Morphology of the retina in the freshwater fish Metynnis roosevelti Eigenmann (Characidae, Serrasalminae) and the effects of monochromatic red light

Donatti, Lucélia; Fanta, Edith

doi:10.1590/S0101-81751999000100011

Abstract

The retina of Metynnis roosevelti Eigenmann, 1915, a very active freshwater fish, was investigated by light and electron microscopy and was found to have a complex neuronal structure that allows rapid responses of visual stimuli. Retina photoreceptors are double cones, single long cones, single short cones and rods. Cone inner segments are arranged as mosaics. The outer nuclear layer contains small nuclei of twin cones, long and wide nuclei of long single cones, spherical large nuclei of short cones, and small dense nuclei of rods. Horizontal, amacrine, bipolar and ganglion neurones are responsible for connections and integration between photoreceptor cells and afferent neurones. The pigmented epithelium comprises a single layer of cylindrical cells each with elongated nuclei, mitochondria at the basal region, and melanin grains that can migrate inside long cell processes, depending on light intensity. In darkness, pigment is concentrated in the basal region of the cells and in daylight it is concentrated in the processes, surrounding and protecting the outer segments of photoreceptors. When exposed experimentally to monochromatic red light, expansion of melanin pigments was provoked at the beginning of light period, followed by their withdrawal after exposure to long wave lengths. No active movements of cones or rods were observed. Considerable renewal of photoreceptor membrane discs occurred after one week in red light, caused by higher level of activation of rods to allow the fish to see in relative darkness. Metynnis roosevelti is a native fish from Brazilian tropical and sub-tropical regions. More recently trials were made to use it in fish cultures in different regions of the countiy. Its capacity to adjust to different photic environments facilitates for rearing in varied environments.

Fish; retina; morphology; red light

Morphology of the retina in the freshwater fish Metynnis roosevelti Eigenmann (Characidae, Serrasalminae) and the effects of monochromatic red light

Lucélia Donatti^I; Edith Fanta^II

^IDepartamento de Ciências Biológicas, Universidade Estadual do Centro Oeste. Guarapuava, Paraná, Brasil

^IICorrespondence address: Departamento de Biologia Celular, Universidade Federal do Paraná. Caixa Postal 19031, 81531-970 Curitiba, Paraná, Brasil. E-mail: fantaf@ineparnet.com.br

ABSTRACT

The retina of Metynnis roosevelti Eigenmann, 1915, a very active freshwater fish, was investigated by light and electron microscopy and was found to have a complex neuronal structure that allows rapid responses of visual stimuli. Retina photoreceptors are double cones, single long cones, single short cones and rods. Cone inner segments are arranged as mosaics. The outer nuclear layer contains small nuclei of twin cones, long and wide nuclei of long single cones, spherical large nuclei of short cones, and small dense nuclei of rods. Horizontal, amacrine, bipolar and ganglion neurones are responsible for connections and integration between photoreceptor cells and afferent neurones. The pigmented epithelium comprises a single layer of cylindrical cells each with elongated nuclei, mitochondria at the basal region, and melanin grains that can migrate inside long cell processes, depending on light intensity. In darkness, pigment is concentrated in the basal region of the cells and in daylight it is concentrated in the processes, surrounding and protecting the outer segments of photoreceptors. When exposed experimentally to monochromatic red light, expansion of melanin pigments was provoked at the beginning of light period, followed by their withdrawal after exposure to long wave lengths. No active movements of cones or rods were observed. Considerable renewal of photoreceptor membrane discs occurred after one week in red light, caused by higher level of activation of rods to allow the fish to see in relative darkness. Metynnis roosevelti is a native fish from Brazilian tropical and sub-tropical regions. More recently trials were made to use it in fish cultures in different regions of the countiy. Its capacity to adjust to different photic environments facilitates for rearing in varied environments.

Key words: Fish, retina, morphology, red light

Full text available only in PDF format.

Texto completo disponível apenas em PDF.

ACKNOWLEDGEMENTS. The authors are indebted to Dr. M.A.H. Dolder and to Prof.Dr. R.L. Smith for their valuable suggestions; to MSc S.R.Grötzner for technical assistance in the preparation of the retinas; to the biologists A.C.C. Vianna and S. Romão for assistance in microphotography; to CAPES for a Master's stipend for Lucélia Donatti; to CNPq for a Scientist's stipend to Dr. Edith Fanta.

