Abstract
The molluscs show every type of eye design from the most simple of eye-cups in limpets to the fish-like lens eyes of squid and octopus, which are every bit as sophisticated as their vertebrate parallels. Even in the bivalves, not a group renowned for their eyesight, there have been a number of curious evolutionary experiments. Thus in scallops one finds eyes that use mirrors rather than lenses to form the image, and in Area and its relatives the mantle bears many small compound eyes not very different from the apposition eyes of insects or sabellid tube worms. These are essentially evolutionary “one-offs” which led nowhere, but which provided their bearers with the ability to respond to moving predators before they are close enough to cast a direct shadow.
Shadow responses, which one finds in bivalve clams and some gastropods, turn out to be generated in a way that is possibly unique in the animal kingdom, in that the photoreceptors that mediate them are primary “off” receptors which hyperpolarise in the light and discharge when the light dims or is turned off. It is ironic that this was discovered Pecten by Hartline in 1938 30 years before it was suspected that vertebrate photoreceptors might behave in a not very different way. The more usual kind of depolarising receptor is also found, usually in the true cephalic eyes of both gastropods and cephalopods. The “off” receptors tend to be highly ciliated and the “on” receptors microvillous, though what this means physiologically is still an interesting open question
In both gastropods and cephalopods the main line of evolutionary development has been in the direction of optically high quality lens eyes. Snails like Helix have only a soft, weakly refracting lens, but in the winkle Littorina this has become hard and inhomogeneous, and has a ratio of focal length to radius of about 2,5 (Matthiessen’s ratio) characteristic of the aplanatic lenses of fish eyes. In the strombids this kind of eye can be quite large — a mm or more — with potentially excellent resolutions (I °), though no-one knows what the eyes are used for. The heteropods are even more intriguing, having fish-like eyes with long narrow retinae only a few cells wide. It now seems that they make scanning eye movements, sweeping through the visual surroundings so that the narrow retina acts as a single like on the TV scan.
Parallels between cephalopod and fish eyes are legendary. They both have Matthiessen’s ratio lenses, mobile pupils and a full complement of eye-movements. The receptors, though, are quite different, and there is no suggestion of colour vision in cephalopods or any other mollusc. Nautilus is a real oddity. How did it last that long with only pinhole optics?
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References
Alkon, D.L. & Fuortes, M.G.F. (1972) Responses of photoreceptors in Hermissenda. J. Gen. Physiol. 60: 631–649.
Arey, L.B. & Crozier, W.J. (1921) On the natural history of Onchidium. J. Exp. Zool. 32: 443–502.
Barber, V.C. & Wright, D.E. (1969a) The fine structure of the eye and optic tentacle of the mollusc Cardium edule. J. Ultrastruct. Res. 26: 515–528.
Barber, V.C. & Wright, D.E. (1969b) The fine structure of the sense organs of the cephalopod mollusc Nautilus. Z. Zellforsch. 102: 293–312.
Barber, V.C., Evans, E.M. & Land, M.F. (1967) The fine structure of the eye of the mollusc Pecten maximus. Z. Zellforsch. 76: 295–312.
Baylor, D.A. & Fuortes, M.G.R (1970) Electrical responses of single cones in the retina of the turtle. J. Physiol. (Lond.) 207: 77–92.
Blest, A.D. & Land, M.F. (1977) The physiological optics of Dinopis subrufus L. Koch: a fish–lens in a spider. Proc. R. Soc. Lond. 196: 197–222.
Boyle, P.R. (1969a) Rhabdomeric ocellus in a chiton. Nature (Lond.) 222: 895–896.
Boyle, P.R. (1969b) Fine structure of the eyes of Onithochiton neglectus ( Mollusca: Polyplacophora). Z. Zellforsch. 102: 313–332.
Boyle, P.R. (1974) The aesthetes of chitons. II. Fine structure in Lepidochitona cinereus L. Cell. Tissue Res. 153: 383–398.
