56. Flamarique, IN; Fujihara, R; Yazawa, R; Bolstad, K; Gowen, B; Yoshizaki, G. (2021) Disrupted eye and head development in rainbow trout with reduced ultraviolet (sws1) opsin expression.J. Comp. Neurol. 529: 3013-3031 Disrupted eye and head development in rainbow trout with reduced ultraviolet (sws1) opsin expression
AB5407; CRISPR; Cas9; fish; photoreceptor; retina; sws1 antiserum; visual opsin
Visual opsins are proteins expressed by retinal photoreceptors that capture light to begin the process of phototransduction. In vertebrates, the two types of photoreceptors (rods and cones) express one or multiple opsins and are distributed in variable patterns across the retina. Some cones form opsin retinal gradients, as in the mouse, whereas others form more demarcated opsin domains, as in the lattice-like mosaic retinas of teleost fishes. Reduced rod opsin (rh1) expression in mouse, zebrafish, and African clawed frog results in lack of photoreceptor outer segments (i.e., the cilium that houses the opsins) and, in the case of the mouse, to retinal degeneration. The effects of diminished cone opsin expression have only been studied in the mouse where knockout of the short-wavelength sensitive 1 (sws1) opsin leads to ventral retinal cones lacking outer segments, but no retinal degeneration. Here we show that, following CRISPR/Cas9 injections that targeted knockout of the sws1 opsin in rainbow trout, fish with diminished sws1 opsin expression exhibited a variety of developmental defects including head and eye malformations, underdeveloped outer retina, mislocalized opsin expression, cone degeneration, and mosaic irregularity. All photoreceptor types were affected even though sws1 is only expressed in the single cones of wild fish. Our results reveal unprecedented developmental defects associated with diminished cone opsin expression and suggest that visual opsin genes are involved in regulatory processes that precede photoreceptor differentiation. DOI PubMed
55. Frau, S; Flamarique, IN; Keeley, PW; Reese, BE; Muñoz-Cueto, JA. (2020) Straying from the flatfish retinal plan: Cone photoreceptor patterning in the common sole (Solea solea) and the Senegalese sole (Solea senegalensis).J. Comp. Neurol. 528: 2283-2307 Straying from the flatfish retinal plan: Cone photoreceptor patterning in the common sole (Solea solea) and the Senegalese sole (Solea senegalensis)
cone distributions; opsin transcript; photoreceptor; retina; visual pigment
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. DOI PubMed
54. Flamarique, IN. (2019) Swimming behaviour tunes fish polarization vision to double prey sighting distance.Sci Rep 9 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 ventrotemporal 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. DOI PubMed
53. Flamarique, IN. (2019) Light exposure during embryonic and yolk-sac alevin development of Chinook salmon Oncorhynchus tshawytscha does not alter the spectral phenotype of photoreceptors.J. Fish Biol. 95: 214-221 Light exposure during embryonic and yolk-sac alevin development of Chinook salmon Oncorhynchus tshawytscha does not alter the spectral phenotype of photoreceptors
in situ hybridization; inheritance; Oncorhynchus tshawytscha; phenotypic plasticity; photoreceptor; retina
Colour vision is mediated by the expression of different visual pigments in photoreceptors of the vertebrate retina. Each visual pigment is a complex of a protein (opsin) and a vitamin A chromophore; alterations to either component affects visual pigment absorbance and, potentially, the visual capabilities of an animal. Many species of fish undergo changes in opsin expression during retinal development. In the case of salmonid fishes the single cone photoreceptors undergo a switch in opsin expression from SWS1 (ultraviolet sensitive) to SWS2 (blue-light sensitive) starting at the yolk-sac alevin stage, around the time when they first experience light. Whether light may initiate this event or produce a plastic response in the various photoreceptors is unknown. In this study, Chinook salmon Oncorhynchus tshawytscha were exposed to light from the embryonic (5 days prior to hatching) into the yolk sac alevin (25 days post hatching) stage and the spectral phenotype of photoreceptors assessed with respect to that of unexposed controls by in situ hybridization with opsin riboprobes. Light exposure did not change the spectral phenotype of photoreceptors, their overall morphology or spatial arrangement. These results concur with those from a variety of fish species and suggest that plasticity in photoreceptor spectral phenotype via changes in opsin expression may not be a widespread occurrence among teleosts. DOI PubMed
52. Flamarique, IN; Ahmed, AS; Cheng, CL; Molday, RS; Devlin, RH. (2019) Growth hormone regulates opsin expression in the retina of a salmonid fish.J. Neuroendocrinol. 31 Growth hormone regulates opsin expression in the retina of a salmonid fish
fish; growth hormone; opsin; retina; visual pigment
Colour vision relies on retinal photoreceptors that express a different predominant visual pigment protein (opsin). In several vertebrates, the primary opsin expressed by a photoreceptor can change throughout ontogeny, although the molecular factors that influence such regulation are poorly understood. One of these factors is thyroid hormone which, together with its receptors, modulates opsin expression in the retinas of multiple vertebrates including rodents and salmonid fishes. In the latter, thyroid hormone induces a switch in opsin expression from SWS1 (ultraviolet light sensitive) to SWS2 (short wavelength or blue light sensitive) in the single cone photoreceptors of the retina. The actions of other hormones on opsin expression have not been investigated. In the present study, we used a transgenic strain of coho salmon (Oncorhynchus kitsutch) with enhanced levels of circulating growth hormone compared to that of wild siblings to assess the effects of this hormone on the SWS1 to SWS2 opsin switch. Transgenic fish showed a developmentally accelerated opsin switch compared to size-matched controls as assessed by immunohistological and in situ hybridisation labelling of photoreceptors and by quantification of transcripts using quantitative polymerase chain reaction. This accelerated switch led to a different spectral sensitivity maximum, under a middle to long wavelength adapting background, from ultraviolet (lambda(max) similar to 380 nm) in controls to short wavelengths (lambda(max) similar to 430 nm) in transgenics, demonstrating altered colour vision. The effects of growth hormone over-expression were independent of circulating levels of thyroid hormone (triiodothyronine), the hormone typically associated with opsin switches in vertebrates. DOI PubMed
51. Savelli, I; Flamarique, IN. (2018) Variation in opsin transcript expression explains intraretinal differences in spectral sensitivity of the northern anchovy.Visual Neurosci. 35 Variation in opsin transcript expression explains intraretinal differences in spectral sensitivity of the northern anchovy
Anchovy; Cone photoreceptor; Chromophore; Optic nerve; Color vision
Vertebrate retinal photoreceptors house visual pigments that absorb light to begin the process of vision. The light absorbed by a visual pigment depends on its two molecular components: protein (opsin) and chromophore (a vitamin A derivative). Although an increasing number of studies show intraretinal variability in visual pigment content, it is only for two mammals (human and mouse) and two birds (chicken and pigeon) that such variability has been demonstrated to underlie differences in spectral sensitivity of the animal. Here, we show that the spectral sensitivity of the northern anchovy varies with retinal quadrant and that this variability can be explained by differences in the expression of opsin transcripts. Retinal (vitamin A1) was the only chromophore detected in the retina, ruling out this molecular component as a source of variation in spectral sensitivity. Chromatic adaptation experiments further showed that the dorsal retina had the capacity to mediate color vision. Together with published results for the ventral retina, this study is the first to demonstrate that intraretinal opsin variability in a fish drives corresponding variation in the animal's spectral sensitivity. DOI PubMed
