Swimming Behaviour Tunes Fish Polarization Vision to Double Prey Sighting Distance

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

Is the Use of Underwater Polarized Light by Fish Restricted to Crepuscular Time Periods?

AbstractWe measured the spectral distributions of the underwater total and polarized light fields in the upper photic zone of meso-eutrophic waters (i.e., blue-green waters containing medium to high chlorophyll a concentrations). Per cent polarization levels during the day were always lower than 40%, but at crepuscular times these values could increase to 67%. A corresponding change occurred in the spectral distribution, with proportionately more shorter wavelength photons contributing to the total spectrum during crepuscular periods. Electrophysiological recordings from the optic nerve of rainbow trout subjected to light stimuli of varying polarization percentages show that the animal's threshold for detecting polarized light is between 63 and 72%. These physiological findings suggest that the use of water-induced polarized light cues by rainbow trout and similar percomorph fish should be restricted to crepuscular time periods. © 1997 Elsevier Science Ltd. All rights reserved

No Evidence of Polarization Sensitivity in Freshwater Sunfish from Multi-unit Optic Nerve Recordings

AbstractThe sensitivities of two species of sunfish (Lepomis gibbosus and Lepomis cyanellus) to the electric field (E-vector) of polarized light were assessed by compound action potential recordings from the optic nerve of live fish. Under white light and long wavelength adapting backgrounds, two cone mechanisms were found with maximum sensitivities in the long wavelength (λmax ≈ 620 nm) and middle wavelength (λmax ≈ 530 nm) regions of the spectrum. In contrast to previous findings (Cameron and Pugh, 1991), no evidence of polarization sensitivity was observed for either species. We conclude from these results that post-larval sunfish do not exhibit polarization sensitivity. © 1997 Elsevier Science Ltd. All rights reserved

Functional significance of the taper of vertebrate cone photoreceptors

© The Author(s), 2012. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Journal of General Physiology 139 (2012): 159-187, doi:10.1085/jgp.201110692.Vertebrate photoreceptors are commonly distinguished based on the shape of their outer segments: those of cones taper, whereas the ones from rods do not. The functional advantages of cone taper, a common occurrence in vertebrate retinas, remain elusive. In this study, we investigate this topic using theoretical analyses aimed at revealing structure–function relationships in photoreceptors. Geometrical optics combined with spectrophotometric and morphological data are used to support the analyses and to test predictions. Three functions are considered for correlations between taper and functionality. The first function proposes that outer segment taper serves to compensate for self-screening of the visual pigment contained within. The second function links outer segment taper to compensation for a signal-to-noise ratio decline along the longitudinal dimension. Both functions are supported by the data: real cones taper more than required for these compensatory roles. The third function relates outer segment taper to the optical properties of the inner compartment whereby the primary determinant is the inner segment’s ability to concentrate light via its ellipsoid. In support of this idea, the rod/cone ratios of primarily diurnal animals are predicted based on a principle of equal light flux gathering between photoreceptors. In addition, ellipsoid concentration factor, a measure of ellipsoid ability to concentrate light onto the outer segment, correlates positively with outer segment taper expressed as a ratio of characteristic lengths, where critical taper is the yardstick. Depending on a light-funneling property and the presence of focusing organelles such as oil droplets, cone outer segments can be reduced in size to various degrees. We conclude that outer segment taper is but one component of a miniaturization process that reduces metabolic costs while improving signal detection. Compromise solutions in the various retinas and retinal regions occur between ellipsoid size and acuity, on the one hand, and faster response time and reduced light sensitivity, on the other.This work was funded by the Natural Sciences and Engineering Research Council of Canada Discovery Grant 238886 and a Grass-Marine Biological Laboratory Sabbatical Fellowship in Neurosciences to I. Novales Flamarique.2012-07-1

Parallel Opsin Switches in Multiple Cone Types of the Starry Flounder Retina: Tuning Visual Pigment Composition for a Demersal Life Style

Variable expression of visual pigment proteins (opsins) in cone photoreceptors of the vertebrate retina is a primary determinant of vision plasticity. Switches in opsin expression or variable co-expression of opsins within differentiated cones have been documented for a few rodents and fishes, but the extent of photoreceptor types affected and potential functional significance are largely unknown. Here, we show that both single and double cones in the retina of a flatfish, the starry flounder (Platichthys stellatus), undergo visual pigment changes through opsin switches or variable opsin co-expression. As the post-metamorphic juvenile (i.e., the young asymmetric flatfish with both eyes on one side of the body) grows from ~5 g to ~196 g, some single cones and one member of unequal double cones switched from a visual pigment with maximum wavelength of absorbance, λmax, at shorter wavelengths (437 nm and 527 nm) to one with longer λmax (456 nm and 545 nm, respectively) whereas other cones had intermediate visual pigments (λmax at 445 nm or 536 nm) suggesting co-expression of two opsins. The shift toward longer wavelength absorbing visual pigments was in line with maximizing sensitivity to the restricted light spectrum at greater depths and achromatic detection of overhead targets

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

The retinas of nonmammalian vertebrates have cone photoreceptor mosaics that are often organized as highly patterned lattice-like distributions. In fishes, the two main lattice-like patterns are composed of double cones and single cones that are either assembled as interdigitized squares or as alternating rows. The functional significance of such orderly patterning is unknown. Here, the cone mosaics in two species of Soleidae flatfishes, the common sole and the Senegalese sole, were characterized and compared to those from other fishes to explore variability in cone patterning and how it may relate to visual function. The cone mosaics of the common sole and the Senegalese sole consisted of single, double, and triple cones in formations that differed from the traditional square mosaic pattern reported for other flatfishes in that no evidence of higher order periodicity was present. Furthermore, mean regularity indices for single and double cones were conspicuously lower than those of other fishes with "typical" square and row mosaics, but comparable to those of goldfish, a species with lattice-like periodicity in its cone mosaic. Opsin transcripts detected by quantitative polymerase chain reaction (sws1, sws2, rh2.3, rh2.4, lws, and rh1) were uniformly expressed across the retina of the common sole but, in the Senegalese sole, sws2, rh2.4, and rh1 were more prevalent in the dorsal retina. Microspectrophotometry revealed five visual pigments in the retina of the common sole [S(472), M(523), M(536), L(559), and rod(511)] corresponding to the repertoire of transcripts quantified except for sws1. Overall, these results indicate a loss of cone mosaic patterning in species that are primarily nocturnal or dwell in low light environments as is the case for the common sole and the Senegalese sole. The corollary is that lattice-like patterning of the cone mosaic may improve visual acuity. Ecological and physiological correlates derived from observations across multiple fish taxa that live in low light environments and do not possess lattice-like cone mosaics are congruent with this claim