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A Sensory Basis for Orientation in Cephalopods

Published online by Cambridge University Press:  11 May 2009

R. Williamson
R. Williamson
Affiliation:
Marine Biological Association, The Laboratory, Citadel Hill, Plymouth, PL1 2PB
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Extract

This brief review describes the sense organs involved in orientation by cephalopods with a view to providing a basis for understanding the mechanisms involved. As in many other animals, vision is probably the most important sense involved in orientation. Cephalopods have paired eyes, sometimes providing binocular vision, and generally similar to those of many vertebrates in terms of their gross structure and performance. The main feature apparently lacking in most cephalopods is colour vision, although many have polarized vision. The second most important sense in cephalopods is the sense of balance provided by the statocysts. These paired organs, are functionally similar to the vertebrate vestibular system, and detect both linear and angular accelerations, giving the animal information on its spatial orientation and rotational movements. The statocysts may also be involved in hearing, for there is no doubt that they can detect some vibrations carried in the water and ground. The recently discovered cephalopod lateral line system also detects water-borne vibrations, but this is more probably used for locating other animals in low light conditions. Behavioural experiments have shown that olfaction is also important in cephalopod orientation, but, although there is good morphological data on the structures involved in olfaction, there are little supporting physiological data. Of the remaining senses used in orientation, touch is important for bottom living species, but less so for the free swimming animals. There is no evidence, so far, for electroreception or magnetic sensitivity in cephalopods.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 75 , Issue 1 , February 1995 , pp. 83 - 92
Copyright
Copyright © Marine Biological Association of the United Kingdom 1995