50. Savelli, I; Flamarique, IN; Iwanicki, T; Taylor, JS. (2018) Parallel opsin switches in multiple cone types of the starry flounder retina: tuning visual pigment composition for a demersal life style.Sci Rep 8 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 similar to 5 g to similar to 196 g, some single cones and one member of unequal double cones switched from a visual pigment with maximum wavelength of absorbance, lambda(max), at shorter wavelengths (437 nm and 527 nm) to one with longer lambda(max) (456 nm and 545 nm, respectively) whereas other cones had intermediate visual pigments (lambda(max) 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. DOI PubMed
49. Zukoshi, R; Savelli, I; Flamarique, IN. (2018) Foraging performance of two fishes, the threespine stickleback and the Cumand guppy, under different light backgrounds.Vision Res. 145 Foraging performance of two fishes, the threespine stickleback and the Cumand guppy, under different light backgrounds
Ultraviolet light; Long wavelength light; Cone photoreceptor; Retina; Daphnia contrast
Many vertebrates have cone photoreceptors that are most sensitive to ultraviolet (UV) light termed UV cones. The ecological functions that these cones contribute to are seldom known though they are suspected of improving foraging and communication in a variety of fishes. In this study, we used several spectral backgrounds to assess the contribution of UV and violet cones, or long wavelength (L) cones, in the foraging performance of juvenile Cumana guppy, Poecilia reticulate, or marine stickleback, Gasterosteus aculeatus. Regardless of whether the light spectrum contained or not wavelengths below 450 nm (the limiting wavelength for UV cone stimulation), the foraging performance of both species was statistically the same, as judged by the mean distance and angle associated with attacks on prey (Daphnia magna). Our experiments also showed that the foraging performance of sticklebacks when only the double cones (and, almost exclusively, the L cones) were active was similar to that when all cones were functional, demonstrating that the double cone was sufficient for prey detection. This result indicates that foraging potentially relied on an achromatic channel serving prey motion detection, as the two spectral cone types that make up the double cone [maximally sensitive to middle (M) and long (L) wavelengths, respectively] form the input to the achromatic channel in cyprinid fishes and double cones are widely associated with achromatic tasks in other vertebrates including reptiles and birds. Stickleback performance was also substantially better when foraging under a 100% linearly polarized light field than when under an unpolarized light field. Together, our results suggest that in some teleost species UV cones exert visually-mediated ecological functions different from foraging, and furthermore that polarization sensitivity could improve the foraging performance of sticklebacks. DOI PubMed
48. Flamarique, IN. (2017) A vertebrate retina with segregated colour and polarization sensitivity.Proceedings of the Royal Society B-Biological Sciences 284 A vertebrate retina with segregated colour and polarization sensitivity
anchovy; optic nerve; cone photoreceptor; axial dichroism
Besides colour and intensity, some invertebrates are able to independently detect the polarization of light. Among vertebrates, such separation of visual modalities has only been hypothesized for some species of anchovies whose cone photoreceptors have unusual ultrastructure that varies with retinal location. Here, I tested this hypothesis by performing physiological experiments of colour and polarization discrimination using the northern anchovy, Engraulis mordax. Optic nerve recordings showed that the ventro-temporal (VT), but not the ventro-nasal (VN), retina was polarization sensitive, and this coincided with the exclusive presence of polarization-sensitive photoreceptors in the VT retina. Spectral (colour) sensitivity recordings from the VN retina indicated the contribution of two spectral cone mechanisms to the optic nerve response, whereas only one contributed to the VT retina. This was supported by the presence of only one visual pigment in the VT retina and two in the VN retina, suggesting that only the VN retina was associated with colour sensitivity. Behavioural tests further demonstrated that anchovies could discriminate colour and the polarization of light using the ventral retina. Thus, in analogy with the visual system of some invertebrates, the northern anchovy has a retina with segregated retinal pathways for colour and polarization vision. DOI
47. Iwanicki, TW; Flamarique, IN; Ausio, J; Morris, E; Taylor, JS. (2017) Fine-tuning light sensitivity in the starry flounder (Platichthys stellatus) retina: Regional variation in photoreceptor cell morphology and opsin gene expression.J. Comp. Neurol. 525: 2328-2342 Fine-tuning light sensitivity in the starry flounder (Platichthys stellatus) retina: Regional variation in photoreceptor cell morphology and opsin gene expression
chromophore; cone; flatfish; histochemistry; microspectrophotometry; rod; visual pigment
Vertebrate color vision relies on the differential expression of visual pigment proteins (opsins) in cone photoreceptors of the retina. The diversity of opsins and their retinal expression patterns appear greatest for animals that experience variable light habitats, as is the case with flatfishes. Yet, opsin repertoires and expression patterns in this group of fishes are poorly described. Here, we unveil the visual opsin expression patterns of juvenile starry flounder (Platichthys stellatus) and describe the localization of cone types, their visual pigments and opsin expression. Juvenile starry flounder express eight opsins (Rh1, Sws1, Sws2A1, Sws2A2, Sws2B, Rh2A1, Rh2A2, Lws) and possess a corresponding number of photoreceptor visual pigments, with peak absorbance ranging from 369 to 557 nm. Retinal (vitamin A1) was the only chromophore detected in the retina. Intraretinal variation in opsin abundance consisted of greater expression of both RH2, and lesser expression of SWS1 and both SWS2A, opsin transcripts in the dorsal compared to the ventral retina. Overall cone density was greater in the dorsal retina which was also characterized by a larger proportion of unequal double cones compared with the ventral retina. Together, our results suggest that large opsin repertoires serve to optimize visual function under variable light environments by differential expression of opsin subsets with retinal location. DOI
46. Flamarique, IN. (2016) Diminished foraging performance of a mutant zebrafish with reduced population of ultraviolet cones.Proceedings of the Royal Society B-Biological Sciences 283 Diminished foraging performance of a mutant zebrafish with reduced population of ultraviolet cones
ultraviolet cone; retina; foraging; zebrafish
Ultraviolet (UV) cones are photoreceptors that sense light in the range 300-450 nm and are found in the retinas of non-mammalian vertebrates and small mammals. Despite their widespread presence across taxa, the functions that these cones exert in the lives of animals remain largely unknown. In this study, I used the zebrafish for (lots of rods) mutant, characterized by a diminished UV cone population compared to that of wild-type zebrafish, to test whether its foraging performance differed from that of the wild-type (control). The mean location distance and angle (variables that are reliable indicators of foraging performance) at which control fish detected zooplankton prey were, on average, 24 and 90% greater than corresponding measures for for fish. Such inferior foraging performance of the mutant could be explained by reduced contrast perception of the prey, resulting from the diminished population of UV cones and associated sensitivity. Thus, UV cones enhance the foraging performance of zebrafish, a crucial ecological function that may explain why small zooplanktivorous fishes retain UV cones throughout their lives. DOI
