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Aquatic Adaptations in Fish Eyes

  • Russell D. Fernald
Conference paper

Abstract

Of all the sense organs, eyes have probably attracted the most attention because of both their central importance and intricate construction. Darwin knew that such “organs of extreme perfection and complication” posed a crucial test of his theory because they seemed too good to have been shaped by natural selection (Darwin [1859] 1958). Since eyes must obey the optical laws of physics, fundamental physical constraints on their structure provide an important analytical basis for understanding adaptive ocular specializations. In light of these physical constraints, inferences about the selective forces that have shaped eye design can be made with some confidence, particularly in the study of aquatic eyes.

Keywords

Outer Segment Outer Nuclear Layer Spherical Aberration Chromatic Aberration External Limit Membrane 
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References

  1. Ali, M.A. and Wagner, H.H. (1975) Distribution and development of retinomotor responses, in Vision in Fishes, Ali, M.A. (ed.), Plenum, New York, pp. 369–396.Google Scholar
  2. Allen, E.E. and Fernald, R.D. (1981) Scotopic visual threshold in the African cichlid fish, Haplochromis burtoni, Soc. Neuro. 7: 270.Google Scholar
  3. Allen, E.A. and Fernald, R.D. (1985) Spectral sensitivity of the African cichlid fish, Haplochromis burtoni, J. Comp. Physiol. 157: 247–253.CrossRefGoogle Scholar
  4. Baburina, E.A. (1955) The eye of the retina in the Caspian shad, Dokl. Akad. Nauk. S.S.S.R., 100(6): 1167–1170.Google Scholar
  5. Bayliss, L.E., Lythgoe, R.J., and Tansley, K. (1936) Some new forms of visual purple found in sea fishes, with a note on the visual cells of origin, Proc. R. Soc. B, 816: 95–113.CrossRefGoogle Scholar
  6. Beer, T. (1894) Die Accommodation des Fischauges, Pfluegers Archiv. Gesamte Physiol. Menschen Tiere, 58: 523–650.CrossRefGoogle Scholar
  7. Boll, F. (1877) Zur Anatomie und Physiologie der Retina, Arch. Anat. Physiol., 4: 783–787.Google Scholar
  8. Borwein, B. (1981) The retinal receptor: a description, in Vertebrate Photoreceptor Optics, Enoch, J.M. and Tobey, F.L., Jr (eds.), Springer-Verlag, New York, pp. 11–81.Google Scholar
  9. Brewster, D. (1816) On the structure of the crystalline lens in fishes and quadrupeds, as ascertained by its action on polarised light, Philos. Trans. R. Soc. Lond., 311–317.Google Scholar
  10. Burkhardt, D.A., Gottesman, J., Levine, J.S., and MacNichol, E.F., Jr. (1983) Cellular mechanisms for color-coding in holostean retinas and the evolution of color vision. Vision Res., 23: 1031–1041.PubMedCrossRefGoogle Scholar
  11. Burnside, B. and Nagle, B. (1983) Retinomotor movements of photoreceptors and retinal pigment epithelium: mechanisms and regulation, in Progress in Retinal Research, vol. 2, Osborne, N. and Chader, G. (eds.), Pergamon Press, New York, p. 67–109.Google Scholar
  12. Campbell, M. and Sands, P.J. (1984) Optical quality during crystalline lens growth, Nature, 312: 291–292.PubMedCrossRefGoogle Scholar
  13. Charman, W.N. and Tucker, J. (1973) The optical system of the goldfish eye, Vision Res., 13: 1–8.PubMedCrossRefGoogle Scholar
  14. Clarke, G.L. (1936) On the depth at which fishes can see, Ecology, 17: 452–456.CrossRefGoogle Scholar
  15. Cuppy, W. (1941) How to Become Extinct, University of Chicago Press.Google Scholar
