Structure and arrangement of photoreceptors in the retina of big eye kilka, Clupeonella grimmi (Kessler 1877)


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2 , N. Shabanipour* and F. Pournajafizadeh


The big eye kilka, Clupeonella grimmi, is a marine fish living in depth of 20 to 200 meter of the Caspian Sea. Its eye and retina were processed for histological and SEM studies. Paraffin embedded retina was cut radially and tangentially in 5 ?m thickness and stained with hematoxylin and eosin method. The unstained sections were manipulated for SEM image observations. Tangential retinal sections showed irregular arrangement of cones. Five morphologically different types of photoreceptors were distinguished as rods, short single cones, long single cones, twin cones and double cones. The cones were counted in each quadrant of the retina and cone density was determined. The cones showed increment in diameter but reduction in number at anti-clockwise direction without any specific arrangement. Presence of four types of cone cells and their pattern of distribution revealed assistance in near surface color vision and more light capture in dim light of deeper waters as an adaptation to planktivorous feeding habit and deep water living habitat.


Ahlbert, I.B.( 1969) The organization of the cone cells in the retina of four teleosts with different feeding habits (Perca fluviatilis L, Lucioperca lucioperca L., Structure and arrangement of...60Acerina cernua L., Coregonus albula L.). Arkiv Für Zoologie. 22: 445-481.Ali, M.A. and Anctil, M. (1976) Retinas of Fishes: An Atlas, Springer -Verlag, Berlin. Bone, Q. and Moore, R.H. (2008) Biology of fishes, 3rd ed., Taylor & Francis, Abingdon, U.K., p.310-326 , 409-436. Boehlert, G.W. (1978) Intraspecific Evidence for the function of single and double cones in the teleost retina. Science. 309-311. Bowmaker, J.K. (1984) Microspectroph-otometry of vertebrate photoreceptors. Vision Research. 24: 1641-1650.Bowmaker, J.K.( 1991) Thorpe, A., Douglas, R.H. Ultraviolet sensitive cones in the goldfish. Vision Research. 31: 349-352.Bowmaker, J.K. (1995) The visual pigments of fish. In: Osborne NN, Chader GJ, (Eds.). Progress in retinal and eye research. 15: 1–31. Braekevelt, C.R. (1984) Retinal fine structure in the European eel (Anguilla anguilla). Anatomischer Anzeiger (Jena), 157: 233-243.Braekevelt, C.R. (1994) Retinal photoreceptor fine structure in the short-tailed stingray (Dasyatis brevicaudata). Histo-logy and Histopathology. 9: 507-514. Browman, H.I., Gordon, W.C., Evans, B.I. and O’Brien, W.J. (1990) Correlation between histological and behavioral measures of visual acuity in a zooplanktivorous fish, the white crappie (Pomoxis annularis). Brain Behavior and Evolution. 35: 85-97. Browman, H.I., Novales-Flamarique, I. and Hawryshyn, C.W. (1994) Ultraviolet photoreception contributes to prey search behavior in two species of zooplanktivorous fishes. Journal of Experimental Biology. 186: 187-198. Burkhardt, D.A., Timothy, W.K. and Gothesman, J.D.N. (1986) Functional properties of twin and single cones. Neuroscience Research Supplements. 4: 45-58. Collin, S.P. and Collin, H.B. (1988) The morphology of the retina and lens of the sand lance, (Limnichthys fasciatus) (Creeiidae). Journal of Experimental Biology. 47: 209-218. Cowing, J.A., Poopalasundaram, S., Wilkie, S.E., Bowmaker, J.K. and Hunt, D.M. (2002) Spectral tuning and evolution of short wave-sensitive cone pigments in cottoid fish from Lake Baikal. Biochemistry. 41: 6019-6025. Dowling, J.E. (1987) The retina: An approachable part of the brain, Harvard University Press, Massachusetts, USA. Engstrom, K. (1963) Cone types and cone arrangements in teleost retinas. Acta Zoolgica. 44: 179-243. Fazli, H., Zhang, C.I., Hay, D.E., and Lee, C.W. (2009) Stock assessment and management implications of anchovy kilka (Clupeonella engrauliformis) in Iranian waters of the Caspian Sea. Fisheries Research. 100: 103–108.Fernald, R.D. (1988) Aquatic adaptations in fish eyes, in: Atema, J., Fay, R.R., Popper, A.N., Tavolga, W.N., (Eds.). Sensory biology of aquatic animals. Springer-Verlag, New York, p. 435-466. Hanlon, R.T. and Shashar, N. (1997) Aspects of the Sensory Ecology of Cephalopods, in: Collin, S.P., Marshall, N.J. (Eds.). Sensory Processing in Aquatic Environments, Springer-Verlag. New York, Inc. p. 266-282. Hawryshyn, C.W.