45. Flamarique, IN; Wachowiak, M. (2015) Functional segregation of retinal ganglion cell projections to the optic tectum of rainbow trout.Journal of Neurophysiology 114: 2703-2717 Functional segregation of retinal ganglion cell projections to the optic tectum of rainbow trout
cone mechanism; fish retina; retinotectal projections; ultraviolet cone; voltage-sensitive dye
The interpretation of visual information relies on precise maps of retinal representation in the brain coupled with local circuitry that encodes specific features of the visual scenery. In nonmammalian vertebrates, the main target of ganglion cell projections is the optic tectum. Although the topography of retinotectal projections has been documented for several species, the spatiotemporal patterns of activity and how these depend on background adaptation have not been explored. In this study, we used a combination of electrical and optical recordings to reveal a retinotectal map of ganglion cell projections to the optic tectum of rainbow trout and characterized the spatial and chromatic distribution of ganglion cell fibers coding for increments (ON) and decrements (OFF) of light. Recordings of optic nerve activity under various adapting light backgrounds, which isolated the input of different cone mechanisms, yielded dynamic patterns of ON and OFF input characterized by segregation of these two fiber types. Chromatic adaptation decreased the sensitivity and response latency of affected cone mechanisms, revealing their variable contributions to the ON and OFF responses. Our experiments further demonstrated restricted input from a UV cone mechanism to the anterolateral optic tectum, in accordance with the limited presence of UV cones in the dorsotemporal retina of juvenile rainbow trout. Together, our findings show that retinal inputs to the optic tectum of this species are not homogeneous, exhibit highly dynamic activity patterns, and are likely determined by a combination of biased projections and specific retinal cell distributions and their activity states. DOI
44. Suliman, T; Flamarique, IN. (2014) Visual Pigments and Opsin Expression in the Juveniles of Three Species of Fish (Rainbow Trout, Zebrafish, and Killifish) Following Prolonged Exposure to Thyroid Hormone or Retinoic Acid.Journal of Comparative Neurology 522: 98-117 Visual Pigments and Opsin Expression in the Juveniles of Three Species of Fish (Rainbow Trout, Zebrafish, and Killifish) Following Prolonged Exposure to Thyroid Hormone or Retinoic Acid
photoreceptor; retina; immunohistochemistry; in situ hybridization; microspectrophotometry
Thyroid hormone (TH) and retinoic acid (RA) are powerful modulators of photoreceptor differentiation during vertebrate retinal development. In the embryos and young juveniles of salmonid fishes and rodents, TH induces switches in opsin expression within individual cones, a phenomenon that also occurs in adult rodents following prolonged (12 week) hypothyroidism. Whether changes in TH levels also modulate opsin expression in the differentiated retina of fish is unknown. Like TH, RA is essential for retinal development, but its role in inducing opsin switches, if any, has not been studied. Here we investigate the action of TH and RA on single-cone opsin expression in juvenile rainbow trout, zebrafish, and killifish and on the absorbance of visual pigments in rainbow trout and zebrafish. Prolonged TH exposure increased the wavelength of maximum absorbance ((max)) of the rod and the medium (M, green) and long (L, red) wavelength visual pigments in all fish species examined. However, unlike the opsin switch that occurred following TH exposure in the single cones of small juvenile rainbow trout (alevin), opsin expression in large juvenile rainbow trout (smolt), zebrafish, or killifish remained unchanged. RA did not induce any opsin switches or change the visual pigment absorbance of photoreceptors. Neither ligand altered cone photoreceptor densities. We conclude that RA has no effect on opsin expression or visual pigment properties in the differentiated retina of these fishes. In contrast, TH affected both single-cone opsin expression and visual pigment absorbance in the rainbow trout alevin but only visual pigment absorbance in the smolt and in zebrafish. The latter results could be explained by a combination of opsin switches and chromophore shifts from vitamin A1 to vitamin A2. J. Comp. Neurol. 522:98-117, 2014. (c) 2013 Wiley Periodicals, Inc. DOI
43. Tarboush, R; Flamarique, IN; Chapman, GB; Connaughton, VP. (2014) Variability in mitochondria of zebrafish photoreceptor ellipsoids.Visual Neuroscience 31: 11-23 Variability in mitochondria of zebrafish photoreceptor ellipsoids
Retina; Development; Inner segment
Ultrastructural examination of photoreceptor inner segment ellipsoids in larval (4, 8, and 15 days postfertilization; dpf) and adult zebrafish identified morphologically different types of mitochondria. All photoreceptors had mitochondria of different sizes (large and small). At 4 dpf, rods had small, moderately stained electron-dense mitochondria (E-DM), and two cone types could be distinguished: (1) those with electron-lucent mitochondria (E-LM) and (2) those with mitochondria of moderate electron density. These distinctions were also apparent at later ages (8 and 15 dpf). Rods from adult fish had fewer mitochondria than their corresponding cones. The ellipsoids of some fully differentiated single and double cones contained large E-DM with few cristae; these were surrounded by small E-LM with typical internal morphology. The mitochondria within the ellipsoids of other single cones showed similar electron density. Microspectrophotometry of cone ellipsoids from adult fish indicated that the large E-DM had a small absorbance peak (similar to 0.03 OD units) and did not contain cytochrome-c, but crocetin, a carotenoid found in old world monkeys. Crocetin functions to prevent oxidative damage to photoreceptors, suggesting that the ellipsoid mitochondria in adult zebrafish cones protect against apoptosis and function metabolically, rather than as a light filter. DOI
42. Flamarique, IN. (2013) Opsin switch reveals function of the ultraviolet cone in fish foraging.Proceedings of the Royal Society B-Biological Sciences 280: Opsin switch reveals function of the ultraviolet cone in fish foraging
visual pigment; cone photoreceptor; retina; rainbow trout
Although several studies have shown that ultraviolet (UV) wavelengths are important in naturally occurring, visually guided behaviours of vertebrates, the function of the UV cone in such behaviours is unknown. Here, I used thyroid hormone to transform the UV cones of young rainbow trout into blue cones, a phenomenon that occurs naturally as the animal grows, to test whether the resulting loss of UV sensitivity affected the animal's foraging performance on Daphnia magna, a prey zooplankton. The distances and angles at which prey were located (variables that are known indicators of foraging performance) were significantly reduced for UV knock-out fish compared with controls. Optical measurements and photon-catch calculations revealed that the contrast of Daphnia was greater when perceived by the visual system of control versus that of thyroid-hormone-treated fish, demonstrating that the UV cone enhanced the foraging performance of young rainbow trout. Because most juvenile fishes have UV cones and feed on zooplankton, this finding has wide implications for understanding the visual ecology of fishes. The enhanced target contrast provided by UV cones could be used by other vertebrates in various behaviours, including foraging, mate selection and communication. DOI
