Spectral and ultraviolet-polarisation sensitivity in juvenile salmonids: a comparative analysis using electrophysiology.

Spectral and polarisation sensitivity were compared among juvenile (parr) rainbow trout (Oncorhynchus mykiss), steelhead (O. mykiss), cutthroat trout (O. clarki clarki), kokanee (O. nerka) and brook char (Salvelinus fontinalis) using multi-unit recording from the optic nerve. Although reared under the same conditions, differences in photopic spectral sensitivity were evident. Specifically, ON-responses were co-dominated by L- and M-cone mechanisms in all fish except O. nerka, consistent with an M-cone mechanism sensitivity. The sensitivity of OFF-responses was dominated by the M-cone mechanism for all fish, but O. mykiss appeared to show an additional contribution from the L-cone mechanism. Using chromatic adaptation, an independent ultraviolet-sensitive mechanism is described for the first time for the salmonid genus Salvelinus. In addition, this ultraviolet-cone mechanism was present in the members of the genus Oncorhynchus that were examined. Thus, ultraviolet sensitivity appears to be common to the major extant clades of the subfamily Salmoninae. All species showed differential sensitivity to both vertical and horizontal linearly polarised light. This sensitivity differed between ON- and OFF-responses. The ON-responses were maximally sensitive to both vertically and horizontally polarised light, whereas the OFF-responses displayed maximal sensitivity to horizontally polarised light in all species, with reduced sensitivity to vertically polarised light compared with ON-responses. Because of the similarity in the physiological characteristics of polarisation sensitivity among the salmonid species examined, no relationship between the degree of migratory tendency and the ability to detect polarised light could be identified.

[1]  N. Fisher,et al.  Statistical Analysis of Circular Data , 1993 .

[2]  R Wehner,et al.  Polarized-light navigation by insects. , 1976, Scientific American.

[3]  P. Demarco,et al.  Spectral sensitivity of ON and OFF responses from the optic nerve of goldfish , 1991, Visual Neuroscience.

[4]  Á. Szél,et al.  Ultrastructure and opsin immunocytochemistry of the pineal complex of the larval Arctic charr Salvelinus alpinus: A comparison with the retina , 1991, Journal of pineal research.

[5]  C. Hawryshyn,et al.  Is the Use of Underwater Polarized Light by Fish Restricted to Crepuscular Time Periods? , 1997, Vision Research.

[6]  R. Harwerth,et al.  Red-Green Cone Interactions in the Increment-Threshold Spectral Sensitivity of Primates , 1971, Science.

[7]  L. Mawdesley-Thomas,et al.  Anaesthesia of fish , 1972, Veterinary Record.

[8]  Christa Neumeyer,et al.  On spectral sensitivity in the goldfish Evidence for neural interactions between different “cone mechanisms” , 1984, Vision Research.

[9]  J. N. Lythgoe,et al.  Problems of Seeing Colours under Water , 1975 .

[10]  C. Hawryshyn Light-adaptation properties of the ultraviolet-sensitive cone mechanism in comparison to the other receptor mechanisms of goldfish , 1991, Visual Neuroscience.

[11]  W. McFarland,et al.  Changes in the visual pigments of trout. , 1973, Canadian journal of zoology.

[12]  E. Batschelet Circular statistics in biology , 1981 .

[13]  H. Dartnall,et al.  Vitamin A1/A2-based visual pigment mixtures in cones of the rudd , 1976, Vision Research.

[14]  G. Wald ON THE DISTRIBUTION OF VITAMINS A 1 AND As , 2022 .

[15]  J. Bowmaker,et al.  Ultraviolet receptors, tetrachromatic colour vision and retinal mosaics in the brown trout (Salmo trutta): Age-dependent changes , 1987, Vision Research.

[16]  L. Barsanti,et al.  Photoreceptor morphology and visual pigment content in the pineal organ and in the retina of juvenile and adult trout, Salmo irideus , 1993 .

[17]  C. Groot On the orientation of young sockeye salmon (Oncorhynchus nerka) during their seaward migration out of lakes , 1965 .

[18]  E N Pugh,et al.  Graded-index model of a fish double cone exhibits differential polarization sensitivity. , 1994, Journal of the Optical Society of America. A, Optics, image science, and vision.

[19]  R. Beauchamp,et al.  Goldfish spectral sensitivity: A conditioned heart rate measure in restrained or curarized fish , 1977, Vision Research.