(1997) Vision. In: Evans, D.H., (Eds). The physiology of fishes, 2nd edition, CRC Press, USA, p. 345-374. Heß, M. (2009) Triple cones in the retinae of three anchovy species: Engraulis encrasicolus, Cetengraulis mysticetus andAnchovia macrolepidota (Engraulididae, Teleostei). Vision Research. 49: 1569-1582. Kawamura, S. and Tachibanaki, S. (2008) Rod and cone photoreceptors: molecular basis of the difference in their physiology. Comparative Biochemistry and Physiology. 150: 369-377. Kusmic, C., Barsanti, L., Passarelli, V. and Gualtieri, P.(1993) Photoreceptor mor-phology and visual pigment content in the pineal organ and in the retina of Khalili et al., 61juvenile and adult trout Salmo irideus. Micron. 24: 279-286. Kusmic, C. and Gualtieri, P. (2000) Morphology and spectral sensitivities of retinal and extra retinal photoreceptors in freshwater teleosts. Micron. 31: 183-200. Levine, J.S. and MacNichol Jr., E.F., (1979) Visual pigments in teleost fishes: effects of habitat, microhabitat, and behavior on visual system evolution. Sensory Processes. 3: 95-131. Losey, G.S., Cronin, T.W., Goldsmith, T.H., Hyde, D., Marshall, N.J. and McFarland, W.N. (1999) The UV visual world of fishes: a review. Journal of Fish Biology.54: 921-943. Lyall, A.H. (1957) Cone arrangement in teleost retinae. Q. J. Micros. Sci. 98, 189-201. MacFarland, W.N. and Munz, F.W.(1975) The evolution of photopic visual pigments in fishes. Vision Research. 15: 1071–1080. McFarland, W.N. and Loew, E.R. (1994) Ultraviolet visual pigments in marine fishes of the family Pomacentridae.Vision Research. 34: 1393-1396.Marks, W.B. (1965) Visual pigments in single goldfish cones. Journal of Physiology. 178: 14-32.Marshall, N.J. and Vorobyev, M.(2003) The design of color Signals and color vision in fishes, in: Collin, S.P., Marshall, N.J. (Eds.), Sensory Processing in Aquatic Environments, Springer-Verlag, New York, p. 194-222. Muller, H.(1952) Bau und Wachstum der Netzhaut des Guppy (Lebistes reticulatus). Zoologische Jahrbueche . 63: 275-324. Nag, T.C. and Bhattacharjee, J.(2002) Retinal cytoarchitecture in some mountain-stream teleosts of India. Environmental Biology of Fishes. 63: 435-449. Novales Flamarique, I. and Harosi, F.I. (2000) Photoreceptors, visual pigments and ellipsosomes in the killifish Fundulus heteroclitus: a microspectrophotometric and histological study. Visual Neuroscience .17: 403-420.Prikhod’ko, B.I. (1981) Ecological features of the Caspian Kilka (Genus Clupeonella), Scripta Publishing Co. Texas, p. 27-35. Reckel, F., Melzer, R.R. and Smola, U. (2001) Outer retinal fine structure of the garfish Belone belone (L.) (Belonidae, Teleostei) during light and dark adaptation-photoreceptors, cone patte-rns and densities. Visual Neuroscie-nce. 82: 89–105. Reckel, F., Hoffmann, B., Melzer, R.R., Horppila, J. and Smola, U. (2003) Photoreceptors and cone patterns in the retina of the smelt Osmerus eperlanus (L.) (Osmeridae: Teleostei. Acta Zoolgica. 84: 161-170Rossetto, E.S., Dolder, H. and Sazima, I. (1992) Double cone mosaic pattern in the retina of larval and adult piranha, (Serrasalmus spilopleura). Experientia, 48, 597-599.Sandy, J.M. and Blaxter, J.H.S. (1980) A study of retinal development in larval herring and sole. Journal of the Marine Biological Association of the United Kingdom . 60: 59-71.Stell, W.K. ( 1972) The morphological organization of the vertebrate retina. In: Handbook of Sensory Physiology. Vol. V11/2. Physiology of Photoreceptor Organs. Fuortes M. (Ed.), Springer-Verlag., Berlin. p. 111-213. Stell, W.S., and Harosi, F.I.(1976) Cone structure and visual pigment content in the retina of goldfish. Vision Research. 16: 647-657. Wagner, H.J., Frohlich, E., Negishi, K., and Collin S.P.(1998) The eyes of deep-sea fish II. Functional morphology of the retina. Progress in Retinal and Eye Research. 17: 637-685.Walls, G.L. (1942) The Vertebrate Eye and its Adaptive Radiation, The Cranbrook Institute of Science Bloomfield Hills, Michigan. Zaunreiter, M., Junger, H., and Kotrschal, K.(1991) Retinal morphology of cyprinid fishes: a quantitative histological study of ontogenetic changes and interspecific variation. Vision Research. 31: 383-394