  16. Darwin, C. (1859) The Origin of Species, New American Library Edition (1958), p. 187.Google Scholar
  17. Daw, N.W. (1967) Goldfish retina: organization for simultaneous color contrast, Science, 158: 942–944.PubMedCrossRefGoogle Scholar
  18. Denton, E.J. and Warren, F.J. (1957) The photosensitive pigments in the retinae of deep-sea fish, J. Mar. Biol. Assoc. U.K., 36: 651–652.CrossRefGoogle Scholar
  19. Devons, S. (1985) Optics through the eyes of the medieval churchmen, in Science and Technology in Medieval Society, Long, P.O. (ed.), Ann. N.Y. Acad. Sci., pp. 205–224.Google Scholar
  20. Douglas, R.H. (1982) The function of the photomechanical movements in the retina of rainbow trout (Salmo gairdnerii), J. Exp. Biol., 96: 389–403.Google Scholar
  21. Douglas, R.H. and Wagner, H-J. (1984) Action specturm of photomechanical cone contraction in the catfish retina, Invest. Ophthalmol. Visual Sci., 25: 534–538.Google Scholar
  22. Easter, S.S., Johns, P.R., and Baumann, L.R. (1977) Growth of the adult goldfish eye. I Optics, Vision Res., 16: 469–476.CrossRefGoogle Scholar
  23. Eberle, H. (1968) Zapfenbau, Zapfenlänge und Chromatische Aberration im Auge von Lebistes reticulatus (Peters Guppy), Zool. Jb. Physiol., 74: 121–154.Google Scholar
  24. Eigenmann, C.H. and Shafer, G.E. (1900) The mosaic of single and twin cones in the retinas of fishes, Am. Nat., 34: 109–118.CrossRefGoogle Scholar
  25. Fernald, R.D. (1980) Optic nerve distention in a cichlid fish, Vision Res., 20: 1015–1019.PubMedCrossRefGoogle Scholar
  26. Fernald, R.D. (1981) Chromatic organization of a cichlid fish retina, Vision Res., 21: 1749–1753.PubMedCrossRefGoogle Scholar
  27. Fernald, R.D. (1982a) Retinal projections in the African cichlid fish, Haplochromis burtoni, J. Comp. Neurol., 206: 379–389.PubMedCrossRefGoogle Scholar
  28. Fernald, R.D. (1982b) Cone mosaic in a teleost retina: no difference between light and dark adapted states, Experentia, 38: 1337–1338.CrossRefGoogle Scholar
  29. Fernald, R.D. (1983) Neural basis of visual pattern recognition, in Advances in Vertebrate Neuroethology, Ewert, J-P., Capranica, R.R., and Ingle, D.J. (eds.), Plenum, New York, pp. 569–580.Google Scholar
  30. Fernald, R.D. (1984) Vision and behavior in an African cichlid fish, Am. Sci., 72(1): 58–65.Google Scholar
  31. Fernald, R.D. (1985a) Growth of the teleost eye: novel solutions to complex constraints, Environ. Biol. Fishes, 13: 113–123.CrossRefGoogle Scholar
  32. Fernald, R.D. (1985b) Eye movements in the African cichlid fish, Haplochromis burtoni, J. Comp. Physiol., 156: 199–208.CrossRefGoogle Scholar
  33. Fernald, R.D. and Johns, P.R. (1980) Retinal structure and growth in the cichlid fish, Haplochromis burtoni, Invest. Ophthalmol. Visual Sci. (supp.) 69.Google Scholar
  34. Fernald, R.D. and Liebman, P. (1980) Visual receptor pigments in the African cichlid fish, Haplochromis burtoni, Vision Res., 20: 857–864.PubMedCrossRefGoogle Scholar
  35. Fernald, R.D. and Scholes, J. (1985a) A zone of exclusive rod neurogenesis in the teleost retina, Soc. Neuro. Abst., 11: 810.Google Scholar
  36. Fernald, R.D. and Scholes, J. (1985b) Retinal neurogenesis in teleosts: a second germinal zone, Submitted.Google Scholar
  37. Fernald, R.D. and Wright, S. (1983) Maintenance of optical quality during crystalline lens growth, Nature, 301: 618–620.PubMedCrossRefGoogle Scholar