REFERENCES

AHLBERT, I.B. 1969. The organisation of the cone cells in the retinae of four teleosts with different feeding habits (Perca fluviatilis L., Lucioperca lucioperca L., Acerina cernua L.and Coregonus albula L). Arkiv. Zool., Stockholm, 22 (11): 445-481.

______ . 1976. Organization of the cone cells in the retinae of salmon (Salmo salar) and trout (Salmo trutta trutta) in relation to their feeding habits. Acta Zool., Stockholm, 57: 13-35.

ALLEN, E.E.; R.D. FERNALD.1985. Spectral sensitivity of the African cichlid fish, Haplochromis burtoni. Jour. Comp. Physiol., Heidelberg, 157A: 247-253.

BEÇAK, W.Y.; J.P. VANRELL. 1970. Técnicas de citologia e histologia. São Paulo, Ed. Nobel, 470p.

BOEHLERT, G. W. 1978. Intraspecific evidence for the function of single and double cones in the teleost retina. Science, Washington, 202: 309-311.

BÜCHERL, W. 1962. Técnica microscópica. São Paulo, Ed. Polígono, 164p.

CLARK, G. 1981. Staining procedures. Baltimore, Willians & Wilkins, 512p.

COLLIN, S.P. 1993. The visual system of the florida garfish, Lepisosteus platyrhincus (Ginglymodi). Brain. Behav. Evol., Basel, 42: 295-320.

CULLING, C.F.A.; R.T. ALLISON & W.T. BARR. 1985. Cellular pathology technique. London, Butterworth, 642p.

DOUGLAS, R.H. 1982. The function of photomechanical movements in the retina of the rainbow trout (Salmo gairdneri). Jour. Exp. Biol., Cambridge, 96: 389-403.

EASTMAN, J.T. 1988. Ocular morphology in antarctic notothenioid fishes. J. Morphol.,New York, 196: 283-306.

ENGSTRÖM, K. 1960. Cones types and cone arrangement in the retina of some cyprinids. Acta. Zool., Stockholm, 41: 277-295.

______ . 1963a. Cone types and cone arrangements in teleost retinae. Acta. Zool., Stockholm, 44: 179-243.

______ . 1963b. Structure, organization and ultrastructure of the visual cells in the teleost family Labridae. Acta. Zool., Stockholm, 44: 1-41.

FANTA, E. 1995. Influence of background colour on the behavior of the fish Oreochromis niloticus (Cichlidae). Arq. Biol. Tecnol., Curitiba, 38 (4): 1237- 1251.

FANTA, E.; S.R. GRÖTZNER; M.F. LUVIZOTTO; M.L. ISHIDA & L.M.P. WACHOWICZ. 1991. The environmental impact and the behavior of antarctic fish: I-Light. In: Abstracts of the SCAR International Conference on "Antarctic Science -Global Concerns", Bremen, 40.

FANTA, E.; A.A. MEYER; S.R. GRÖTZNER & M.F. LUVIZOTTO. 1994. Comparative study on feeding strategy and activity patterns of two antarctic fish: Trematomus newnesi Boulenger, 1902 and Gobionotothen gibberifrons (Lönnberg, 1905) (Pisces, Nototheniidae) under different light conditions. Nankyoku Shiriô (Antarctic Rec), Tokyo, 38 (1): 13-29.

GÉRY, J.; C.N.R.S. FRANCE. 1979. The Serrasalmidae (Pisces, Characoidei) from the Serrado Roncador, Mato Grosso, Brasil. Amazoniana, Kiel, 6 (4): 467-495.

HAIRSTON JR., N.G.; K.T. LI & S.S. EASTER JR. 1982. Fish vision and the detection of planktonic prey. Science, Washington, 218: 1240-1242.

KUNZ, Y.W. 1980. Cone mosaics in a teleost retina: changes during light and dark adaptation. Experientia, Basel, 36 (12): 1371-1374.

LEVINE, J.S. & E.F. MACNICHOL JR. 1982. Colour vision in fishes. Sci. Amer., New York, 216 (2): 108-117.

LOUKASHKIN, A.S. & N. GRANT. 1959. Behavior and reactions of the pacific sardine, Sardinops caerulea (Girard), under the influence of white and colored lights and darkness. Proc. Calif. Acad. Sci., San Francisco, 29 (15): 509-548.

