryptic, motionless triplefin predator with retroreflective eyes. After overnight acclimatization, we determined the average distance triplefins kept from the display compartment over two days. Both in the laboratory (n= 15 replicates per treatment) and in a similar field experiment at 15 m depth (n= 43 replicates per treatment) fish kept longer distances from the scorpionfish than from the stone. This response varied between hat treatments: shaded triplefins stayed significantly closer to the scorpionfish in the laboratory and in one of two orientations tested in the field. A follow-up field experiment at 10 m depth revealed the immediate response of triplefins to a scorpionfish. At first, many individuals (n= 80) moved towards it, with shaded triplefins getting significantly closer. All individuals then gradually moved to a safer distance at the opposite half of the tank. Visual modelling supported the experimental results by showing that triplefins can redirect enough light with their iris to increase a scorpionfish’s pupil brightness above detection threshold at a distance of 7 cm under average field conditions and at more than 12 cm under favorable conditions. We conclude that triplefins are generally good in the visual detection of a cryptic predator, but can significantly improve this ability when able to redirect downwelling light with their iris and induce eyeshine in the predator’s pupil. We discuss the consequences of “diurnal active photolocation” for visual detection and camouflage among fish species.

The environment and lifestyle of a species are known to exert selective pressure on the visual system, often demonstrating a tight link between visual morphology and ecology. Many studies have predicted the visual requirements of a species by examining the anatomical features of the eye. However, among the vast number of studies on visual specializations in aquatic animals, only a few have focused on small benthic fishes that occupy a heterogeneous and spatially complex visual environment. This study investigates the general retinal anatomy including the topography of both the photoreceptor and ganglion cell populations and estimates the spatial resolving power of the eye of the Mediterranean triplefin Tripterygion delaisi. Retinal wholemounts were prepared to systematically and quantitatively analyze photoreceptor and retinal ganglion cell densities using design-based stereology. To further examine the retinal structure, we also used magnetic resonance imaging and histological examination of retinal cross sections. Observations of the triplefin's eyes revealed them to be highly mobile, allowing them to view the surroundings without body movements. A rostral aphakic gap and the elliptical shape of the eye extend its visual field rostrally and allow for a rostro-caudal accommodatory axis, enabling this species to focus on prey at close range. Single and twin cones dominate the retina and are consistently arranged in one of two regular patterns, which may enhance motion detection and color vision. The retina features a prominent, dorso-temporal, convexiclivate fovea with an average density of 104,400 double and 30,800 single cones per mm2, and 81,000 retinal ganglion cells per mm2. Based on photoreceptor spacing, spatial resolving power was calculated to be between 6.7 and 9.0 cycles per degree. Location and resolving power of the fovea would benefit the detection and identification of small prey in the lower frontal region of the visual field.

The light environment in water bodies changes with depth due to the absorption of short and long wavelengths. Below 10 m depth, red wavelengths are almost completely absent rendering any red-reflecting animal dark and achromatic. However, fluorescence may produce red coloration even when red light is not available for reflection. A large number of marine taxa including over 270 fish species are known to produce red fluorescence, yet it is unclear under which natural light environment fluorescence contributes perceptively to their colours. To address this question we: (i) characterized the visual system ofTripterygion delaisi,which possesses fluorescent irides, (ii) separated the colour of the irides into its reflectance and fluorescence components and (iii) combined these data with field measurements of the ambient light environment to calculate depth-dependent perceptual chromatic and achromatic contrasts using visual modelling. We found that triplefins have cones with at least three different spectral sensitivities, including differences between the two members of the double cones, giving them the potential for trichromatic colour vision. We also show that fluorescence contributes increasingly to the radiance of the irides with increasing depth. Our results support the potential functionality of red fluorescence, including communicative roles such as species and sex identity, and non-communicative roles such as camouflage.