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References

Alexandrowicz, J.S., 1960. A muscle receptor organ in Eledone cirrhosa. Journal of the Marine Biological Association of the United Kingdom, 39,419431.CrossRefGoogle Scholar
Barber, V.C., 1968. The sense organs of Nautilus: preliminary observations on their fine structure. Journal of Microscopy, 6,1067–1072.Google Scholar
Barber, V.C. & Wright, D.E., 1969. The fine structure of the sensory organs of the cephalopod mollusc Nautilus. Zeitschrift fur Mikroskopisch Anatomische Forschung, 102, 293–312.CrossRefGoogle ScholarPubMed
Bergeijk, W.A. Van, 1964. Directional and non-directional hearing in fish. In Marine bio-acoustics (ed. W.N., Tavolga), pp. 1–49. Oxford: Pergamon Press.Google Scholar
Blaxter, J.H.S., Denton, E.J. & Gray, J.A.B., 1981. Acousticolateralis system in clupeid fish. In Hearing and sound communication in fish (ed. W.N., Tavolga et al.), pp. 39–59. New York: Springer-Verlag.CrossRefGoogle Scholar
Bleckmann, H., Budelmann, B.U. & Bullock, T.H., 1991. Peripheral and central nervous responses evoked by small water movements in a cephalopod. Journal of Comparative Physiology, 168A, 247–257.Google Scholar
Boyle, P.R., 1986. Responses to water-borne chemicals by the octopus Eledone cirrhosa (Lamarck, 1798). Journal of Experimental Marine Biology and Ecology, 104, 23–30.CrossRefGoogle Scholar
Budelmann, B.U., 1975. Gravity receptor function in cephalopods with particular reference to Sepia officinalis. Fortschritte der Zoologie, 23, 84—98.Google ScholarPubMed
Budelmann, B.U., 1990. The statocysts of squid. In Squid as experimental animals (ed. D.L., Gilbert et al.), pp. 421–442. New York: Plenum Press.CrossRefGoogle Scholar
Budelmann, B.U. & Bleckmann, H., 1988. A lateral line analogue in cephalopods: water waves generate microphonic potentials in the epidermal head lines of Sepia and Lolliguncula. Journal of Comparative Physiology, 164A, 1–5.CrossRefGoogle ScholarPubMed
Budelmann, B.U., Riese, U. & Bleckmann, H., 1991. Structure, function, biological significance of the cuttlefish ‘lateral lines’. In The cuttlefish (ed. E., Boucaud-Camou), pp. 201–210. Caen, France: Centre de Publication de l'Universite de Caen.Google Scholar
Budelmann, B.U., Sachse, M. & Staudigl, M., 1987. The angular acceleration receptor system of the statocyst of Octopus vulgaris: morphometry, ultrastructure, and neuronal and synaptic organization. Philosophical Transactions of the Royal Society B, 315, 305–343.Google Scholar
Budelmann, B.U. & Williamson, R., 1994. Directional sensitivity of hair cell afferents in the Octopus statocyst. Journal of Experimental Biology, 187, 245–259.CrossRefGoogle ScholarPubMed
Bullock, T.H. & Budelmann, B.U., 1991. Sensory evoked potential in unanesthetized unrestrained cuttlefish: a new preparation for brain physiology in cephalopods. Journal of Comparative Physiology, 168A, 141–150.CrossRefGoogle ScholarPubMed
Chapman, C.J. & Hawkins, A.D., 1973. A field study of hearing in the cod, Gadus morhua L. Journal of Comparative Physiology, 85, 147–167.CrossRefGoogle Scholar
Chase, R. & Wells, M.J., 1986. Chemotactic behaviour in Octopus. Journal of Comparative Physiology, 158A, 375–381.CrossRefGoogle Scholar
Collewijn, H., 1970. Oculomotor reactions in the cuttlefish, Sepia officinalis. Journal of Experimental Biology, 52, 369–384.CrossRefGoogle Scholar
Denton, E.J. & Gilpin-Brown, J.B., 1961. The buoyancy of the cuttlefish, Sepia officinalis (L.). Journal of the Marine Biological Association of the United Kingdom, 41, 319–342.CrossRefGoogle Scholar
Emery, D.G., 1975. Ciliated sensory neurons in the lips of the squid Lolliguncula brevis Blainville. Cell and Tissue Research, 157, 323–329.CrossRefGoogle ScholarPubMed
Emery, D.G., 1976. Observations on the olfactory organ of adult and juvenile Octopus joubini. Tissue and Cell, 8, 33–46.CrossRefGoogle ScholarPubMed
Ferguson, G.P. & Messenger, J.B., 1991. A countershading reflex in cephalopods. Proceedings of the Royal Society B, 243, 63–67.Google Scholar
Fraser, Rowell C.H. & Wells, M.J., 1961. Retinal orientation and the discrimination of polarized light by octopuses. Journal of Experimental Biology, 38, 827–831.Google Scholar
Gilly, W.F. & Lucero, M.T., 1992. Behavioural responses to chemical stimulation of the olfactory organ in the squid Loligo opalescens. Journal of Experimental Biology, 162, 209–229.CrossRefGoogle Scholar
Graziadei, P.P.C. & Gagne, H.T., 1976. Sensory innervation in the rim of the octopus sucker. Journal of Morphology, 150, 639–680.CrossRefGoogle ScholarPubMed
Hanlon, R.T. & Budelmann, B.U., 1987. Why cephalopods are probably not ‘deaf’. American Naturalist, 129, 312–317.CrossRefGoogle Scholar
Hartline, P.H., Hurley, A.C. & Lange, G.D., 1979. Eye stabilization by statocyst mediated oculo-motor reflex in Nautilus. Journal of Comparative Physiology, 132A, 117–126.CrossRefGoogle Scholar