Braun, R. (1954) Zum Lichtsinn facettenaugentragender Muscheln. Zool. Jb. (Zool. u. Physiol. ) 65: 91–125.
Buddenbrock, W.V. & Moller-Racke, I. (1953) über den Lichtsinn von Pecten. Pubbl. Staz. zool. Napoli. 24: 217–245.
Bullock, T.H. (1965) The Mollusca. In: Structure and Function in the Nervous Systems of Invertebrates. Ed. T.H. Bullock & G.A. Horridge, San Francisco, W.H. Freeman, p. 1273–1515.
Collett, T.S. & Land, M.F. (1975) Visual control of flight behaviour in the hoverfly Syritta pipiens L. J. Comp. Physiol. 99: 1–66.
Collewijn, H. (1970) Oculomotor reactions in the cuttlefish, Sepia officinalis. J. Exp. Biol. 52: 369–384.
Dahmen, H.J. (1977) The menotactic orientation of the prosobranch mollusc Littorina littorea. Biol. Cybern. 26: 17–23.
Dakin, W.J. (1910) The eye of Pecten. Quart. J. Microsc. Sei. 55: 49–112.
Dennis, M.J. (1967) Electrophysiology of the visual system of a nudibranch mollusc. 3. Neurophysiol. 30: 1439–1465.
Denton, E.J. (1970) On the organization of the reflecting surfaces in some marine animals. Phil. Trans. R. Soc. Lond. 258B: 285–313.
Dilly, P.N. (1969) The structure of a photoreceptor organelle in the eye of Pterotrachea mutica. Z. Zellforsch. 99: 420–429.
Eakin, R.M. (1972) Structure of invertebrate photoreceptors. In: Handbook of Sensory Physiology Vol. VII/1 • Ed. H.J.A. Dartnall, Berlin, Springer, p. 625–684.
Fletcher, A., Murphy, T. & Young, A. (1954) Solutions of two optical problems. Proc. R. Soc. Lond. 223A: 216–225.
Föh, H. (1932) Der Schattenreflex bei Helix pomatia. Zool. Jb. (Zool. u. Physiol.) 52: 1–78.
Fraenkel, G.S. & Gunn, D.L. (1961) The Orientation of Animals. New York: Dover.
Fujimoto, K., Yanase, T., Okuno, Y. & Iwata, K. (1966) Electrical responses in Onchidium eyes. Mem. Osaka Gakugei Univ. B 15: 98–108.
Gillary, H.L. (1974) Light–evoked potentials from the eye and optic nerve of Strombus: response wave form and spectral sensitivity. J. Exp. Biol. 60: 383–396.
Gillary, H.L. & Gillary, E.W. (1979) Ultrastructural features of the retina and optic nerve of Strombus luhuanus, a marine gastropod. 3. Morph. 159: 89–116.
Gorman, A.L.F. & McReynolds, J.S. (1978) Ionic effects on the membrane potential of hyperpolarizing receptors in the scallop retina. J. Physiol. ( Lond. ) 275: 345–355.
Gwilliam, G.F. (1963) The mechanism of the shadow reflex in Cirripedia. Biol. Bull. Woods Hole 125: 470–485.
Hamilton, P.V. (1977) Daily movements and visual location of plant stems by Littorina irrorata ( Mollusca: Gastropoda). Mar. Behav. Physiol. 4: 293–304.
Hamilton, P.V. & Russell, B.J. (1982) Celestial orientation by surface– swimming Aplysia brasiliana Rang (Mollusca: Gastropoda). J. Exp. Mar. Biol. Ecol. 56: 145–152.
Hartline, H.K. (1938) The discharge of impulses in the optic nerve of Pecten in response to illumination of the eye. J. Cell. Comp. Physiol. 11: 465–477.
