Polarisation Vision of Fishes

  • Nicholas William RobertsEmail author
Part of the Springer Series in Vision Research book series (SSVR, volume 2)


Since the first edition of this book, our understanding of vertebrate polarisation vision has increased significantly. Much of this work has concentrated on a number of species of fish, and the aim of this updated chapter is to highlight some of the new discoveries and new directions this area of animal polarisation vision has seen. Three distinctive research directions stand out and form the main sections of this chapter update: (1) mechanisms of polarisation sensitivity, (2) neural processing of polarisation information and (3) behavioural evidence of polarisation vision and associated visual ecology. The new additions to this chapter bring together work on molecular mechanisms of dichroism in cone photoreceptors and new evidence that questions the original measures of the levels of diffusion of the visual pigment in outer segment membranes. Advances in our understanding of how intra-retinal feedback influences the neural coding of polarisation information are also considered. Finally, several studies into the ability of fish to react to dynamic polarisation-based stimuli are also presented in conjunction with evidence that some fish also manipulate the degree of polarisation in the light that they reflect. However, it is still clear that this area of research lacks depth in much of the evidence, leaving many questions still wide open for future studies.


Atlantic Salmon Outer Segment Visual Pigment Horizontal Cell Double Cone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Supplementary material (4.4 mb)
Colour Version of Fig. 9.1 The retinal specialisation in the northern anchovy, Engraulis mordax. (a) The right eye with the arrows D and T depicting the dorsal and temporal directions, respectively (scale bar = 2.2 mm). (b) Cone densities [×103 mm−2] across the retina (top number), and percentage packing (bottom number). (c, d, e, f) Schematic of the cone type distributions in the retina colour matched with cartoons of the cone morphology. (g) The anchovy long cones with vertically oriented lamellae (scale bar = 5 μm). Note that the base of the outer segment is laterally displaced towards the temporal side of the inner segment (double black arrowheads). (h) Higher magnification view of the vertically orientated lamellae from a long cone outer segments (scale bar = 0.5 μm). At this level, the black arrowhead shows the closed ends of the lamellae on the right (temporal) side of the outer segment. On the other side (white arrow head) the membranes run parallel to the plasma membrane. (i) Confocal images from whole-mount retina showing opsin expression in the rows of alternating long and short (bilobed) cones. The outer segments of long cones label with two types of M/LWS opsin antibodies (dark grey colour), but the bilobed outer segments label exclusively with the mouse rod opsin antibody (light grey colour) [adapted from Novales-Flamarique (2011)] (TIFF 12152 kb) (487 kb)
Colour Version of Fig. 9.2 Rhodopsin dimerisation in photoreceptor membranes. (a) Atomic force microscopy image of rod outer segment discs illustrating the homodimer ordering of rhodopsin into a paracrystalline array. Insets are X-ray diffraction profiles with the peaks detailing the protein–protein interaction distances [adapted from Fotiadis et al. (2003)]. (b) Similar evidence of phase separation in the plane of the discs taken by a transmission electron microscope [adapted from Corless et al. (1994)]. (c) A calculated top view of a photoactivated rhodopsin dimer taken from the cytoplasmic side. This cytoplasmic surface of photoactivated rhodopsin, Rho*, and rhodopsin, Rho, interacts with the G protein transducin [adapted from Palczewski (2006)] (TIFF 15658 kb) (4.1 mb)