Land, M.F., 1984. Molluscs. In Photoreception and vision in invertebrates (ed. M.A., Ali), pp. 699–725. New York: Plenum Press.CrossRefGoogle Scholar
Lee, P.G., 1992. Chemotaxis by Octopus may a in a Y-maze. Journal of Experimental Marine Biology and Ecology, 153, 53–67.CrossRefGoogle Scholar
Loew, E.R. & McFarland, W.N., 1990. The underwater visual environment. In The visual system of fish (ed. R.H., Douglas and M.B.A., Djamgoz), pp. 1–43. London: Chapman & Hall.Google Scholar
Lucero, M.T, Horrigan, Ft. & Gilly, W.F., 1992. Electrical responses to chemical stimulation of squid olfactory receptor cells. Journal of Experimental Biology, 162, 231–249.CrossRefGoogle Scholar
Macginitie, G.E. & Macginitie, N., ed., 1968. Natural history of marine animals, pp. 523. New York: McGraw-Hill.Google Scholar
Maniwa, Y., 1976. Attraction of bony fish, squid and crab by sound. In Sound reception in fish (ed. A., Schuijf and A.D., Hawkins), pp. 271–283. Amsterdam: Elsevier.Google Scholar
Mather, J.A., 1991. Navigation by spatial memory and use of visual landmarks in octopuses. Journal of Comparative Physiology, 168A, 491–497.CrossRefGoogle Scholar
Messenger, J.B., 1967. The peduncle lobe: a visuo-motor centre in Octopus. Proceedings of the Royal Society B, 167, 225–251.Google Scholar
Messenger, J.B., 1970. Optomotor responses and nystagmus in intact, blinded and statocystless cuttlefish (Sepia officinalis L.). Journal of Experimental Biology, 53, 789–796.CrossRefGoogle ScholarPubMed
Messenger, J.B., 1977. Prey capture and learning in the cuttlefish, Sepia. Symposia of the Zoological Society of London, 38, 347–376.Google Scholar
Messenger, J.B., 1981. Comparative physiology of vision in molluscs. In Handbook of sensory physiology vol. VII/6C (ed. H., Autrum), pp. 93–200. Berlin: Springer-Verlag.Google Scholar
Messenger, J.B., 1991. Photoreception and vision in molluscs. In Evolution of the eye and visual system (ed. J.R., Crony-Dillon and R.L., Gregory), pp. 364–397. Basingstoke: MacMillan.Google Scholar
Moody, M.F. & Parriss, J.R., 1961. The discrimination of polarized light by Octopus: a behavioural and morphological study. Zeitschrift fur Vergleichende Physiologie, 44, 268–291.CrossRefGoogle Scholar
Moynihan, M., 1985. Why are cephalopods deaf? American Naturalist, 125, 465–469.CrossRefGoogle Scholar
Muntz, W.R.A. & Raj, U., 1984. On the visual system of Nautilus pompilius. Journal of Experimental Biology, 109, 253–263.CrossRefGoogle Scholar
Packard, A., 1972. Cephalopods and fish: the limits of convergence. Biological Reviews, 47, 241–307.CrossRefGoogle Scholar
Packard, A., Karlsen, H.E. & Sand, O., 1990. Low frequency hearing in cephalopods. Journal of Comparative Physiology, 166A, 501–505.Google Scholar
Pumphrey, R.J., 1950. Hearing. Symposia of the Zoological Society of London, 4, 3–18.Google Scholar
Roper, C.F.E. & Boss, K.J., 1982. The giant squid. Scientific American, 246, 82–89.CrossRefGoogle Scholar
Saidel, W.M., Lettvin, J.Y. & Macnichol, E.F. Jr 1983. Processing of polarized light by squid photoreceptors. Nature, London, 304, 534–536.CrossRefGoogle ScholarPubMed
Seidou, M., Sugahara, M., Uchiyama, H., Hiraki, K., Hamanaka, T., Michinomae, M., Yoshihara, K. & Kito, Y., 1990. On the three visual pigments in the retina of the firefly squid, Watasenia scintillans. Journal of Comparative Physiology, 166A, 769–773.Google Scholar
Sundermann, G., 1983. The fine structure of epidermal lines on the arms and head of postembryonic Sepia officinalis and Loligo vulgaris (Mollusca, Cephalopoda). Cell and Tissue Research, 232, 669–677.CrossRefGoogle ScholarPubMed
Watkinson, G.B., 1909. Untersuchungen iiber die sogenannten Geruchsorgane der Cephalopoden. Jenaische Zeitschrift fur Naturwissenschaft, 37, 353–414.Google Scholar
Wells, M.J., 1960. Proprioception and visual discrimination of orientation in Octopus. Journal of Experimental Biology, 37,489–499.CrossRefGoogle Scholar
Wells, M.J., 1963. Taste by touch: some experiments with Octopus. Journal of Experimental Biology, 40,187–193.CrossRefGoogle Scholar
Wells, M.J., ed., 1978. Octopus: physiology and behaviour of an advanced invertebrate, pp. 217–245. London: Chapman & Hall.CrossRefGoogle Scholar
Willey, A., ed., 1902. Contribution to the natural history of the pearly Nautilus. Part 6. In Zoological results, pp. 691–830. London: Cambridge University Press.Google Scholar
Williamson, R., 1988. Vibration sensitivity in the statocyst of the northern octopus, Eledone cirrosa. Journal of Experimental Biology, 134, 451–454.CrossRefGoogle Scholar
Williamson, R. & Budelmann, B.U., 1985. The response of the Octopus angular acceleration receptor system to sinusoidal stimulation. Journal of Comparative Physiology, 156A, 403–412.CrossRefGoogle Scholar
Woodhams, P.L. & Messenger, J.B., 1974. A note on the ultrastructure of the Octopus olfactory organ. Cell and Tissue Research, 152, 253–258.CrossRefGoogle ScholarPubMed
Young, J.Z., 1960. The statocysts of Octopus vulgaris. Proceedings of the Royal Society B, 152, 3–29.Google ScholarPubMed