41. Flamarique, IN; Bergstrom, C; Cheng, CL; Reimchen, TE. (2013) Role of the iridescent eye in stickleback female mate choice.Journal of Experimental Biology 216: 2806-2812 Role of the iridescent eye in stickleback female mate choice
PREY-SEARCH BEHAVIOR; GASTEROSTEUS-ACULEATUS; THREESPINE STICKLEBACKS; NUPTIAL COLOR; 3-SPINED STICKLEBACKS; SPECTRAL SENSITIVITY; POLARIZED-LIGHT; VISUAL-SYSTEMS; ULTRAVIOLET; SIGNAL
Many vertebrates exhibit prominent body colours that are used in courtship and territorial communication. Some fishes also have an eye whose iris becomes iridescent during the mating season, as in the threespine stickleback. Behavioural studies in this species have focused on the redness of the throat/jaw as the primary determinant of female mate choice. Unlike the iridescent eye, however, the red throat/jaw is not present in all stickleback populations, suggesting that the colour of the eye may be equally important for female mate choice. Here, we used data on photoreceptors and environmental light to assess body conspicuousness and the colour contrast of courtship signals for stickleback populations living in a range of waters, from clear (mesotrophic) to red light shifted (dystrophic). This analysis indicated that the redness of the throat/jaw is expressed to enhance the contrast of the eye. To test the importance of eye colour as a courtship signal, we carried out mate choice experiments in which females were presented with identical videos of a courting male but for the colour of the eye and/or the throat/jaw. Females did not choose based on differences in throat/jaw redness between videos, but preferred males with the highest contrast between the eye and the throat/jaw. This result points to the blue iridescent eye as a primary courtship signal in stickleback female mate choice. DOI
40. Flamarique, IN; Cheng, CL; Bergstrom, C; Reimchen, TE. (2013) Pronounced heritable variation and limited phenotypic plasticity in visual pigments and opsin expression of threespine stickleback photoreceptors.Journal of Experimental Biology 216: 656-667 Pronounced heritable variation and limited phenotypic plasticity in visual pigments and opsin expression of threespine stickleback photoreceptors
INNER NUCLEAR LAYER; SALMONID FISHES; GASTEROSTEUS-ACULEATUS; CONE PHOTORECEPTORS; BLUEFIN KILLIFISH; LUCANIA-GOODEI; NUPTIAL COLOR; SINGLE CONES; POLARIZED-LIGHT; GENE-EXPRESSION
Vertebrate colour vision is mediated by the differential expression of visual pigment proteins (opsins) in retinal cone photoreceptors. Many species alter opsin expression during life, either as part of development or as a result of changes in habitat. The latter, a result of phenotypic plasticity, appears common among fishes, but its cellular origin and ecological significance are unknown. Here, we used adult threespine stickleback fish from different photic regimes to investigate heritable variability and phenotypic plasticity in opsin expression. Fish from clear waters had double cones that expressed long (LWS) and middle (RH2) wavelength opsins, one per double cone member. In contrast, fish from red light-shifted lakes had double cones that were >95% LWS/LWS pairs. All fish had single cones that predominantly expressed a short wavelength (SWS2) opsin but ultraviolet cones, expressing a SWS1 opsin, were present throughout the retina. Fish from red light-shifted lakes, when transferred to clear waters, had a similar to 2% increase in RH2/LWS double cones, though double cone density remained constant. Comparison of visual pigment absorbance and light transmission in the environment indicated that the opsin complements of double cones maximized sensitivity to the background light, whereas single cones had visual pigments that were spectrally offset from the dominant background wavelengths. Our results indicate that phenotypic plasticity in opsin expression is minor in sticklebacks and of questionable functional significance. DOI
39. Harosi, FI; Flamarique, IN. (2012) Functional significance of the taper of vertebrate cone photoreceptors.Journal of General Physiology 139: 159-187 Functional significance of the taper of vertebrate cone photoreceptors
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. DOI
38. Flamarique, IN. (2011) Unique Photoreceptor Arrangements in a Fish with Polarized Light Discrimination.Journal of Comparative Neurology 519: 714-737 Unique Photoreceptor Arrangements in a Fish with Polarized Light Discrimination
photoreceptor; outer segment; lamella; disk; axial dichroism; cilium; visual pigment; opsin; polarization detection; retinal development; electron microscopy; immunohistochemistry; anchovy; fish
In contrast to other vertebrates, some anchovies have cone photoreceptors with longitudinally oriented outer segment lamellae. These photoreceptors are axially dichroic (i.e., they are sensitive to the polarization of axially incident light) and form the basis of a polarization detection system in the northern anchovy, Engraulis mordax. Whether other cone types exist in the retina of this animal, and whether multiple cone opsins are expressed in the retinas of anchovies, is unknown. Likewise, a detailed examination of photoreceptor ultrastructure in nondichroic photoreceptors has not been carried out despite its importance to understand visual specializations within the retina and its use in the formulation of Models to explain cellular structure. Here, I combined light and electron microscopy with immunohistochemical studies of opsin expression to infer mechanisms of lamellar formation and to evaluate the potential for color vision in the northern anchovy retina. Morphological observations revealed three cone formations: 1) continuous rows made up of alternating long and short (bilobed) cones with longitudinally oriented lamellae that are orthogonal between cone types; 2) continuous rows of alternating long and short cones in which only the short cones have longitudinally oriented lamellae; and 3) rows of triple cones with transversely oriented lamellae, each triple cone consisting of two lateral cones flanking a small central cone. Ultrastructure investigations supported two models of outer segment formation resulting in the longitudinally oriented lamellae of long and short cones. In the case of the long cone, lateral compression of the outer segment, potentially via the formation of guanine platelet stacks in neighboring pigment epithelium cells, results in a shape transformation from conical to cunate and a tilt from transverse to longitudinal lamellae. In the case of the short (bilobed) cone, membrane invaginations from the connecting ciliary structure grow longitudinally to form a dichroic stack. Opsin expression studies indicated that all cones express middle-to-long wavelength opsins, with long and lateral cones possessing a different opsin from that in short and central cones, confirming the potential for color vision. Together with the ultrastructural observations, these results suggest that the unique cone topography in the northern anchovy retina may underlie a visual system with segregated color and polarization detection channels. J. Comp. Neurol. 519:714-737, 2011. (C) 2010 Wiley-Liss, Inc. DOI
37. Gan, KJ; Flamarique, IN. (2010) Thyroid Hormone Accelerates Opsin Expression During Early Photoreceptor Differentiation and Induces Opsin Switching in Differentiated TR alpha-Expressing Cones of the Salmonid Retina.Developmental Dynamics 239: 2700-2713 Thyroid Hormone Accelerates Opsin Expression During Early Photoreceptor Differentiation and Induces Opsin Switching in Differentiated TR alpha-Expressing Cones of the Salmonid Retina
retinal development; photoreceptor differentiation; thyroid hormone; thyroid hormone receptor; opsin expression; cone; rod; in situ hybridization; immunohistochemistry; fish