LUFT, J.H. 1961. Improvements in epoxy resin embedding methods. J. Biophys. Biochem. Cytol., New York, 9: 409-414.

LYALL, A.H. 1957. Cone arrangements in teleost retinae. Q.J. Microsc. Sci., Cambridge, 98 (2): 189-201.

MACHADO-ALLISSON, A. 1983. Estudios sobre la sistemática de la subfamilia Serrasalminae (Teleostei, Characidae). Parte II. Discusion sobre la condición monofiletica de la subfamilia. Acta. Biol. Venez., Caracas, 11 (4): 145-195.

MENEZES, N.A.; H.J. WAGNER & M.A. ALF. 1981. Retinal adaptations in fishes from a floodplain environment in the central amazon basin. Rev. Can. Biol., Montreal, 40 (1): 111-132.

MUNK, O. 1981. On the cones of the mesopelagic teleost Trachipterus trachypterus (Gmelin, 1789). Vidensk. Medd Dan. Naturhist Foren., Copenhagen, 143: 101-111.

______ . 1982. Cones in the eye of the deep-sea teleost Diretmus argenteus. Vision Res., Oxford, 22: 179-181.

NAG, T.C. & R.K. SUR. 1992. Cones in the retina of the catfish, Clarias batrachus (L). Jour. Fish. Biol., London, 40: 967-969.

NICOL, J.A.C. 1963. Some aspects of photoreception and vision in fishes. Adv. Mar. Biol., San Diego, 1: 171-208.

OMURA, Y.; M. OGURI. 1991. Photoreceptor development in the pineal organ and the eye of Plecoglossus altivelis and Paralichthys olivaceus (Teleostei). Cell Tissue Res., Heidelberg, 266: 315-323.

PANKHURST, N.W.; J.C. MONTGOMERY. 1989. Visual function in four antarctic nototheniid fishes. Jour. Exp. Biol., Cambridge, 142: 311-324.

PAULUS, W.M.; V. HÖMBERG; K. CUNNINGHAM; A.M. HALLIDAY. 1986. Colour and brightness coding in the central nervous system: theoretical aspects and visual-evoked potentials to homogeneous red and green stimuli. Proc. R. Soc. Lond. B. Biol. Sci., London, 227: 53-66.

POGGIO, T. & C. KOCH. 1987. Synapses that compute motion. Sci. Amer., New York, 256 (2): 42-48.

REYNOLDS, E.S. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Jour. Cell Biol., New York, 17: 208-212.

ROSSETO, E.S.; H. DOLDER & I. SAZIMA. 1992. Double cone mosaic pattern in the retina of larval and adult piranha, Serrasalmus spilopleura. Experientia, Basel, 48: 597-599.

SAMEJIMA, M.; S. TAMOTSU; Y. MURANAKA & Y. MORITA. 1991. Dissociation of photoreceptor cells from the pineal organ of the lamprey, Lampetra japonica. Cell Tissue. Res., Heidelberg, 263: 589-592.

TEYKE, T. & S. SCHAERER. 1994. Blind mexican cave fish (Astyanax hubbsi) respond to moving visual stimuli. Jour. Exp. Biol., Cambridge, 188: 89-101.

WATSON, M.L. 1958. Staining of tissue sections for electron microscopy with heavy metals. Jour. Biophys. Biochem. Cytol., New York, 4 (4): 475-478.

WHEELER, T.G. 1979. Retinal red sensitivity under dark-adapted conditions. Brain Res. Rev., Amsterdam, 175: 140-144.

______ . 1982. Colour vision and retinal chromatic information processing in teleost: a review. Brain Res. Rev., Amsterdam, 4: 177-235.

WILLIAMSON, M. & A. KEAST. 1988. Retinal structure relative to feeding in the rock bass (Ambloplites rupestris) and bluegill (Lepomis macrochirus). Can. Jour. Zool., Ottawa, 66: 2840-2846.

ZAUNREITER, M.; H. JUNGER & K. KOTRSCHAL. 1991. Retinal structure; physiology and pharmacology. Vision Res., Oxford, 31 (3): 383-394.

Recebido em 17.X.1997; aceito em 22.II.1999.