  38. Fernald, R.D. and Wright, S. (1985a) Growth of the visual system of the African cichlid fish, H. burtoni: optics, Vision Res., 25(2): 155–161.PubMedCrossRefGoogle Scholar
  39. Fernald, R.D. and Wright S. (1985b) Growth of the visual system of the African cichlid fish, H. burtoni: accommodation, Vision Res., 25(2): 163–170.PubMedCrossRefGoogle Scholar
  40. Fernald, R.D., Wright, S., and Shelton, L.C. (1986) Growth of the visual system of the African cichlid fish, H. burtoni: optic field and retinal field, (in preparation).Google Scholar
  41. Fincham, W.H.A. (1959) Optics, Hatton Press, London.Google Scholar
  42. Fletcher, A., Murphy T., and Young, A. (1954) Solutions of two optical problems, Proc. R. Soc. Lond. A., 223: 216–225.CrossRefGoogle Scholar
  43. Fraley, N.B. and Fernald, R.D. (1982) Social control of developmental rate in the African cichlid fish, Haplochromis burtoni, Z. Tierpsychol. 60: 66–82.Google Scholar
  44. Frederikson, R.D. (1973) On the retinal diverticula in the tubular-eyed opisthoproctid deep-sea fishes Macropinna microstoma and Dolichopteryx longipes. Vidensk, Medd. Dan. Naturhist. Foren., 136: 233–244.Google Scholar
  45. Garten, S. (1907) Die Veränderungen der Netzhaut durch Licht, Graefe-Saemisch Handbuch der gesamten Augenheilkunde, Leipzig, pp. 250–280.Google Scholar
  46. Geiger, W. (1956) Quantitative Untersuchungen über das Gehirn der Knochenfische, mit besonderer Berücksichtigung seines relativen Wachstums, Acta Anat. 26: 121–163; 27: 324–350.PubMedCrossRefGoogle Scholar
  47. Hairston, N.G., Jr. Li, K.T., and Easter, S.S., Jr. (1982) Fish vision and the detection of planktonic prey, Science, 218: 1240–1242.PubMedCrossRefGoogle Scholar
  48. Herzog, H. (1905) Experimented Untersuchungen zur Physiologie der Bewegungsorgange in der Netzhaut, Arch. Anat. Physiol. (Physiol. Abst.), 516: 413–464.Google Scholar
  49. Hobson, E.S. (1972) Activity of Hawaiian reef fishes during evening and morning transitions between daylight and darkness, U.S. Fish. Bull. 70: 715–740.Google Scholar
  50. Hueter, R.E. and Gruber, S.H. (1980) Retinoscopy of aquatic eyes, Vision Res., 20: 197–200.PubMedCrossRefGoogle Scholar
  51. Johns, P.R. (1977) Growth of the adult goldfish eye. III. Source of the new retinal retinal cell number, J. Comp. Neurol., 176: 331–342.PubMedCrossRefGoogle Scholar
  52. Johns, P.R. and Fernald, R.D. (1981) Genesis of rods in teleost fish retina, Nature, 293: 141–142.PubMedCrossRefGoogle Scholar
  53. Kahmenn, H. (1936) Über das foveale sehen der Wirbeltiere. I. Über die Fovea centralis und die Fovea lateralis bei einigen Wirbeltieren. Albrecht von Graefe’s Arch. Ophthalmol., 135: 265–276.Google Scholar
  54. Kirschfeld, K. (1976) The resolution of lens and compound eyes, in Neural Principles of Vision, Zettler, F. and Weiler, R. (eds.), Springer-Verlag, Berlin, pp. 354–369.CrossRefGoogle Scholar
  55. Kong, K.L., Fung, Y.M., and Wasserman, G.S. (1980) Filter mediated color vision with one visual pigment, Science, 207: 783–786.PubMedCrossRefGoogle Scholar
  56. Kühne, W. (1887) Fortgesetzte Untersuchungen über die Retina und die Pigmente des Auges, Untersuch. Physiol. Inst. Univ. Heildelberg, 2: 89–109.Google Scholar
  57. Kunz, Y. and Ennis, S. (1983) Ultrastructural diurnal changes of the retinal photoreceptors in the embryo of a viviparous teleost (Poecilia reticulata P.), Cell. Differ. 13: 115–123.PubMedCrossRefGoogle Scholar