Colour Version of Fig. 9.6 Weakly polarising guanine-based multilayer reflectors in fish. (a) Measurements of the degree of polarisation at λ = 600 nm for azimuthal (dorsoventral; grey cardinal crosses) angles of illumination from Clupea harengus. Solid grey line is a parametric best fit for multilayer model with a mixture of 75 % Type 1 and 25 % Type 2 crystals. The model explained 95 % of the variation in the data, assessed by the R 2 from linear regression. There was no systematic difference between model and data (mean pairwise difference and standard deviation = 0.0044 ± 0.0132, t = 0.7512, d.f. = 9, p = 0.472). The best fit parameters are N = 37 crystal layers in each multilayer structure, with sampling intervals for guanine and cytoplasm thicknesses of [55, 110] nm and [30, 300] nm, respectively. Black solid circles and black line represent a positive control and are experimental data and a theoretical curve for a double surface Fresnel reflection (front and back reflection) from a glass microscope slide with a refractive index of 1.5, in air. (b) Schematic illustrating the multilayer model used and the two populations of guanine crystals: Type 1 crystals (dark grey) and Type 2 crystals (light grey). The orientation of the principle refractive indices’ coordinate axes in each crystal layer are indicated [adapted from Jordan et al. (2012)] (TIFF 12566 kb)


  1. Boesze-Battaglia K, Schimmel RJ (1997) Cell membrane lipid composition and distribution: implications for cell function and lessons learned from photoreceptors and platelets. J Exp Biol 200:2927–2936PubMedGoogle Scholar
  2. Born M, Wolf E (1999) Principles of optics, 7th edn. Cambridge University Press, Cambridge, UKCrossRefGoogle Scholar
  3. Botelho A, Wang Y, Gibson N, Brown M (2006) Membrane bilayer properties influence photoactivation of rhodopsin. Biophys J 78:198–210Google Scholar
  4. Brady PC, Travis KA, Maginnis T, Cummings ME (2013) Polaro-cryptic mirror of the lookdown as a biological model for open ocean camouflage. Proc Natl Acad Sci USA 110:9764–9769PubMedCrossRefPubMedCentralGoogle Scholar
  5. Browman HI, Skiftesvik AB, Kuhn P (2006) The relationship between ultraviolet and polarized light and growth rate in the early larval stages of turbot (Scophtalmus maximus), Atlantic cod (Gadus morhua) and Atlantic herring (Clupea harengus) reared in intensive culture conditions. Aquaculture 256:296–301CrossRefGoogle Scholar
  6. Bruckert F, Chabre M, Vuong TM (1992) Kinetic analysis of the activation of transducin by photoexcited rhodopsin: influence of the lateral diffusion of transducin and competition of guanosine diphosphate and guanosine triphosphate for the nucleotide site. Biophys J 63:616–629PubMedCrossRefPubMedCentralGoogle Scholar
  7. Brzustowicz MR, Stillwell W, Wassall SR (1999) Molecular organization in polyunsaturated phospholipid membranes: a solid state 2H NMR investigation. FEBS Lett 451:197–202PubMedCrossRefGoogle Scholar
  8. Cone RA (1972) Rotational diffusion of rhodopsin in visual receptor membrane. Nat New Biol 236:39–43PubMedCrossRefGoogle Scholar
  9. Corless JM, Worniallo E, Fetter RD (1994) 3-dimensional membrane crystals in amphibian cone outer segments. I. Light-dependent crystal-formation in frog retinas. J Struct Biol 113:64–86PubMedCrossRefGoogle Scholar
  10. Corless J, Worniallo E, Schneider T (1995) 3-dimensional membrane crystals in amphibian cone outer segments. II. Crystal type associated with the saddle-point regions of cone disks. J Struct Biol 61:335–349Google Scholar
  11. Dell-Orco D (2013) A physiological role for the supramolecular organization of rhodopsin and transducin in rod photoreceptors. FEBS Lett 587:2060–2066CrossRefGoogle Scholar
  12. Denton EJ, Nicol JAC (1965) Polarization of light reflected from the silvery exterior of the bleak, Alburnus alburnus. J Mar Biol Assoc UK 45:705–709CrossRefGoogle Scholar
  13. Douglas RH, Hawryshyn CW (1990) Behavioural studies of fish vision: an analysis of visual capabilities. In: Douglas RH, Djamgoz MBA (eds) The visual system of fish. Chapman and Hall, New York, pp 373–418CrossRefGoogle Scholar
