Active sensing with light improves predator detection in a diurnal fish

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.