[20]  C D Bridges,et al.  Distribution and evolution of visual pigments in salmonid fishes. , 1970, Vision research.

[21]  C. Hawryshyn,et al.  Behavioural studies of fish vision: an analysis of visual capabilities , 1990 .

[22]  C. Hawryshyn,et al.  Thyroxine induces a precocial loss of ultraviolet photo sensitivity in rainbow trout (Oncorhynchus mykiss, teleostei) , 1992, Vision Research.

[23]  Craig W. Hawryshyn,et al.  Ultraviolet photosensitivity in goldfish: An independent U.V. retinal mechanism , 1985, Vision Research.

[24]  W. Muntz,et al.  Scotopic spectral sensitivity in a teleost fish (Scardinius erytheophthalamus) adapted to different daylengths. , 1973, Vision research.

[25]  F. Crescitelli Chapter 1 The natural history of visual pigments: 1990 , 1991 .

[26]  A. Lyall The Growth of the Trout Reina , 1957 .

[27]  Sunny Bains Sunfish Shows the Way Through the Fog , 1996 .

[28]  Y. Kunz,et al.  Embryonic Fissures in Teleost Eyes and Their Possible Role in Detection of Polarized Light , 1989 .

[29]  Levine Js,et al.  Visual pigments in teleost fishes : effects of habitat, microhabitat, and behavior on visual system evolution , 1979 .

[30]  P. Dill Perception of Polarized Light by Yearling Sockeye Salmon (Oncorhynchus nerka) , 1971 .

[31]  David J. Groggel,et al.  Practical Nonparametric Statistics , 2000, Technometrics.

[32]  C. Hawryshyn,et al.  Ultraviolet sensitivity in the torus semicircularis of juvenile rainbow trout (Oncorhynchus mykiss) , 1994, Vision Research.

[33]  Inga-Britt Ahlbert Organization of the Cone Cells in the Retinae of Salmon (Salmo salar) and Trout (Salmo trutta trutta) in Relation to Their Feeding Habits , 1976 .

[34]  D. Beatty A study of the succession of visual pigments in Pacific salmon (Oncorhynchus). , 1966, Canadian journal of zoology.

[35]  Gerald R. Smith,et al.  Phylogeny of the Pacific Trouts and Salmons (Oncorhynchus) and Genera of the Family Salmonidae , 1993 .

[36]  D. Beatty,et al.  Visual pigments and the labile scotopic visual system of fish , 1984, Vision Research.

[37]  T. G. Wheeler Color vision and retinal chromatic information processing in teleost: A review , 1982, Brain Research Reviews.

[38]  P. Raymond,et al.  Molecular Cloning and characterization of the putative ultraviolet-sensitive visual pigment of goldfish , 1996, Vision Research.

[39]  J. Lythgoe The Ecology of vision , 1979 .

[40]  S. S. Easter Retinal Specialisations for Aquatic Vision: Theory and Facts , 1975 .

[41]  N. Daw Colour‐coded ganglion cells in the goldfish retina: extension of their receptive fields by means of new stimuli , 1968, The Journal of physiology.

[42]  P. Demarco,et al.  The contributions of ON- and OFF-pathways to contrast sensitivity and spatial resolution in goldfish , 1995, Vision Research.

[43]  F. I. Hárosi Microspectrophotometry: The Technique and Some of Its Pitfalls , 1975 .

[44]  F. I. Hárosi,et al.  Ultraviolet visual pigment in a vertebrate: a tetrachromatic cone system in the dace. , 1983, Science.

[45]  J. S. Nelson,et al.  Fishes of the World, 3rd Edition , 1994 .

[46]  C. Hawryshyn,et al.  Cone photoreceptor topography in the retina of sexually mature Pacific salmonid fishes , 1997, The Journal of comparative neurology.

[47]  G. L. Clarke On the Depth at Which Fish Can See , 1936 .

[48]  J. Lythgoe Visual pigments and visual range underwater. , 1968, Vision research.

[49]  W. McFarland,et al.  Evolutionary Adaptations of Fishes to the Photic Environment , 1977 .

[50]  C. Hawryshyn,et al.  THE PHOTIC ENVIRONMENT OF A SALMONTD NURSERY LAKE , 1992 .

[51]  F. Crescitelli THE NATURAL HISTORY OF VISUAL PIGMENTS , 1958, Annals of the New York Academy of Sciences.

[52]  R. Dodge,et al.  Histological Techniques , 1977, British Journal of Cancer.