  14. Fahrenfort I, Sjoerdsma T, Ripps H, Kamermans M (2004) Cobalt ions inhibit negative feedback in the outer retina by blocking hemichannels on horizontal cells. Vis Neurosci 21:501–511PubMedCrossRefGoogle Scholar
  15. Fineran BA, Nicol JAC (1978) Studies on the photoreceptors of Anchoa mitchilli and A. Hepsetus (Engraulidae) with particular reference to the cones. Philos Trans R Soc Lond B 283:25–60CrossRefGoogle Scholar
  16. Firsov ML, Govardovskii VI, Donner K (1994) Response univariance in bull-frog rods with two visual pigments. Vis Res 34:839–847PubMedCrossRefGoogle Scholar
  17. Fotiadis D, Liang Y, Filipek S, Saperstein D, Engel A, Palczewski K (2003) Atomic-force microscopy: rhodopsin dimers in native disc membranes. Nature 421:127–128PubMedCrossRefGoogle Scholar
  18. George S, O’Dowd B, Lee S (2002) G-protein-coupled receptor oligomerization and its potential for drug discovery. Nat Rev Drug Discov 1:808–820PubMedCrossRefGoogle Scholar
  19. Govardovskii VI, Korenyak DA, Shukolyukov SA, Zueva LV (2009) Lateral diffusion of rhodopsin in photoreceptor membrane: a reappraisal. Mol Vis 15:1717–1729PubMedPubMedCentralGoogle Scholar
  20. Gupta BD, Williams TP (1990) Lateral diffusion of visual pigments in toad (Bufo marinus) rods and in catfish (Ictalurus punctatus) cones. J Physiol 430:483–496PubMedPubMedCentralGoogle Scholar
  21. Hárosi FI (1981) Microspectrophotometry and optical phenomena: birefringence, dichroism and anomalous dispersion. In: Enoch JM, Tobey FL (eds) Vertebrate photoreceptor optics. Berlin, Springer, pp 337–399CrossRefGoogle Scholar
  22. Hawryshyn CW (2010) Ultraviolet polarization vision and visually guided behavior in fishes. Brain Behav Evol 75:186–194PubMedCrossRefGoogle Scholar
  23. Hawryshyn CW, McFarland WN (1987) Cone photoreceptor mechanisms and the detection of polarized light in fish. J Comp Physiol A 160:459–465CrossRefGoogle Scholar
  24. Hawryshyn CW, Moyer HD, Allison WT, Haimberger TJ, McFarland WN (2003) Multidi- mensional polarization sensitivity in damselfishes. J Comp Physiol A 189:213–220Google Scholar
  25. Hawryshyn CW, Ramsden SD, Betke KM, Sabbah S (2010) Spectral and polarization sensitivity of juvenile Atlantic salmon (Salmo salar): phylogenetic considerations. J Exp Biol 213:3187–3197PubMedCrossRefGoogle Scholar
  26. Horváth G, Varjú D (2004) Polarized light in animal vision—polarization patterns in nature. Springer, HeidelbergCrossRefGoogle Scholar
  27. Israelachvili JN, Sammut RA, Snyder AW (1975) Birefringence and dichroism of photoreceptors. Vis Res 16:47–52CrossRefGoogle Scholar
  28. Jäger S, Lewis JW, Zvyaga TA, Szundi I, Sakmar TP, Kliger DS (1997) Chromophore structural changes in rhodopsin from nanoseconds to microseconds following pigment photolysis. Proc Natl Acad Sci USA 94:8557–8562PubMedCrossRefPubMedCentralGoogle Scholar
  29. Johnsen S, Marshall NJ, Widder EA (2011) Polarization sensitivity as a contrast enhancer in pelagic predators: lessons from in situ polarization imaging of transparent zooplankton. Philos Trans R Soc B 366:655–670CrossRefGoogle Scholar
  30. Jordan TM, Partridge JC, Roberts NW (2012) Non-polarizing broadband multilayer reflectors in fish. Nat Photonics 6:759–763PubMedCrossRefPubMedCentralGoogle Scholar
  31. Kammermans M, Hawryshyn C (2011) Teleost polarization vision: how it might work and what it might be good for. Philos Trans R Soc B 366:742–756CrossRefGoogle Scholar
  32. Kondrashev SL, Gnyubkina VP, Zueva LV (2012) Structure and spectral sensitivity of photoreceptors of two anchovy species: Engraulis japonicus and Engraulis encrasicolus. Vis Res 68:19–27PubMedCrossRefGoogle Scholar
  33. Kota P, Reeves PJ, RajBhandary UL, Khorana HG (2006) Opsin is present as dimers in COS1 cells: identification of amino acids at the dimeric interface. Proc Natl Acad Sci USA 103:3054–3059PubMedCrossRefPubMedCentralGoogle Scholar
  34. Kroeger K, Pfleger KDG, Eidne KA (2003) G-protein-coupled receptor oligomerization in neuroendocrine pathways. Front Neuroendocrinol 24:254–278PubMedCrossRefGoogle Scholar