Hartline, P.H., Hurley, A.C. & Lange, G.D. (1979) Eye stabilization by statocyst mediated oculomotor reflex in Nautilus. J. Comp. Physiol. 132: 117–126.
Hesse, R. (1900) Untersuchungen über die Organe der Lichtempfindung bei niederen Thieren. VI. Die Augen einiger Mollusken. Z. wiss. Zoll. 68: 379–477.
Hesse, R. (1908) Das Sehen der niederen Tiere. Jena: Fischer.
Holland, C.H. (1979) Early Cephalopoda. In: The Origin of the Major Invertebrate Groups. Ed. M.R. House, London, Academic Press, p. 367–379.
Hurley, A.C., Lange, G.D. & Hartline, P.H. (1978) The adjustable “pinhole camera” eye of Nautilus. J. Exp. Zool. 205: 37–44.
Kennedy, D. (1960) Neural photoreception in a lamellibranch mollusc. J. Gen. Physiol. 44: 277–299.
Krasne, F.B. & Lawrence, P.A. (1966) Structure of the photoreceptors in the compound eyespots of Branchiomma vesiculosum. J. Cell Sei. 1: 239–248.
Land, M.F. (1965) Image formation by a concave reflector in the eye of the scallop Pecten maximus. J. Physiol. ( Lond. ) 179: 138–153.
Land, M.F. (1966a) Activity in the optic nerve of Pecten maximus in response to changes in light intensity, and to pattern and movement in the optical environment. J. Exp. Biol. 45: 83–99.
Land, M.F. (1966b) A multilayer interference reflector in the eye of the scallop, Pecten maximus. J. Exp. Biol. 45: 433–437.
Land, M.F. (1968) Functional aspects of the optical and retinal organization of the mollusc eye. Symp. Zool. Soc. Lond. 23: 75–96.
Land, M.F. (1972) The physics and biology of animal reflectors. Prog. Biophys. Mol. Biol. 24: 75–106.
Land, M.F. (1975) Similarities in the visual behavior of arthropods and men. In: Handbook of Psychobiology. Ed. M.S. Grazzaniga & C. Blakemore, New York, Academic Press, p. 49–72.
Land, M.F. (1981) Optics and vision in invertebrates. In: Handbook of Sensory Physiology Vol. VII/6B. Ed. H. Autrum, Berlin, Springer, p. 471–592.
Land, M.F. (1982) Scanning eye movements in a heteropod mollusc. J. Exp. Biol. 96: 427–430.
Land, M.F. (1983) Crustacea. (This volume).
Light, V.E. (1930) Photoreceptors in Mya arenaria, with special reference to their distribution, structure and function. 3. Morph. 49: 1–42.
Locket, N.A. (1977) Adaptations to the deep–sea environment. In: Handbook of Sensory Physiology Vol. VII/5. Ed. F. Crescitelli, Berlin, Springer, p. 67–192.
Matthiessen, L. (1886) Ueber den physikalisch–optischen Bau des Auges der Cetaceen und der Fische. Pflügers Archiv 38: 521–528.
McReynolds, J.S. & Gorman, A.L.F. (1970a) Photoreceptor potentials of opposite polarity in the eye of the scallop, Pecten irradians. J. Gen. Physiol. 56: 376–391.
McReynolds, J.S. & Gorman, A.L.F. (1970b) Membrane conductances and spectral sensitivities of Pecten photoreceptors. J. Gen. Physiol. 56: 392–406.
McReynolds, J.A. & Gorman, A.L.F. (1974) Ionic basis of hyperpolarizing receptor potential in scallop eye: increase in permeability to potassium ions. Science 183: 658–659.
Messenger, J.B. (1981) Comparative physiology of vision in molluscs. In: Handbook of Sensory Physiology Vol. VII/6C. Ed. H. Autrum, Berlin, Springer, p. 93–2Q0.