Thyroid hormone and its receptors (TRs) regulate photoreceptor differentiation and visual pigment protein (opsin) expression in the retinas of several vertebrates, including rodents and fish. In some of these animals, opsin expression can arise through switches within differentiated cone photoreceptors. In salmonid fishes, single cones express ultraviolet (SWS1) opsin during embryonic development and switch to blue (SWS2) opsin as the fishes grow. It is unknown whether thyroid hormone regulates opsin expression during early cone differentiation and acts through TRs to induce opsin switches in differentiated cones of the salmonid retina. Using in situ hybridization, we characterized the spatiotemporal dynamics of opsin expression and switching in embryos treated with exogenous thyroid hormone or propylthiouracil (PTU), a pharmacological inhibitor of thyroid hormone synthesis. We combined immunohistochemistry with in situ hybridization to map TR alpha expression with respect to cones undergoing the opsin switch in older juvenile fish. Thyroid hormone accelerated opsin expression in differentiating cones and induced the opsin switch in differentiated single cones, whereas PTU repressed the opsin switch. TR alpha was not detected in differentiating photoreceptors as opsin expression initiated, but was later expressed in differentiated single cones before the onset of the opsin switch. TR alpha expression exhibited a dynamic dorsoventral distribution that paralleled the progression of the opsin switch. Together, our results show that thyroid hormone is required for opsin switching in the retina of salmonid fishes and suggest that TR alpha may be involved in regulating this phenomenon. Developmental Dynamics 239:2700-2713, 2010. (C) 2010 Wiley-Liss, Inc. DOI
36. Cheng, CL; Gan, KJ; Flamarique, IN. (2009) Thyroid Hormone Induces a Time-Dependent Opsin Switch in the Retina of Salmonid Fishes.Investigative Ophthalmology & Visual Science 50: 3024-3032 Thyroid Hormone Induces a Time-Dependent Opsin Switch in the Retina of Salmonid Fishes
ULTRAVIOLET-SENSITIVE CONES; VERTEBRATE VISUAL PIGMENTS; DEVELOPING MOUSE RETINA; INNER NUCLEAR LAYER; RAINBOW-TROUT; GOLDFISH RETINA; SINGLE CONES; TEMPORAL EXPRESSION; NATURAL DEVELOPMENT; RECEPTOR-ALPHA
PURPOSE. To determine the role of thyroid hormone in inducing the UV (SWS1)-to-blue (SWS2) opsin switch in the retina of two salmonid fishes, the coho salmon (Oncorhynchus kisutch) and the rainbow trout (O. mykiss). METHODS. Fish were treated with thyroid hormone (T 4) or the vehicle solution (0.1 M NaOH, control), exogenously or by intraocular injection, at different life history stages. Microspectrophotometry and in situ hybridization with riboprobes against the SWS1 and SWS2 opsins were used to reveal the dynamics of opsin expression in treated and control animals. To assess whether thyroid hormone induced differentiation of retinal progenitor cells into cones, treated and control fish were injected intraocularly with bromodeoxyuridine (BrdU) and the number of proliferating cells in the outer nuclear layer (ONL) determined. These observations were accompanied by histologic counts of cone densities. RESULTS. Thyroid hormone induced a reversible UV-to-blue opsin switch in differentiated single cones of juvenile salmonids (alevin and parr stages), but failed to exert any effect in the retina of older fish (smolt stage). The switch progressed from the ventral to the dorsal retina in clockwise fashion. Thyroid hormone did not induce cone density changes or alterations in the number of BrdU-labeled cells, which were the same in control and treated animals. CONCLUSIONS. Thyroid hormone induces a UV (SWS1)-to-blue (SWS2) opsin switch in the retina of young salmonid fishes that is identical with that occurring during natural development. The switch occurs in differentiated photoreceptors, is reversible (maintained by thyroid hormone exposure), and can be induced only before its natural onset. Thyroid hormone did not cause changes in the number of proliferating cells in the ONL. These results conform to the dynamics of thyroid hormone-induced opsin expression in the mouse and are consistent with the opsin plasticity found in differentiated photoreceptors of the fruit fly, Drosophila melanogaster. This work establishes a role for thyroid hormone in triggering opsin switches in the vertebrate retina. (Invest Ophthalmol Vis Sci. 2009;50: 3024-3032) DOI:10.1167/iovs.08-2713 DOI
35. Flamarique, IN; Gulbransen, C; Galbraith, M; Stucchi, D. (2009) Monitoring and potential control of sea lice using an LED-based light trap.Canadian Journal of Fisheries and Aquatic Sciences 66: 1371-1382 Monitoring and potential control of sea lice using an LED-based light trap
LEPEOPHTHEIRUS-SALMONIS KROYER; FARMED ATLANTIC SALMON; BRITISH-COLUMBIA; PACIFIC SALMON; SALAR L.; ONCORHYNCHUS-GORBUSCHA; BROUGHTON ARCHIPELAGO; LOUSE INFESTATION; VANCOUVER-ISLAND; WESTERN SCOTLAND
Sea lice are ectoparasitic copepods that threaten salmon farming aquaculture and the viability of wild salmon populations. To control infestations on farmed salmon, several chemotherapeutants have been developed, but these are invasive (often causing fish stress and loss in production), costly, may induce parasite resistance over time, and their impact on the environment is a major social concern. Here, we show that a light-emitting diode (LED)-based light trap can be used to monitor sea lice presence on fish and in the water. The performance of the light trap was tested in experimental tanks and in the ocean. Plankton net tows were also performed to compare catches with those from light traps. The light trap caught similar to 70% of salmon lice larval stages loaded onto a tank and similar to 24% of the adults. It also acted as a delousing agent by removing similar to 8% of adult salmon lice infective on Chinook salmon ( Oncorhynchus tshawytscha) smolts in tank experiments. In the ocean, the light trap caught 21 sea lice (10 Lepeophtheirus salmonis and 11 Caligus clemensi), comprising free-swimming and attached stages, while plankton net tows failed to capture any. We conclude that light traps constitute an effective, noninvasive, environmentally friendly method to monitor sea lice. DOI
34. Cheng, CL; Flamarique, IN. (2007) Chromatic organization of cone photoreceptors in the retina of rainbow trout: single cones irreversibly switch from UV (SWS1) to blue (SWS2) light sensitive opsin during natural development.Journal of Experimental Biology 210: 4123-4135 Chromatic organization of cone photoreceptors in the retina of rainbow trout: single cones irreversibly switch from UV (SWS1) to blue (SWS2) light sensitive opsin during natural development
UV cone; blue cone; double cone; opsin; cone mosaic; retinal development; in situ hybridization; microspectrophotometry; thyroid hormone; fish
The retinas of salmonid fishes have single and double cones arranged in square to row formations termed mosaics. The square mosaic unit is formed by four double cones that make the sides of the square with a single (centre) cone in the middle, and a single (corner) cone at each corner of the square when present. Previous research using coho salmon-derived riboprobes on four species of anadromous Pacific salmon has shown that all single cones express a SWS1 (UV sensitive) visual pigment protein (opsin) at hatching, and that these cones switch to a SWS2 (blue light sensitive) opsin during the juvenile period. Whether this opsin switch applies to non-anadromous species, like the rainbow trout, is under debate as species-specific riboprobes have not been used to study opsin expression during development of a trout. As well, a postulated recovery of SWS1 opsin expression in the retina of adult rainbow trout, perhaps via a reverse process to that occurring in the juvenile, has not been investigated. Here, we used in situ hybridization with species-specific riboprobes and microspectrophotometry on rainbow trout retina to show that: (1) single cones in the juvenile switch opsin expression from SWS1 to SWS2, (2) this switch is not reversed in the adult, i.e. all single cones in the main retina continue to express SWS2 opsin, and (3) opsin switches do not occur in double cones: each member expresses one opsin, maximally sensitive to green (RH2) or red (LWS) light. The opsin switch in the single cones of salmonid fishes may be a general process of chromatic organization that occurs during retinal development of most vertebrates. DOI