  35. Laughlin SB, Menzel R, Snyder AW (1975) Membranes, dichroism and receptor sensitivity. In: Menzel R (ed) Photoreceptor optics AW Snyder. Springer, Berlin, pp 237–259CrossRefGoogle Scholar
  36. Lerner A, Sabbah S, Erlick C, Shashar N (2011) Navigation by light polarization in clear and turbid waters. Philos Trans R Soc B 366:671–679CrossRefGoogle Scholar
  37. Levine JS, MacNichol EF Jr, Kraft T, Collins BA (1979) Intraretinal distribution of cone pigments in certain teleost fishes. Science 204:523–526PubMedCrossRefGoogle Scholar
  38. Liang Y (2003) Organization of the G-protein-coupled receptors rhodopsin and opsin in native membranes. J Biol Chem 278:21655–21662PubMedCrossRefPubMedCentralGoogle Scholar
  39. Liebman PA (1975) Birefringence, dichroism and rod outer segment structure. In: Snyder AW, Menzel R (eds) Photoreceptor optics. Springer, Berlin, pp 199–214CrossRefGoogle Scholar
  40. Liebman PA, Entine G (1974) Lateral diffusion of visual pigment in photoreceptor disk membranes. Science 185:457–459PubMedCrossRefGoogle Scholar
  41. Liebman PA, Jagger WS, Kaplan MW, Bargoot FG (1974) Membrane structure changes in rod outer segments with rhodopsin bleaching. Nature 251:31–36PubMedCrossRefGoogle Scholar
  42. Liebman PA, Weiner HL, Drzymala RE (1982) Lateral diffusion of visual pigment in rod disk membranes. Methods Enzymol 81:660–668PubMedCrossRefGoogle Scholar
  43. Lukáts A, Szabó A, Röhlich P, Vígh B, Szél A (2005) Photopigment coexpression in mammals: comparative and developmental aspects. Histol Histopathol 20:551–574PubMedGoogle Scholar
  44. MacIntosh TJ (1973) The effect of cholesterol on the structure of phosphatidycholine bilayers. Biochim Biophys Acta 513:43–58CrossRefGoogle Scholar
  45. Maldonado PE, Maturana H, Varela FJ (1988) Frontal and lateral visual system in birds: frontal and lateral gaze. Brain Behav Evol 32:57–62PubMedCrossRefGoogle Scholar
  46. Marc RE, Sperling HG (1976) The chromatic organization of the goldfish cone mosaic. Vis Res 16:1211–1224PubMedCrossRefGoogle Scholar
  47. Molloy JE, Padgett MJ (2002) Lights, action: optical tweezers. Contemp Phys 43:241–258CrossRefGoogle Scholar
  48. Murari R, Murari MP, Baumann WJ (1986) Sterol orientations in phosphatidylcholine liposomes as determined by deuterium NMR. Biochemistry 25:1062–1067PubMedCrossRefGoogle Scholar
  49. Mussi M, Haimberger TJ, Hawryshyn CW (2005) Behavioural discrimination of polarized light in the damselfish Chromis viridis (family Pomacentridae). J Exp Biol 208:3037–3046PubMedCrossRefGoogle Scholar
  50. Novales-Flamarique I (2011) Unique photoreceptor arrangements in a fish with polarized light discrimination. J Comp Neurol 519:714–737PubMedCrossRefGoogle Scholar
  51. Novales-Flamarique I, Hárosi FI (2002) Visual pigments and dichroism of anchovy cones: a model system for polarization detection. Vis Neurosci 19:467–473Google Scholar
  52. Palczewski K (2006) G protein-coupled receptor rhodopsin. Annu Rev Biochem 75:743–767PubMedCrossRefPubMedCentralGoogle Scholar
  53. Palczewski K (2010) Oligomeric forms of G protein-coupled receptors (GPCRs). Trends Biochem Sci 35:595–600PubMedCrossRefPubMedCentralGoogle Scholar
  54. Park PSH, Filipek S, Wells JW, Palczewski K (2004) Oligomerization of G protein-coupled receptors: past, present, and future. Biochemistry 43:15643–15656PubMedCrossRefPubMedCentralGoogle Scholar
  55. Parkyn DC, Hawryshyn CW (2000) Spectral and ultraviolet-polarisation sensitivity in juvenile salmonids: a comparative analysis using electrophysiology. J Exp Biol 203:1173–1191PubMedGoogle Scholar
  56. Parkyn DC, Austin JD, Hawryshyn CW (2003) Acquisition of polarized-light orientation in salmonids under laboratory conditions. Anim Behav 65:893–904CrossRefGoogle Scholar
  57. Pignatelli V, Temple SE, Chiou TH, Roberts NW, Collin SP, Marshall NJ (2011) Behavioural relevance of polarization sensitivity as a target detection mechanism in cephalopods and fishes. Philos Trans R Soc B 366:734–741CrossRefGoogle Scholar