[53]  M. Vorobyev,et al.  Receptor noise as a determinant of colour thresholds , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[54]  C. Hawryshyn,et al.  ULTRAVIOLET PHOTORECEPTION CONTRIBUTES TO PREY SEARCH BEHAVIOUR IN TWO SPECIES OF ZOOPLANKTIVOROUS FISHES , 1994, The Journal of experimental biology.

[55]  J. Lythgoe Visual pigments and underwater vision , 1966 .

[56]  C. Hawryshyn,et al.  Spectral characteristics of visual pigments in rainbow trout (Oncorhynchus mykiss) , 1994, Vision Research.

[57]  H Spekreijse,et al.  Spectral and spatial coding of ganglion cell responses in goldfish retina. , 1972, Journal of neurophysiology.

[58]  W. Stiles COLOR VISION: THE APPROACH THROUGH INCREMENT-THRESHOLD SENSITIVITY. , 1959 .

[59]  C. Hawryshyn,et al.  Optic nerve response and retinal structure in rainbow trout of different sizes , 1993, Vision Research.

[60]  J. Bowmaker,et al.  Visual pigments and the photic environment: The cottoid fish of Lake Baikal , 1994, Vision Research.

[61]  C. Hawryshyn,et al.  Double-cone internal reflection as a basis for polarization detection in fish. , 1998, Journal of the Optical Society of America. A, Optics, image science, and vision.

[62]  C. Hawryshyn,et al.  Ethambutol affects the spectral and polarisation sensitivity of on-responses in the optic nerve of rainbow trout , 1999, Vision Research.

[63]  J. Lythgoe,et al.  Visual pigments and the acquisition of visual information. , 1989, The Journal of experimental biology.

[64]  A. Tsin,et al.  Visual pigment changes in rainbow trout in response to temperature , 1977, Science.

[65]  F. Utter,et al.  Natural hybridization between steelhead trout (Salmo gairdneri) and coastal cutthroat trout (Salmo clarki clarki) in two Puget Sound streams , 1985 .

[66]  R. Douglas,et al.  The spectral transmission of freshwater teleost ocular media—An interspecific comparison and a guide to potential ultraviolet sensitivity , 1989, Vision Research.

[67]  W. McFarland,et al.  A chromatic action spectrum for planktonic predation by juvenile yellow perch, Perca flavescens , 1993 .

[68]  G. Wald,et al.  Visual Pigments and Depths of Habitat of Marine Fishes , 1957, Nature.

[69]  D. F. Horne Annual meeting of the optical society of America , 1982 .

[70]  C. Hawryshyn,et al.  Spectral Characteristics of Salmonid Migratory Routes from Southern Vancouver Island (British Columbia) , 1993 .

[71]  Garrett K. Mandeville,et al.  Validity conditions in repeated measures designs. , 1979 .

[72]  C. Hawryshyn,et al.  The ontogeny of ultraviolet photosensitivity in rainbow trout (Salmo gairdneri) , 1989, Visual Neuroscience.

[73]  K. V. Mardia,et al.  Linear-Circular Correlation Coefficients and Rhythmometry , 1976 .

[74]  G. Wald THE VISUAL SYSTEMS OF EURYHALINE FISHES , 1941, The Journal of general physiology.

[75]  C. Hawryshyn,et al.  Retinal development and visual sensitivity of young Pacific sockeye salmon (Oncorhynchus nerka) , 1996, The Journal of experimental biology.

[76]  W. Muntz Behavioural Studies of Vision in a Fish and Possible Relationships to the Environment , 1975 .

[77]  T. G. Wheeler Retinal ON and OFF responses convey different chromatic information to the CNS , 1979, Brain Research.

[78]  Hj Norussis,et al.  SPSS for Windows , 1993 .

[79]  J. R. Hoffert,et al.  Light transmission by corneas, aqueous humor and crystalline lenses of fishes. , 1969, Vision research.

[80]  M. Anctil,et al.  Retinas of Fishes: An Atlas , 1976 .

[81]  E. MacNichol,et al.  Visual pigments in teleost fishes: effects of habitat, microhabitat, and behavior on visual system evolution. , 1979, Sensory processes.

[82]  R. Douglas,et al.  Spectral transmission and short-wave absorbing pigments in the fish lens—II. Effects of age , 1993, Vision Research.

[83]  W. B. Scott,et al.  Freshwater fishes of Canada , 1974 .