AHLBERT, I.B. 1969. The organisation of the cone cells in the retinae of four teleosts with different feeding habits (Perca fluviatilis L., Lucioperca lucioperca L., Acerina cernua L.and Coregonus albula L). Arkiv. Zool., Stockholm, 22 (11): 445-481.
______ . 1976. Organization of the cone cells in the retinae of salmon (Salmo salar) and trout (Salmo trutta trutta) in relation to their feeding habits. Acta Zool., Stockholm, 57: 13-35.
ALLEN, E.E.; R.D. FERNALD.1985. Spectral sensitivity of the African cichlid fish, Haplochromis burtoni. Jour. Comp. Physiol., Heidelberg, 157A: 247-253.
BEÇAK, W.Y.; J.P. VANRELL. 1970. Técnicas de citologia e histologia. São Paulo, Ed. Nobel, 470p.
BOEHLERT, G. W. 1978. Intraspecific evidence for the function of single and double cones in the teleost retina. Science, Washington, 202: 309-311.
BÜCHERL, W. 1962. Técnica microscópica. São Paulo, Ed. Polígono, 164p.
CLARK, G. 1981. Staining procedures. Baltimore, Willians & Wilkins, 512p.
COLLIN, S.P. 1993. The visual system of the florida garfish, Lepisosteus platyrhincus (Ginglymodi). Brain. Behav. Evol., Basel, 42: 295-320.
CULLING, C.F.A.; R.T. ALLISON & W.T. BARR. 1985. Cellular pathology technique. London, Butterworth, 642p.
DOUGLAS, R.H. 1982. The function of photomechanical movements in the retina of the rainbow trout (Salmo gairdneri). Jour. Exp. Biol., Cambridge, 96: 389-403.
EASTMAN, J.T. 1988. Ocular morphology in antarctic notothenioid fishes. J. Morphol,New York, 196: 283-306.
ENGSTRÖM, K. 1960. Cones types and cone arrangement in the retina of some cyprinids. Acta. Zool., Stockholm, 41: 277-295.
______ . 1963a. Cone types and cone arrangements in teleost retinae. Acta. Zool., Stockholm, 44: 179-243.
______ . 1963b. Structure, organization and ultrastructure of the visual cells in the teleost family Labridae. Acta. Zool., Stockholm, 44: 1-41.
FANTA, E. 1995. Influence of background colour on the behavior of the fish Oreochromis niloticus (Cichlidae). Arq. Biol. Tecnol., Curitiba, 38 (4): 1237- 1251.
FANTA, E.; S.R. GRÖTZNER; M.F. LUVIZOTTO; M.L. ISHIDA & L.M.P. WACHOWICZ. 1991. The environmental impact and the behavior of antarctic fish: I-Light. In: Abstracts of the SCAR International Conference on "Antarctic Science -Global Concerns", Bremen, 40.
FANTA, E.; A.A. MEYER; S.R. GRÖTZNER & M.F. LUVIZOTTO. 1994. Comparative study on feeding strategy and activity patterns of two antarctic fish: Trematomus newnesi Boulenger, 1902 and Gobionotothen gibberifrons (Lönnberg, 1905) (Pisces, Nototheniidae) under different light conditions. Nankyoku Shiriô (Antarctic Rec), Tokyo, 38 (1): 13-29.
GÉRY, J.; C.N.R.S. FRANCE. 1979. The Serrasalmidae (Pisces, Characoidei) from the Serrado Roncador, Mato Grosso, Brasil. Amazoniana, Kiel, 6 (4): 467-495.
HAIRSTON JR., N.G.; K.T. LI & S.S. EASTER JR. 1982. Fish vision and the detection of planktonic prey. Science, Washington, 218: 1240-1242.
KUNZ, Y.W. 1980. Cone mosaics in a teleost retina: changes during light and dark adaptation. Experientia, Basel, 36 (12): 1371-1374.
LEVINE, J.S. & E.F. MACNICHOL JR. 1982. Colour vision in fishes. Sci. Amer., New York, 216 (2): 108-117.
LOUKASHKIN, A.S. & N. GRANT. 1959. Behavior and reactions of the pacific sardine, Sardinops caerulea (Girard), under the influence of white and colored lights and darkness. Proc. Calif. Acad. Sci., San Francisco, 29 (15): 509-548.