  58. Land, M.C. (1981) Optics and vision in invertebrates, in Handbook of Sensory Physiology, vol. VII 6B, Autrum, H.J. (ed.), Springer-Verlag, Berlin, pp. 472–592.Google Scholar
  59. Liebman, P.A. and Entine, G. (1964) Sensitive low-light level microspectrophotometer: detection of photo-sensitive pigments of retinal cones, J. Opt. Soc. Am., 54: 1451–1459.PubMedCrossRefGoogle Scholar
  60. Liebman, P.A., Carroll, S., and Laties, A. (1969) Spectral sensitivity of retinal screening pigment migration in the frog, Vision Res. 9: 377–384.PubMedCrossRefGoogle Scholar
  61. Locket, N.A. (1977) Adaptations to the deep-sea environment, in Handbook of Sensory Physiology, vol. VII/5, Crescitelli, F. (ed.), Springer-Verlag, Berlin, pp. 67–192.Google Scholar
  62. Lowe, E.R. and Lythgoe, J.N. (1978) The ecology of cone pigments in teleost fishes, Vision Res., 18: 715–722.CrossRefGoogle Scholar
  63. Luneberg, R.K. (1944) Mathematical Theory of Optics, Brown University Press, Providence, R.I., pp. 208–213.Google Scholar
  64. Lyall, A.H., (1957a) The growth of the trout retina, Q. J. Microsc. Sci., 98: 101–110Google Scholar
  65. Lyall A.H. (1957b) Cone arrangements in teleost retinae. Q. J. Microsc. Sci., 98: 189–209.Google Scholar
  66. Lythgoe, J.N. (1979) The Ecology of Vision, Clarendon Press, Oxford.Google Scholar
  67. Marc, R.E. and Sperling, H.G. (1976) Color receptor identities of goldfish cones, Science, 191: 487–489.PubMedCrossRefGoogle Scholar
  68. Marshall, N.B. (1971) Explorations in the life of fishes, Harvard University Press, Cambridge, Mass.Google Scholar
  69. Matthiessen, L. (1882) Über die Beziehungen, welche zwischen dem Brechungsindex des Kernzentrums der Krystalllinse und den Dimensionen des Auges bestehen, Pflügers Arch ges Physiol, 27: 510–523.CrossRefGoogle Scholar
  70. Matthiessen, L. (1886) Über den physikalisch-optischen Bau des Auges der Cetacean und der Fische, Pflügers Archiv. Gesamte Physiol., Menschen Tierre, 38: 521–528.CrossRefGoogle Scholar
  71. Maxwell, J.C. (1854) Some solutions of problems, Cambridge & Dublin Math. J., 1: 76–78.Google Scholar
  72. Meyer, D.L. and Schwassmann, H.O. (1970) Electrophysiological method for determination of refractive state in fish eyes, Vision Res., 10: 1301–1303.PubMedCrossRefGoogle Scholar
  73. Moreland, J.D. and Lythgoe, J.N. (1968) Yellow corneas in fishes, Vision Res., 8: 1377–1380.PubMedCrossRefGoogle Scholar
  74. Müller, H. (1952) Bau und Wachstum der Netzhaut des Guppy (Lebistes reticulatus), Zool. Jb. Allgemein Zool. Physiol. Tier, 63: 275–324.Google Scholar
  75. Munk, O. (1966) Ocular anatomy of some deep-sea teleosts, Dana-Rep Carlsberg Found., 70: 1–62.Google Scholar
  76. Munz, F.W. (1958) Photosensitive pigments from the retinae of certain deep sea fishes, J. Physiol., 140: 220–225.PubMedGoogle Scholar
  77. Munz, F.W. and McFarland, W.N. (1977) Evolutionary adaptations of fishes to the photic environment, in Handbook of Sensory Physiology, vol. VII/5, Crescitelli, F. (ed.), Springer-Verlag, Berlin, pp. 193–274.Google Scholar
  78. Nuboer, J.F.W. and van Genderen-Takken, H. (1978) The artifact of retinoscopy, Vision Res., 18: 1091–1096.PubMedCrossRefGoogle Scholar
  79. Ohtsuka, T. (1985) Relation of spectral types to oil droplets in cones of turtle retina, Science, 229: 874–976.PubMedCrossRefGoogle Scholar
