Redirection of ambient light improves predator detection in a diurnal fish

Abstract

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 on Tripterygion 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 improves T. delaisi 's ability to detect the cryptobenthic sit-and-wait predator Scorpaena 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.

A context analysis of bobbing and fin‐flicking in a small marine benthic fish

“…When released on the gravel lane, triplefins immediately started to show fin flicks and bobs while carefully approaching the display compartment. This is consistent with previous laboratory and field experiments that showed that a differentiated response between visual stimuli can be observed very soon after release in the experimental tank (Santon et al., 2020). Based on these tests, we set the observation time at 10 min for each stimulus.…”

“…Triplefins were gently released in the middle of the gravel lane and, during the subsequent 10 min, a single observer (FD) counted the number of bobs and fin flicks observed in one‐minute intervals and noted the distance from the tip of triplefins’ snout to the stimulus at the end of each full minute. Other typical behaviors in T. delaisi such as bright spots of focussed light on the iris, termed ocular sparks (Michiels et al., 2018; Santon et al., 2020), and tail flicks (Wirtz, 1978) were also noted, but ignored in the analysis due to their very low frequencies. Before each 10‐min session, the focal triplefin was temporarily placed in a dark container for 5 min while the visual stimulus was put in place.…”

“…delaisi, such as being bottom‐dwelling, small, and cryptic (Brandl et al., 2018; McCormick & Manassa, 2008). Furthermore, previous laboratory and field experiments already showed that T. delaisi responds strongly to the visual presence of predators in comparison to control stones, while keeping chemical and sound cues mixed (Santon et al., 2020). We thus compared the response of triplefins to the visual presence of a cryptobenthic macropredator, the black scorpionfish ( Scorpaena porcus ), and to three harmless visual stimuli: a stone, a conspecific triplefin, and a nonpredatory cryptobenthic heterospecific combtooth blenny ( Parablennius sanguinolentus ).…”

Small benthic fish strike at prey over distances that fall within theoretical predictions for active sensing using light

“…Although this small light source next to the pupil is weak, its close alignment with the visual axis makes it sufficiently strong to induce perceivable reflections in the reflective eyes of target organisms. Recently, we showed that this mechanism can contribute to the visual detection of the retroreflective eyes of cryptic, predatory scorpionfish (Santon et al ., 2018, 2020). Whether active sensing with light or diurnal active photolocation contributes to prey detection has not yet been experimentally demonstrated.…”

“…Recently, it has been shown that micropredatory fish are able to redirect enough downwelling sunlight sideways to illuminate and thus improve visual detection of nearby organisms (Bitton et al, 2019;Santon et al, 2020). This suggestion follows the simple observation that a small amount of light suffices to generate a perceivable increase in eyeshine in the pupils of species with retroreflective eyes, provided the observer possesses a (small) light source near-coaxial to its viewing axis, for example on its iris (Jack, 2014(Jack, , 2015Santon et al, 2018).…”