LUFT, J.H. 1961. Improvements in epoxy resin embedding methods. J. Biophys. Biochem. Cytol., New York, 9: 409-414.
LYALL, A.H. 1957. Cone arrangements in teleost retinae. Q.J. Microsc. Sci., Cambridge, 98 (2): 189-201.
MACHADO-ALLISSON, A. 1983. Estudios sobre la sistemática de la subfamilia Serrasalminae (Teleostei, Characidae). Parte II. Discusion sobre la condición monofiletica de la subfamilia. Acta. Biol. Venez., Caracas, 11 (4): 145-195.
MENEZES, N.A.; H.J. WAGNER & M.A. ALF. 1981. Retinal adaptations in fishes from a floodplain environment in the central amazon basin. Rev. Can. Biol., Montreal, 40 (1): 111-132.
MUNK, O. 1981. On the cones of the mesopelagic teleost Trachipterus trachypterus (Gmelin, 1789). Vidensk. Medd Dan. Naturhist Foren., Copenhagen, 143: 101-111.
______ . 1982. Cones in the eye of the deep-sea teleost Diretmus argenteus. Vision Res., Oxford, 22: 179-181.
NAG, T.C. & R.K. SUR. 1992. Cones in the retina of the catfish, Clarias batrachus (L). Jour. Fish. Biol., London, 40: 967-969.
NICOL, J.A.C. 1963. Some aspects of photoreception and vision in fishes. Adv. Mar. Biol., San Diego, 1: 171-208.
OMURA, Y.; M. OGURI. 1991. Photoreceptor development in the pineal organ and the eye of Plecoglossus altivelis and Paralichthys olivaceus (Teleostei). Cell Tissue Res., Heidelberg, 266: 315-323.
PANKHURST, N.W.; J.C. MONTGOMERY. 1989. Visual function in four antarctic nototheniid fishes. Jour. Exp. Biol., Cambridge, 142: 311-324.
PAULUS, W.M.; V. HÖMBERG; K. CUNNINGHAM; A.M. HALLIDAY. 1986. Colour and brightness coding in the central nervous system: theoretical aspects and visual-evoked potentials to homogeneous red and green stimuli. Proc. R. Soc. Lond. B. Biol. Sci., London, 227: 53-66.
POGGIO, T. & C. KOCH. 1987. Synapses that compute motion. Sci. Amer., New York, 256 (2): 42-48.
REYNOLDS, E.S. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Jour. Cell Biol., New York, 17: 208-212.
ROSSETO, E.S.; H. DOLDER & I. SAZIMA. 1992. Double cone mosaic pattern in the retina of larval and adult piranha, Serrasalmus spilopleura. Experientia, Basel, 48: 597-599.
SAMEJIMA, M.; S. TAMOTSU; Y. MURANAKA & Y. MORITA. 1991. Dissociation of photoreceptor cells from the pineal organ of the lamprey, Lampetra japonica. Cell Tissue. Res., Heidelberg, 263: 589-592.
TEYKE, T. & S. SCHAERER. 1994. Blind mexican cave fish (Astyanax hubbsi) respond to moving visual stimuli. Jour. Exp. Biol., Cambridge, 188: 89-101.
WATSON, M.L. 1958. Staining of tissue sections for electron microscopy with heavy metals. Jour. Biophys. Biochem. Cytol., New York, 4 (4): 475-478.
WHEELER, T.G. 1979. Retinal red sensitivity under dark-adapted conditions. Brain Res. Rev., Amsterdam, 175: 140-144.
______ . 1982. Colour vision and retinal chromatic information processing in teleost: a review. Brain Res. Rev., Amsterdam, 4: 177-235.
WILLIAMSON, M. & A. KEAST. 1988. Retinal structure relative to feeding in the rock bass (Ambloplites rupestris) and bluegill (Lepomis macrochirus). Can. Jour. Zool., Ottawa, 66: 2840-2846.
ZAUNREITER, M.; H. JUNGER & K. KOTRSCHAL. 1991. Retinal structure; physiology and pharmacology. Vision Res., Oxford, 31 (3): 383-394.