Miller, W.H. (1958) Derivatives of cilia in the distal sense cells in the retina of Pecten. J. Biophys. Biochem. Cytol. 4: 227–228.
Moody, M.F. & Parriss, J.R. (1961) The discrimination of polarized light by Octopus: a behavioural and morphological study. Z. vergl. Physiol. 44: 268–291.
Mpistos, G.J. (1973) Physiology of vision in the mollusk Lima scabra. J. Neurophysiol. 36: 371–383.
Müntz, W.R.A. (1977) Pupillary response of cephalopods. Symp. Zool. Soc. Lond. 38: 277–285.
Newell, G.E. (1965) The eye of Littorina littorea. Proc. Zool. Soc. Lond. 144: 75–86.
Packard, A. (1972) Cephalopods and fish: the limits of convergence. Biol. Rev. 47: 241–307.
Patten, W. (1886) Eyes of molluscs and arthropods. Mitt. Zool. Staz. Neapel. 6: 542–756.
Pumphrey, R.J. (1961) Concerning vision. In: The Cell and the Organism. Ed. J.A. Ramsay & V.B. Wigglesworth, Cambridge, University Press, p. 193–208.
Roper, C.F.E. & Boss, K.J. (1982) The giant squid. Sci. Am. 246(4): 82–89.
Rosen, M.D., Stasek, C.R. & Hermans, C.O. (1978) The ultrastructure and evolutionary significance of the cerebral ocelli of Mytilus edulis, the bay mussel. Veliger21: 10–18. Sivak, J.G. (1982) Optical properties of a cephalopod eye (the shortfinned squid, Illex illecebrosus). J. Comp. Physiol. 147: 323–327.
Sivak, J.G. (1982) Optical properties of a cephalopod eye (the shortfinned squid, Illex illecebrosus). J. Comp. Physiol. 147: 323–327.
Stoll, C.J. (1973) Observations on the ultrastructure of the eye of the basommatophoran snail Lymnea stagnalis. Proc. K. Ned. Akad. Wet. C. 76: 1–11.
Sutherland, N.S. & Macintosh, N.J. (1971) Mechanisms of Animal Discrimination Learning. New York, Academic Press.
Toyoda, J. & Shapley, R.M. (1967) The intracellular recorded response in the scallop eye. Biol. Bull. Woods Hole 133: 490.
Toyoda, J., Nosaki, H. & Tomita, T. (1969) Light induced resistance changes in single photoreceptors of Necturus and Gecko. Vision Res. 9: 453–463.
Wells, M.J. (1978) Octopus: Physiology and Behaviour of an Advanced Invertebrate. London: Chapman and Hall.
Wiederhold, M.L., MacNichol, E.F. & Bell, A.L. (1973) Photoreceptor spike responses in the hard shell clam, Mercenaria mercenaria. J. Gen. Physiol. 61: 24–55.
Yanase, T. & Sakamoto, S. (1965) Fine structure of the visual cells of the dorsal eye in molluscan Onchidium verruculatum. Zool. Mag. ( Tokyo ) 74: 238–242.
Yochelson, E.I. (1979) Early radiation of Mollusca and mollusc–like groups. In: The Origin of Major Invertebrate Groups. Ed. M.R. House, London, Academic Press, p. 323–358.
Young, J.Z. (1964) A Model of the Brain. Oxford, Clarendon.
Young, J.Z. (1977) Brain, behaviour and evolution of cephalopods. Symp. Zool. Soc. Lond. 38: 377–434.
Young, R.E. (1975) Function of the dimorphic eyes of the midwater squid Histioteuthis dofleini. Pacific Sci. 29: 211–218.
Zonana, H.V. (1961) Fine structure of the squid retina. Bull. 3ohns Hopkins Hosp. 109: 185–205.
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Land, M.F. (1984). Molluscs. In: Ali, M.A. (eds) Photoreception and Vision in Invertebrates. NATO ASI Series, vol 74. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-2743-1_20
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