  58. Poo M, Cone RA (1973) Lateral diffusion of rhodopsin in Necturus rods. Exp Eye Res 17:503–510PubMedCrossRefGoogle Scholar
  59. Poo MM, Cone RA (1974) Lateral diffusion of rhodopsin in the photoreceptor membrane. Nature 247:438–441PubMedCrossRefGoogle Scholar
  60. Ramsden SD, Anderson L, Mussi M, Kamermans M, Hawryshyn CW (2008) Retinal processing and opponent mechanisms mediating ultraviolet polarization sensitivity in rainbow trout (Oncorhynchus mykiss). J Exp Biol 211:1376–1385PubMedCrossRefGoogle Scholar
  61. Reckel F, Hoffman B, Melzer RR, Horppila J, Smola U (2003) Photoreceptors and cone patterns in the retina of the smelt Osmerus eperlanus (L.) (Osmeridae: Teleostei). Acta Zool (Stockholm) 84:161–170CrossRefGoogle Scholar
  62. Roberts NW (2006) The optics of vertebrate photoreceptors: anisotropy and form birefringence. Vis Res 46:3259–3266PubMedCrossRefGoogle Scholar
  63. Roberts NW, Gleeson HF (2004) The absorption of polarized light by vertebrate photoreceptors. Vis Res 44:2643–2652PubMedCrossRefGoogle Scholar
  64. Roberts NW, Needham MG (2007) A mechanism of polarized light sensitivity in cone photoreceptors of the goldfish Carassius auratus. Biophys J 93:3241–3248PubMedCrossRefPubMedCentralGoogle Scholar
  65. Roberts NW, Gleeson HF, Temple SE, Haimberger TJ, Hawryshyn CW (2004) Differences in the optical properties of vertebrate photoreceptor classes leading to axial polarization sensitivity. J Opt Soc Am A 21:335–345CrossRefGoogle Scholar
  66. Roberts NW, Chiou TH, Marshall NJ, Cronin TW (2009) A biological quarter-wave retarder with excellent achromaticity in the visible wavelength region. Nat Photonics 3:641–644CrossRefGoogle Scholar
  67. Roberts NW, Porter ML, Cronin TW (2011) The molecular basis of mechanisms underlying polarization vision. Philos Trans R Soc B 366:627–637CrossRefGoogle Scholar
  68. Ryba N, Marsh D (1992) Protein rotational diffusion and lipid protein interactions in recombinants of bovine rhodopsin with saturated diacylphosphatidylcholines of different chain lengths studied by conventional and saturation-transfer electron-spin-resonance. Biochemistry 31:7511–7518PubMedCrossRefGoogle Scholar
  69. Sabbah S, Habib-Nayany MF, Dargaei Z, Hauser FE, Kamermans M, Hawryshyn CW (2013) Retinal region of polarization sensitivity switches during ontogeny of rainbow trout. J Neurosci 33:7428–7438PubMedCrossRefGoogle Scholar
  70. Saibil HR (1982) An ordered membrane-cytoskeleton network in squid photoreceptor microvilli. J Mol Biol 158:435–456PubMedCrossRefGoogle Scholar
  71. Shashar N, Hagan R, Boal JG, Hanlon RT (2000) Cuttlefish use polarization sensitivity in predation on silvery fish. Vis Res 40:71–75PubMedCrossRefGoogle Scholar
  72. Shukolyukov SA (2009) Aggregation of frog rhodopsin to oligomers and their dissociation to monomer: application of BN-and SDS-PAGE. Biochem Mosc 74:599–604CrossRefGoogle Scholar
  73. Snyder AW (1973) Polarization sensitivity of individual retinula cells. J Comp Physiol 83:331–360CrossRefGoogle Scholar
  74. Temple S, Hart NS, Marshall NJ, Collin SP (2010) A spitting image: specializations in archerfish eyes for vision at the interface between air and water. Proc R Soc B 277:2607–2615PubMedCrossRefPubMedCentralGoogle Scholar
  75. Thoreson WB, Burkhardt DA (1990) Effects of synaptic blocking agents on the depolarizing responses of turtle cones evoked by surround illumination. Vis Neurosci 5:571–583PubMedCrossRefGoogle Scholar
  76. Townes-Anderson E, St Jules RS, Sherry DM, Lichtenberger J, Hassanain M (1998) Micromanipulation of retinal neurons by optical tweezers. Mol Vis 4:12PubMedGoogle Scholar
  77. Waterman TH (2006) Reviving a neglected celestial underwater polarization compass for aquatic animals. Biol Rev 81:111–115PubMedCrossRefGoogle Scholar
  78. Wey CL, Cone RA (1981) Lateral diffusion of rhodopsin in photoreceptor cells measured by fluorescence photobleaching and recovery. Biophys J 33:225–232PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Bristol Life Science BuildingUniversity of BristolBristolUK

Personalised recommendations