Publication Dates

Publication in this collection
10 July 2009
Date of issue
Mar 1999

History

Received
17 Oct 1997
Accepted
22 Feb 1999

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

[1] AHLBERT, I.B. 1969. The organisation of the cone cells in the retinae of four teleosts with different feeding habits (Perca fluviatilis L., Lucioperca lucioperca L., Acerina cernua L.and Coregonus albula L). Arkiv. Zool., Stockholm, 22 (11): 445-481.

[2] ______ . 1976. Organization of the cone cells in the retinae of salmon (Salmo salar) and trout (Salmo trutta trutta) in relation to their feeding habits. Acta Zool., Stockholm, 57: 13-35.

[3] ALLEN, E.E.; R.D. FERNALD.1985. Spectral sensitivity of the African cichlid fish, Haplochromis burtoni. Jour. Comp. Physiol., Heidelberg, 157A: 247-253.

[4] BEÇAK, W.Y.; J.P. VANRELL. 1970. Técnicas de citologia e histologia. São Paulo, Ed. Nobel, 470p.

[5] BOEHLERT, G. W. 1978. Intraspecific evidence for the function of single and double cones in the teleost retina. Science, Washington, 202: 309-311.

[6] BÜCHERL, W. 1962. Técnica microscópica. São Paulo, Ed. Polígono, 164p.

[7] CLARK, G. 1981. Staining procedures. Baltimore, Willians & Wilkins, 512p.

[8] COLLIN, S.P. 1993. The visual system of the florida garfish, Lepisosteus platyrhincus (Ginglymodi). Brain. Behav. Evol., Basel, 42: 295-320.

[9] CULLING, C.F.A.; R.T. ALLISON & W.T. BARR. 1985. Cellular pathology technique. London, Butterworth, 642p.

[10] DOUGLAS, R.H. 1982. The function of photomechanical movements in the retina of the rainbow trout (Salmo gairdneri). Jour. Exp. Biol., Cambridge, 96: 389-403.

[11] EASTMAN, J.T. 1988. Ocular morphology in antarctic notothenioid fishes. J. Morphol,New York, 196: 283-306.

[12] ENGSTRÖM, K. 1960. Cones types and cone arrangement in the retina of some cyprinids. Acta. Zool., Stockholm, 41: 277-295.

[13] ______ . 1963a. Cone types and cone arrangements in teleost retinae. Acta. Zool., Stockholm, 44: 179-243.

[14] ______ . 1963b. Structure, organization and ultrastructure of the visual cells in the teleost family Labridae. Acta. Zool., Stockholm, 44: 1-41.

[15] FANTA, E. 1995. Influence of background colour on the behavior of the fish Oreochromis niloticus (Cichlidae). Arq. Biol. Tecnol., Curitiba, 38 (4): 1237- 1251.

[16] FANTA, E.; S.R. GRÖTZNER; M.F. LUVIZOTTO; M.L. ISHIDA & L.M.P. WACHOWICZ. 1991. The environmental impact and the behavior of antarctic fish: I-Light. In: Abstracts of the SCAR International Conference on "Antarctic Science -Global Concerns", Bremen, 40.

[17] FANTA, E.; A.A. MEYER; S.R. GRÖTZNER & M.F. LUVIZOTTO. 1994. Comparative study on feeding strategy and activity patterns of two antarctic fish: Trematomus newnesi Boulenger, 1902 and Gobionotothen gibberifrons (Lönnberg, 1905) (Pisces, Nototheniidae) under different light conditions. Nankyoku Shiriô (Antarctic Rec), Tokyo, 38 (1): 13-29.

[18] GÉRY, J.; C.N.R.S. FRANCE. 1979. The Serrasalmidae (Pisces, Characoidei) from the Serrado Roncador, Mato Grosso, Brasil. Amazoniana, Kiel, 6 (4): 467-495.

[19] HAIRSTON JR., N.G.; K.T. LI & S.S. EASTER JR. 1982. Fish vision and the detection of planktonic prey. Science, Washington, 218: 1240-1242.

[20] KUNZ, Y.W. 1980. Cone mosaics in a teleost retina: changes during light and dark adaptation. Experientia, Basel, 36 (12): 1371-1374.

[21] LEVINE, J.S. & E.F. MACNICHOL JR. 1982. Colour vision in fishes. Sci. Amer., New York, 216 (2): 108-117.

[22] LOUKASHKIN, A.S. & N. GRANT. 1959. Behavior and reactions of the pacific sardine, Sardinops caerulea (Girard), under the influence of white and colored lights and darkness. Proc. Calif. Acad. Sci., San Francisco, 29 (15): 509-548.