33. Cheng, CL; Flamarique, IN. (2007) Photoreceptor distribution in the retina of adult Pacific salmon: Corner cones express blue opsin.Visual Neuroscience 24: 269-276 Photoreceptor distribution in the retina of adult Pacific salmon: Corner cones express blue opsin
ultraviolet opsin; visual pigment; cone mosaic; regeneration; fish retina
The retina of salmonid fishes has two types of cone photoreceptors: single and double cones. At the nuclear level, these cones are distributed in a square mosaic such that the double cones form the sides of the square and the single cones occupy positions at the centre and at the corners of the square. Double cones consist of two members, one having visual pigment protein maximally sensitive to green light (RH2 opsin), the other maximally sensitive to red light (LWS opsin). Single cones can have opsins maximally sensitive to ultraviolet (UV) or blue light (SWS1 and SWS2 opsins. respectively). In Pacific salmonids, all single cones express UV opsin at hatching. Around the time of yolk sac absorption, single cones start switching opsin expression from UV to blue, in an event that proceeds from the ventral to the dorsal retina. This transformation is accompanied by a loss of single corner cones such that the large juvenile shows corner cones and UV opsin expression in the dorsal retina only. Previous research has shown that adult Pacific salmon have corner cones over large areas of retina suggesting that these cones may be regenerated and that they may express UV opsin. Here we used in-situ hybridization with cRNA probes and RT-PCR to show that: (I) all single cones in non-growth zone areas of the retina express blue opsin and (2) double cone opsin expression alternates around the square mosaic unit. Our results indicate that single cone driven UV sensitivity in adult salmon must emanate from stimulation of growth zone areas. DOI
32. Cheng, CL; Gan, KJ; Flamarique, IN. (2007) The ultraviolet opsin is the first opsin expressed during retinal development of salmonid fishes.Investigative Ophthalmology & Visual Science 48: 866-873 The ultraviolet opsin is the first opsin expressed during retinal development of salmonid fishes
PURPOSE. To determine the spatial and temporal progression of opsin appearance during retinal development of salmonid fishes (genus Oncorhynchus and Salmo). METHODS. Reverse transcription-polymerase chain reaction (RT-PCR) and in situ hybridization with riboprobes against the five classes of opsins present in salmonids (UV, blue, green, red, and rhodopsin) were used to establish the sequence of opsin appearance and the localization of opsins to specific morphologic photoreceptor types. RESULTS. Both detection methods revealed that UV opsin mRNA was expressed first and was followed closely by red opsin mRNA. In situ hybridization results indicated the following opsin sequence: UV, red, rhodopsin, green, and blue. The UV opsin riboprobe labeled single cones, whereas the red and green riboprobes labeled opposite members of double cones. The blue riboprobe started labeling single center cones similar to 1 month after initial UV riboprobe labeling, confirming a switch in opsin expression of these cones from UV to blue. All probes first labeled a small patch of cells in the centrotemporal retina, and expression then expanded primarily toward the temporal and dorsal retina, with the exception of the blue opsin which expanded ventrally at first. CONCLUSIONS. The sequence of cone opsin appearance in salmonid fishes is similar to that in mammals, in which a violet-blue (SWS1) opsin is expressed first followed by a red (M/LWS) opsin. This sequence is different from that in zebrafish, goldfish, and chick, in which red and green opsins are expressed first. As in mammals, rhodopsin expression in salmonid fishes arises after the first cone opsin. The findings show similarity in the sequence of opsin expression between a group of lower vertebrates, the salmonid fishes, and mammals. DOI
31. Flamarique, IN; Mueller, GA; Cheng, CL; Figiel, CR. (2007) Communication using eye roll reflective signalling.Proceedings of the Royal Society B-Biological Sciences 274: 877-882 Communication using eye roll reflective signalling
visual communication; ultraviolet cones; sucker; territoriality
Body reflections in the ultraviolet (UV) are a common occurrence in nature. Despite the abundance of such signals and the presence of UV cones in the retinas of many vertebrates, the function of UV cones in the majority of taxa remains unclear. Here, we report on an unusual communication system in the razorback sucker, Xyrauchen texanus, that involves flash signals produced by quick eye rolls. Behavioural experiments and field observations indicate that this form of communication is used to signal territorial presence between males. The flash signal shows highest contrast in the UV region of the visual spectrum (lambda(max) similar to 380 nm), corresponding to the maximum wavelength of absorption of the UV cone mechanism in suckers. Furthermore, these cones are restricted to the dorsal retina of the animal and the upwelling light background is such that their relative sensitivity would be enhanced by chromatic adaptation of the other cone mechanisms. Thus, the UV cones in the sucker have optimal characteristics (both in terms of absorbance and retinal topography) to constitute the main detectors of the flash signal. Our findings provide the first ecological evidence for restricted distribution of UV cones in the retina of a vertebrate. DOI
30. Cheng, CL; Flamarique, IN; Harosi, FI; Rickers-Haunerland, J; Haunerland, NH. (2006) Photoreceptor layer of salmonid fishes: Transformation and loss of single cones in juvenile fish.J Comp Neurol 495: 213-235 Photoreceptor layer of salmonid fishes: Transformation and loss of single cones in juvenile fish
UV cone; blue cone; opsin; apoptosis; cone mosaic; retinal development
The retinas of many vertebrates have cone photoreceptors that express multiple visual pigments. In many of these animals, including humans, the original cones to appear in the retina (which express UV or blue opsin) may change opsin types, giving rise to new spectral phenotypes. Here we used microspectrophotometry and in situ hybridization with cDNA probes to study the distribution of UV and blue cones in the retinas of four species of Pacific salmon (coho, chum, chinook, and pink salmon), in the Atlantic salmon, and in the rainbow/ steelhead trout. In Pacific salmon and in the trout, all single cones express a UV opsin at hatching lambda(max) of the visual pigment similar to 365 nm), and these cones later transform into blue cones by opsin changeover (lambda(max) of the blue visual pigment similar to 434 nm). Cones undergoing UV opsin downregulation exhibit either of two spectral absorbance profiles. The first is characterized by UV and blue absorbance peaks, with blue absorbance dominating the base of the outer segment. The second shows U-V absorbance diminishing from the outer segment tip to the base, with no sign of blue absorbance. The first absorbance profile indicates a transformation from U-V to blue phenotype by opsin changeover, while the second type suggests that the cone is undergoing apoptosis. These two events (transformation and loss of corner cones) are closely associated in time and progress from ventral to dorsal retina. Each double cone member contains green (lambda(max) similar to 510 nm) or red (lambda(max) similar to 565 nm) visual pigment (double cones are green/red pairs), and, like the rods (lambda(max) similar to 508 nm), do not exhibit opsin changeover. Unlike Pacific salmonids, the Atlantic salmon shows a mixture of ILTV and blue cones and a partial loss of corner cones at hatching. This study establishes the UV-to-blue cone transformation as a general feature of retinal growth in Pacific salmonids (genus Oncorhynchus).