  80. Orlov, O.Y. and Gamburtzeva, A.G. (1975) Dynamics of corneal colorations in fish, Hexagrammos octagrammus, Biofizika, 21: 362–365.Google Scholar
  81. Otten, E. (1981) Vision during growth of a generalized Haplochromis species: H. Elegans Trewavas 1933 (Pisces, Cichlidae), Neth. J. Zool., 31: 650–700.CrossRefGoogle Scholar
  82. Powers, M.K. and Bassi, C.J. (1981) Absolute visual threshold is determined by the proportion of stimulated rods in the growing goldfish retina, Neurosci. Abst., 7: 541.Google Scholar
  83. Powers, M.K. and Easter, S.S., Jr. (1983) Behavioral significance of retinal structure and function in fishes, in Fish Neurobiology, Northcutt, R.G., and Davis, R.E. (eds.), University of Michigan Press, Ann Arbor, pp. 377–404.Google Scholar
  84. Pumphrey, R.J. (1961) Concerning vision, in The Cell and the Organism, Ramsay, J.A. (ed.), Cambridge University Press, pp. 193–208.Google Scholar
  85. Sadler, J.D. (1973) The focal length of the fish eye lens and visual acuity, Vision Res., 13: 417–423.PubMedCrossRefGoogle Scholar
  86. Scholes, J.H. (1975) Colour receptors and the synaptic connexions in the retina of a cyprinid fish, Philos. Trans. R. Soc. B Lond., 270: 61–118.CrossRefGoogle Scholar
  87. Scholes, J.H. (1976) Neuronal connections and cellular arrangement in the fish retina, in Neural Principles of Vision, Zettler, F., and Weiler, R. (eds.), Springer-Verlag, Berlin, pp. 354–369.Google Scholar
  88. Scroczyński, S. (1975a) Die sphärische Aberration der Augenlinse der Regenbogenforelle (Salmo gairdnerii Rich), Zool. Jb. Physiol., 79: 204–212.Google Scholar
  89. Scroczyński, S. (1975b) Die sphärische Aberration der Augenlinse des Hechts (Esox luciusL.), Zool. Jb. Physiol., 79: 547–558.Google Scholar
  90. Scroczyński, S. (1977) Spherical aberration of crystalline lens in the roach Rutilus rutilus L., J. Comp. Physiol., 121: 135–144.CrossRefGoogle Scholar
  91. Sivak, J.G (1982) Optical characteristics of the eye of the flounder, J. Comp. Physiol., 146: 345–349.CrossRefGoogle Scholar
  92. Sivak, J.G., and Bobier, W.R. (1978) Chromatic aberration of the fish eye and its effect on refractive state, Vision Res., 18: 453–455.PubMedCrossRefGoogle Scholar
  93. Soemmering, D.W. (1818) De Oculorum Hominis Animaliumque Secone Horizontali Commentatio, Vandenhoeck and Ruprecht, Göttingen.Google Scholar
  94. Stevens, J.K. and Parsons, K.E. (1980) A fish with double vision, Nat. Hist., 89: 62–67.Google Scholar
  95. Tansley, K. (1965) Vision in Vertebrates, Chapman and Hall, London.Google Scholar
  96. Vilter, V. (1953) Existence d’une rétine à plusieur mosaîques photoréceptrice chez un poisson abyssal bathypelagique, Bathylagus benedicei, C. R. Soc. Biol. (Paris), 147: 1937–1939.Google Scholar
  97. Walls, G.L. (1942) The vertebrate eye and its adaptive radiation, Hafner, New York [1962].Google Scholar
  98. Westheimer, G. (1968) “The eye”, in Mountcastle, V.B. (ed.), Medical Physiology, 12th ed., Mosby, St. Louis, pp. 1532–1553.Google Scholar
  99. Young, R.W. (1967) The renewal of photoreceptor outer segments, J. Cell Biol., 33: 61–72.PubMedCrossRefGoogle Scholar
  100. Young, T. (1801) On the mechanism of the eye, Philos. Trans., 92: 23–88.Google Scholar

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© Springer-Verlag New York Inc. 1988

Authors and Affiliations

  • Russell D. Fernald
    • 1
  1. 1.Institute of NeuroscienceUniversity of OregonEugeneUSA

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