Swimming behaviour tunes fish polarization vision to double prey sighting distance

Abstract

The analysis of the polarization of light expands vision beyond the realm of colour and intensity and is used for multiple ecological purposes among invertebrates including orientation, object recognition, and communication. How vertebrates use polarization vision as part of natural behaviours is widely unknown. In this study, I tested the hypothesis that polarization vision improves the detection of zooplankton prey by the northern anchovy, Engraulis mordax, the only vertebrate with a demonstrated photoreceptor basis explaining its polarization sensitivity. Juvenile anchovies were recorded free foraging on zooplankton under downwelling light fields of varying percent polarization (98%, 67%, 19%, and 0% - unpolarized light). Analyses of prey attack sequences showed that anchovies swam in the horizontal plane perpendicular, on average, to the polarization direction of downwelling light and attacked prey at pitch angles that maximized polarization contrast perception of prey by the ventro-temporal retina, the area devoted to polarization vision in this animal. Consequently, the mean prey location distance under polarized light was up to 2.1 times that under unpolarized conditions. All indicators of polarization vision mediated foraging were present under 19% polarization, which is within the polarization range commonly found in nature during daylight hours. These results demonstrate: (i) the first use of oriented swimming for enhancing polarization contrast detection of prey, (ii) its relevance to improved foraging under available light cues in nature, and (iii) an increase in target detection distance that is only matched by polarization based artificial systems.

Photoreceptor distributions, visual pigments and the opsin repertoire of Atlantic halibut (Hippoglossus hippoglossus)

“…The shift in area of greatest resolving power conforms with the foraging needs of the fish as it transforms from a bilaterally symmetric larva to a flattened, demersal juvenile. Pelagic fishes, including larvae, often have the highest cone densities in the ventrotemporal retina and strike at prey that contrast against the water background located in front of them or slightly above 25 – 27 . Demersal fishes, on the other hand, often strike at prey that contrasts against the bottom of the water body 28 .…”

Straying from the flatfish retinal plan: Cone photoreceptor patterning in the common sole (Solea solea) and the Senegalese sole (Solea senegalensis)

“…Triple cones have also been reported in other fish species (Fritsch, Collin, & Michiels, ; Miyazaki, Iwami, Somiya, & Meyer‐Rochow, ; Reckel & Melzer, ; Shand, Archer, & Collin, ) but, in these, the morphology is different from that found in anchovies and they constitute less than 1% of the cone population (though the triple cone can be dominant where found at highest density, Miyazaki et al, ; Fritsch et al, ). These three exceptions appear to have evolved for life in darkness or in very low light conditions, where maximum sensitivity is achieved by an almost rod exclusive retina (deep water fishes, Wagner et al, ; night‐active eels, Heβ et al, ), and for polarization vision, at least in part, in the case of anchovies (Novales Flamarique, , ).…”

“…The third is found among anchovies where a variety of unusual polycone formations have been reported (Fineran & Nicol, 1978;Heβ, Melzer, Eser, & Smola, 2006). In some anchovy species, the cones are morphologically segregated in that continuous rows of two alternating types of single cone dominate the ventro-temporal retina whereas rows of triple cones and single cones are found in other parts of the retina (Heβ et al, 2006;Kondrashev, Gnyubkina, Valentina, & Zueva, 2012;Novales Flamarique, 2011). Triple cones have also been reported in other fish species (Fritsch, Collin, & Michiels, 2017;Miyazaki, Iwami, Somiya, & Meyer-Rochow, 2002;Shand, Archer, & Collin, 1999) but, in these, the morphology is different from that found in anchovies and they constitute less than 1% of the cone population (though the triple cone can be dominant where found at highest density, Miyazaki et al, 2002;Fritsch et al, 2017).…”

Horsefly object-directed polarotaxis is mediated by a stochastically distributed ommatidial subtype in the ventral retina

“…Linearly polarized light is exploited by many terrestrial animals as an important celestial navigational cue (1, 2). On the other hand, some animals use polarization vision to enhance the visual contrast (3–5). Horseflies are attracted to linearly polarized light, reflected from natural or man-made objects (6, 7).…”