29. Flamarique, IN; Hiebert, S; Sechrist, J. (2006) Visual performance and ocular system structure of kokanee and sockeye salmon following strobe light exposure.N Am J Fish Manage 26: 453-459 Visual performance and ocular system structure of kokanee and sockeye salmon following strobe light exposure
The use of flashing strobe lights to deter salmon from dam intakes and other hazardous underwater structures has become an appealing method for reducing salmon mortalities. However, no research has been carried out to determine how strobe light emission could affect the visual system of salmonid fishes. The present study investigated behavioral and ocular system changes after short-term (1- and 5-min) and longterm (3-h) exposure of kokanee and sockeye salmon (the lacustrine and anadromous forms of Oncorhynchus nerka). The onset of the escape response to an overhead shadow was different between treatments. Fish exposed for 1 or 5 min showed a response within 5 and 25 min of treatment, respectively, whereas the 3-hexposed sockeye salmon responded a minimum of 64 h postexposure. All the retinas and lenses examined showed the same characteristics regardless of treatment. We conclude from these results that strobe exposure for 1 min or more induces a state of torpor in sockeye salmon, but exposure for no longer than 5 min does not induce permanent damage to the ocular system.
28. Flamarique, IN. (2005) Temporal shifts in visual pigment absorbance in the retina of Pacific salmon.Journal of Comparative Physiology A-Neuroethology Sensory Neural and Behavioral Physiology 191: 37-49 Temporal shifts in visual pigment absorbance in the retina of Pacific salmon
visual pigment; chromophore; photoreceptor; microspectrophotometry; retina
The visual pigments and photoreceptor types in the retinas of three species of Pacific salmon (coho, chum, and chinook) were examined using microspectrophotometry and histological sections for light microscopy. All three species had four cone visual pigments with maximum absorbance in the UV (lambda(max): 357 382 nm), blue (lambda(max): 431 - 446 nm), green (lambda(max): 490 - 553 nm) and red (lambda(max): 548 - 607 nm) parts of the spectrum, and a rod visual pigment with lambda(max): 504 - 531 nm. The youngest fish (yolk-sac alevins) did not have blue visual pigment, but only UV pigment in the single cones. Older juveniles (smolts) had predominantly single cones with blue visual pigment. Coho and chinook smolts (> 1 year old) switched from a vitamin A(1)- to a vitamin A(2)-dominated retina during the spring, while the retina of chum smolts and that of the younger alevin-to-parr coho did not. Adult spawners caught during the Fall had vitamin A(2)- dominated retinas. The central retina of all species had three types of double cones ( large, medium and small). The small double cones were situated toward the ventral retina and had lower red visual pigment lambda(max) than that of medium and large double cones, which were found more dorsally. Temperature affected visual pigment lambda(max) during smoltification.
26. Flamarique, IN. (2002) Partial re-incorporation of corner cones in the retina of the Atlantic salmon (Salmo salar).Vision Research 42: 2737-2745 Partial re-incorporation of corner cones in the retina of the Atlantic salmon (Salmo salar)
ultraviolet cone; cone mosaic; visual acuity; smoltification; salmonid fish
The distribution of corner (putative ultraviolet-sensitive) cones in the retina of Atlantic salmon was examined from the small juvenile (parr) stage to the adult stage (approaching sexual maturation). Small parr weighing similar to5 g lacked corner cones everywhere except, mainly, near the dorsal periphery. Large fish (similar to5 kg) approaching sexual maturation showed corner cones in other areas of the dorsal retina besides the periphery. These areas, characterized by low resolving power, had similar corner corn densities to analogous areas in the smolt retina, suggesting that corner cones are formed in the periphery and incorporated into the dorsal retina of the Atlantic salmon sometime during the smolt stage. This incorporation is partial both in numbers of cones and in location (only the dorsal retina is affected). These findings contrast with the situation in rainbow trout where corner cones from existing mosaics are only partially lost from the ventral retina, if at all, and where production and incorporation of these cones into the dorsal retina occurs throughout life. Thus, in salmonids, there are at least two different strategies that determine retinal corner cone distributions. (C) 2002 Elsevier Science Ltd. All rights reserved.
25. Flamarique, IN. (2002) A novel function for the pineal organ in the control of swim depth in the Atlantic halibut larva.Naturwissenschaften 89: 163-166 A novel function for the pineal organ in the control of swim depth in the Atlantic halibut larva
The pineal organ of vertebrates is a photo-sensitive structure that conveys photoperiod information to the brain. This information influences circadian rhythm and related metabolic processes such as thermoregulation, hatching time, body growth, and the timing of reproduction. This study demonstrates extra-ocular light responses that control swim depth in the larva of the Atlantic halibut, Hyppoglosus hyppoglosus. Young larvae without a functional eye (<29 days) swim upwards after an average delay of 5 s following the onset of a downwelling light stimulus, but sink downwards a few seconds later. Older larvae (greater than or equal to29 days), which possess a functional eye, swim immediately downwards (microsecond delay) following the onset of the light stimulus, but proceed to swim upwards several seconds later. These two response patterns are thus opposite in polarity and have different time kinetics, Because the pineal organ of the Atlantic halibut develops during the embryonic stage, and because it is the only centre in the brain that expresses functional visual pigments (opsins) at early larval stages, it is the only photosensory organ capable of generating the extra-ocular responses observed.