[23] LUFT, J.H. 1961. Improvements in epoxy resin embedding methods. J. Biophys. Biochem. Cytol., New York, 9: 409-414.

[24] LYALL, A.H. 1957. Cone arrangements in teleost retinae. Q.J. Microsc. Sci., Cambridge, 98 (2): 189-201.

[25] MACHADO-ALLISSON, A. 1983. Estudios sobre la sistemática de la subfamilia Serrasalminae (Teleostei, Characidae). Parte II. Discusion sobre la condición monofiletica de la subfamilia. Acta. Biol. Venez., Caracas, 11 (4): 145-195.

[26] MENEZES, N.A.; H.J. WAGNER & M.A. ALF. 1981. Retinal adaptations in fishes from a floodplain environment in the central amazon basin. Rev. Can. Biol., Montreal, 40 (1): 111-132.

[27] MUNK, O. 1981. On the cones of the mesopelagic teleost Trachipterus trachypterus (Gmelin, 1789). Vidensk. Medd Dan. Naturhist Foren., Copenhagen, 143: 101-111.

[28] ______ . 1982. Cones in the eye of the deep-sea teleost Diretmus argenteus. Vision Res., Oxford, 22: 179-181.

[29] NAG, T.C. & R.K. SUR. 1992. Cones in the retina of the catfish, Clarias batrachus (L). Jour. Fish. Biol., London, 40: 967-969.

[30] NICOL, J.A.C. 1963. Some aspects of photoreception and vision in fishes. Adv. Mar. Biol., San Diego, 1: 171-208.

[31] OMURA, Y.; M. OGURI. 1991. Photoreceptor development in the pineal organ and the eye of Plecoglossus altivelis and Paralichthys olivaceus (Teleostei). Cell Tissue Res., Heidelberg, 266: 315-323.

[32] PANKHURST, N.W.; J.C. MONTGOMERY. 1989. Visual function in four antarctic nototheniid fishes. Jour. Exp. Biol., Cambridge, 142: 311-324.

[33] PAULUS, W.M.; V. HÖMBERG; K. CUNNINGHAM; A.M. HALLIDAY. 1986. Colour and brightness coding in the central nervous system: theoretical aspects and visual-evoked potentials to homogeneous red and green stimuli. Proc. R. Soc. Lond. B. Biol. Sci., London, 227: 53-66.

[34] POGGIO, T. & C. KOCH. 1987. Synapses that compute motion. Sci. Amer., New York, 256 (2): 42-48.

[35] REYNOLDS, E.S. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. Jour. Cell Biol., New York, 17: 208-212.

[36] ROSSETO, E.S.; H. DOLDER & I. SAZIMA. 1992. Double cone mosaic pattern in the retina of larval and adult piranha, Serrasalmus spilopleura. Experientia, Basel, 48: 597-599.

[37] SAMEJIMA, M.; S. TAMOTSU; Y. MURANAKA & Y. MORITA. 1991. Dissociation of photoreceptor cells from the pineal organ of the lamprey, Lampetra japonica. Cell Tissue. Res., Heidelberg, 263: 589-592.

[38] TEYKE, T. & S. SCHAERER. 1994. Blind mexican cave fish (Astyanax hubbsi) respond to moving visual stimuli. Jour. Exp. Biol., Cambridge, 188: 89-101.

[39] WATSON, M.L. 1958. Staining of tissue sections for electron microscopy with heavy metals. Jour. Biophys. Biochem. Cytol., New York, 4 (4): 475-478.

[40] WHEELER, T.G. 1979. Retinal red sensitivity under dark-adapted conditions. Brain Res. Rev., Amsterdam, 175: 140-144.

[41] ______ . 1982. Colour vision and retinal chromatic information processing in teleost: a review. Brain Res. Rev., Amsterdam, 4: 177-235.

[42] WILLIAMSON, M. & A. KEAST. 1988. Retinal structure relative to feeding in the rock bass (Ambloplites rupestris) and bluegill (Lepomis macrochirus). Can. Jour. Zool., Ottawa, 66: 2840-2846.

[43] ZAUNREITER, M.; H. JUNGER & K. KOTRSCHAL. 1991. Retinal structure; physiology and pharmacology. Vision Res., Oxford, 31 (3): 383-394.