24. Flamarique, IN; Harosi, FI. (2002) Visual pigments and dichroism of anchovy cones: A model system for polarization detection.Visual Neuroscience 19: 467-473 Visual pigments and dichroism of anchovy cones: A model system for polarization detection.
polarization; photoreceptor; cone; rod; dichroism; retina; visual pigment; fish
The retinas of anchovies have two unique photoreceptor types: "bifid" and "long" cones (Fineran & Nicol, 1976). The outer segments of these cells contain multiple layers of membranes (lamellae) oriented longitudinally (axially). This orientation is distinct from that in all other vertebrate rods and cones, where the lamellae are stacked transversely with their planes perpendicular to the incident light path. Although the common arrangement provides optimal absorption for normally incident light rays, it is also insensitive to the rays' direction of vibration (i.e. their polarization). In contrast, the two mutually perpendicular sets of axially oriented lamellae segregated into bifid and long cones could function as the principal analyzers for linearly polarized light, as previously hypothesized (Fineran & Nicol, 1976, 1978). Here, we report on a microspectrophotometric study that shows (1) the presence of two spectrally distinct visual pigments in the three photoreceptor types of the bay anchovy retina; these are typical vertebrate pigments in that they bleach, when exposed to light, and have absorption spectra like all other vitamin A(1)-based visual pigments; (2) that the rods and cones exhibit dichroic absorption of light in accordance with their lamellar orientation, and (3) that the two cone types of the retina contain a spectrally indistinguishable pigment with peak absorbance (lambda(max)) around 540 nm, while the rods contain a rhodopsin-like pigment with lambda(max) near 500 nm. Compared to other vertebrates, anchovies are remarkable for using a monochromatic cone system with unusual specializations supportive of a polarization detection system.
23. Flamarique, IN. (2001) Gradual and partial loss of corner cone-occupied area in the retina of rainbow trout.Vision Research 41: 3073-3082 Gradual and partial loss of corner cone-occupied area in the retina of rainbow trout
ultraviolet cone; cone mosaic; smoltification; histology; salmonid fish
Several Studies have indicated that the rainbow trout (Oncorhynchus mykiss) loses ultraviolet (UV) sensitivity and the associated UV-sensitive corner cones when the animal transforms from a small (parr) juvenile to a larger, silver-coloured, smolt. Similar changes supposedly take place when parr juveniles are treated with thyroid hormone (T-4) or retinoic acid. In contrast to previous investigations, this study shows that parr juveniles lack corner cones throughout the lower half of the ventral retina, suggesting that corner cones cease to be incorporated into the ventral retina some time after hatching. This uneven incorporation of corner cones across the retina, when combined with retinal growth, creates a progressively smaller area of lower retina occupied by corner cones. Because in previous studies, the stimulating illumination was directed primarily at the ventral retina, the reported age-dependent changes in UV or polarization sensitivities can be explained by differences in the area of corner cones that was illuminated, and not necessarily by a loss of corner cones. This study also shows: (1) that the double cones from non-ventral mosaics of parr rainbow trout may change in cross-sectional shape, altering the mosaic formation from a square to a row, (2) the existence of a 'pure' (non-changing) square mosaic in the ventral retina, and (3) a potential method. based on differential staining of cone nuclei, to classify paired cones into double or twin cones. (C) 2001 Elsevier Science Ltd. All rights reserved.
22. Flamarique, IN; Browman, HI. (2001) Foraging and prey-search behaviour of small juvenile rainbow trout (Oncorhynchus mykiss) under polarized light.Journal of Experimental Biology 204: 2415-2422 Foraging and prey-search behaviour of small juvenile rainbow trout (Oncorhynchus mykiss) under polarized light
polarization; salmonid; rainbow trout; Oncorhynchus mykiss; zooplankton; ultraviolet light; target contrast; foraging; prey-search behaviour
Several fish species appear to be polarization sensitive, i.e. to be able to discriminate a light source's maximum plane of polarization from any other plane. However, the functional significance of this ability remains unclear. We tested the hypothesis that polarized light improves the prey location ability of free-swimming rainbow trout (Oncorhynchus mykiss) in laboratory aquaria. We found that prey location distances increased while the vertical component of prey location angle decreased under polarized compared with unpolarized (diffuse) illumination. The average frequency distribution of the horizontal component of prey location angle was more bimodal under polarized than unpolarized illumination. These results indicate that polarization sensitivity enhances prey location by juvenile rainbow trout.
19. Flamarique, IN; Browman, HI. (2000) Wavelength-dependent polarization orientation in Daphnia.Journal of Comparative Physiology A-Neuroethology Sensory Neural and Behavioral Physiology 186: 1073-1087 Wavelength-dependent polarization orientation in Daphnia
polarotaxis; crustacean; visual pigments; rhabdom; Daphnia
The ability to detect and use the polarization of light for orientation is widespread among invertebrates. Among terrestrial insects, the retinula cells that are responsible for polarization detection contain a single visual pigment, either ultraviolet or short (blue) wavelength sensitive. With the exception of a few aquatic insects, the visual pigments underlying polarization sensitivity in aquatic invertebrates have yet to be determined. Here we report that polarotaxis in Daphnia pulex, a freshwater crustacean, is wavelength dependent and most likely mediated by two visual pigments with absorbance maxima in the middle (green) and long wavelength (red) parts of the spectrum. This contrasts with the response of a closely related species, D. magna, in which polarotaxis is wavelength independent and based on a single middle wavelength visual pigment. The visual systems in Daphnia are the first among crustaceans shown to utilize a middle wavelength pigment for polarization detection and, in the case of D. pulex, the first shown to use more than one visual Figment for such a purpose.
18. Flamarique, IN; Browman, HI; Belanger, M; Boxaspen, K. (2000) Ontogenetic changes in visual sensitivity of the parasitic salmon louse Lepeophtheirus salmonis.Journal of Experimental Biology 203 Ontogenetic changes in visual sensitivity of the parasitic salmon louse Lepeophtheirus salmonis
copepod; Lepeophtheirus salmonis; fish parasite; spectral sensitivity; ON/OFF response; aquaculture
6. Flamarique, IN; Hawryshyn, CW. (1996) Retinal development and visual sensitivity of young Pacific sockeye salmon (Oncorhynchus nerka).Journal of Experimental Biology 199 Retinal development and visual sensitivity of young Pacific sockeye salmon (Oncorhynchus nerka)
sockeye salmon; Oncorhynchus nerka; retina; development; spectral and polarized light; sensitivities; ultraviolet cones
1. NOVALES FLAMARIQUE, I; HENDRY, A; HAWRYSHYN, CW. (1992) THE PHOTIC ENVIRONMENT OF A SALMONID NURSERY LAKE.Journal of Experimental Biology 169 THE PHOTIC ENVIRONMENT OF A SALMONID NURSERY LAKE
SPECTRAL IRRADIANCE; ULTRAVIOLET LIGHT; PHOTORECEPTOR; PHYTOPLANKTON; SALMONIDS; NURSERY LAKE
