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Vision in the southern hemisphere lamprey Mordacia mordax: Spatial distribution, spectral absorption characteristics, and optical sensitivity of a single class of retinal photoreceptor

Published online by Cambridge University Press:  01 September 2004

SHAUN P. COLLIN
Affiliation:
Department of Anatomy and Developmental Biology, School of Biomedical Sciences, The University of Queensland, Queensland, Australia
NATHAN S. HART
Affiliation:
Vision, Touch and Hearing Research Centre, School of Biomedical Sciences, The University of Queensland, Queensland, Australia
KATE M. WALLACE
Affiliation:
Department of Anatomy and Developmental Biology, School of Biomedical Sciences, The University of Queensland, Queensland, Australia
JULIA SHAND
Affiliation:
School of Animal Biology, The University of Western Australia, Western Australia, Australia
IAN C. POTTER
Affiliation:
School of Biological Sciences and Biotechnology, Murdoch University, Murdoch, Western Australia, Australia

Abstract

The dorso-laterally located eyes of the southern hemisphere lamprey Mordacia mordax (Agnatha) contain a single morphological type of retinal photoreceptor, which possesses ultrastructural characteristics of both rods and cones. This photoreceptor has a large refractile ellipsosome in the inner segment and a long cylindrical outer segment surrounded by a retinal pigment epithelium that contains two types of tapetal reflectors. The photoreceptors form a hexagonal array and attain their peak density (33,200 receptors/mm2) in the ventro-temporal retina. Using the size and spacing of the photoreceptors and direct measures of aperture size and eye dimensions, the peak spatial resolving power and optical sensitivity are estimated to be 1.7 cycles deg−1 (minimum separable angle of 34′7′′) and 0.64 μm2 steradian (white light) and 1.38 μm2 steradian (preferred wavelength or λmax), respectively. Microspectrophotometry reveals that the visual pigment located within the outer segment is a rhodopsin with a wavelength of maximum absorbance (λmax) at 514 nm. The ellipsosome has very low absorptance (<0.05) across the measured spectrum (350–750 nm) and probably does not act as a spectral filter. In contrast to all other lampreys studied, the optimized receptor packing, the large width of the ellipsosome-bearing inner segment, together with the presence of a retinal tapetum in the photophobic Mordacia, all represent adaptations for low light vision and optimizing photon capture.

Type
Research Article
Copyright
2004 Cambridge University Press

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References

REFERENCES

Alpern, M. & Pugh, E.N. (1974). The density of photosensitivity of human rhodopsin in the living retina. Journal of Physiology 237, 341370.Google Scholar
Browman, H.I., Gordon, W.C., Evans, B.I., & O'brien, W.J. (1990). Correlation between histological and behavioural measures of visual acuity in a zooplanktivirous fish, the white crappie (Pomoxis annularis). Brain Behavior and Evolution 35, 8597.Google Scholar
Collin, S.P. & Pettigrew, J.D. (1988). Retinal topography in reef teleosts. I. Some species with well-developed areae but poorly-developed streaks. Brain Behavior and Evolution 31, 269282.Google Scholar
Collin, S.P. & Pettigrew, J.D. (1989). Quantitative comparison of the limits on visual spatial resolution set by the ganglion cell layer in twelve species of reef teleosts. Brain Behavior and Evolution 34, 184192.Google Scholar
Collin, S.P. & Collin, H.B. (1995). Ultrastructure and organization of the cornea, lens and iris in the pipefish, Corythoichthyes paxtoni (Syngnathidae, Teleostei). Histology and Histopathology 10, 313323.Google Scholar
Collin, S.P. & Collin, H.B. (1999). The foveal photoreceptor mosaic in the pipefish, Corythoichthyes paxtoni (Syngnathidae, Teleostei). Histology and Histopathology 14, 369382.Google Scholar
Collin, S.P. & Fritzsch, B. (1993). Observations on the shape of the lens in the eye of the silver lamprey, Ichthyomyzon unicuspis. Canadian Journal of Zoology 71, 3441.Google Scholar
Collin, S.P. & Potter, I.C. (2000). The ocular morphology of the southern hemisphere lamprey Mordacia mordax Richardson with special reference to a single class of photoreceptor and a retinal tapetum. Brain Behavior and Evolution 55, 120138.Google Scholar
Collin, S.P. & Trezise, A.E.O. (2004). The origins of colour vision in vertebrates. Clinical and Experimental Optometry 87, 217223.Google Scholar
Collin, S.P., Hoskins, R.V., & Partridge, J.C. (1998). Seven retinal specialisations in the tubular eye of the deep-sea pearleye, Scopelarchus michaelsarsi: A case study in visual optimisation. Brain Behavior and Evolution 51, 291314.Google Scholar
Collin, S.P., Potter, I.C., & Braekevelt, C.R. (1999). The ocular morphology of the southern hemisphere lamprey Geotria australis Gray, with special reference to the characterisation and phylogeny of photoreceptor types. Brain Behavior and Evolution 54, 96118.Google Scholar
Collin, S.P., Hart, N.S., Shand, J., & Potter, I.C. (2003a). Morphology and spectral absorption characteristics of retinal photoreceptors in the southern hemisphere lamprey (Geotria australis). Visual Neuroscience 20, 119130.Google Scholar
Collin, S.P., Knight, M.A., Davies, W.L., Potter, I.C, Hunt, D.M., & Trezise, A.E.O. (2003b). Ancient colour vision: Multiple opsin genes in the ancestral vertebrates. Current Biology 13, R864R865.Google Scholar
Cornwall, M.C., Ripps, H., Chappell, R.L., & Jones, G.J. (1989). Membrane current responses of skate photoreceptors. Journal of General Physiology 94, 633647.Google Scholar
Dickson, D.H. & Graves, D.A. (1979). Fine structure of the lamprey photoreceptors and retinal pigment epithelium (Petromyzon marinus L.). Experimental Eye Research 29, 4560.Google Scholar
Dickson, D.H. & Graves, D.A. (1982). The ultrastructure and development of the eye. In The Biology of Lampreys, Vol. 3, ed. Hardisty, M.W. & Potter, I.C., pp. 4394. London, UK: Academic Press.
Douglas, R.H., Harper, R.D., & Case, J.F. (1998). The pupil response of a teleost fish, Porichthys notatus: Description and comparison to other species. Vision Research 38, 26972710.Google Scholar
Douglas, R.H., Collin, S.P., & Corrigan, J. (2002). The pupillary response of suckermouth armoured catfish (Loricariidae, subfamily Hypostomus): Basic dynamics and the function of a crescent-shaped pupil in relation to both lenticular spherical aberration and retinal topography. Journal of Experimental Biology 205, 34253433.Google Scholar
Dowling, J.E. & Ripps, H. (1972). Adaptation in skate photoreceptors. Journal of General Physiology 60, 698719.Google Scholar
Duke-Elder, S. (1958). System of Ophthalmology. 1. The Eye in Evolution. St. Louis, Missouri: C. V. Mosby.
Fernald, R.D. (1990). The optical system of fishes. In The Visual System of Fish, ed. Douglas, R.H. & Djamgoz, M.B.A., pp. 4561. London, UK: Chapman and Hall.
Fritsches, K.A., Marshall, N.J., & Warrant, E.J. (2003). Retinal specializations in the blue marlin: Eyes designed for sensitivity to low light levels. Marine and Freshwater Research 54, 333341.Google Scholar
Fritzsch, B. & Collin, S.P. (1990). The distribution and dendritic fields of two populations of ganglion cells and the retinopetal fibers in the retina of the lamprey, Ichthyomyzon unicuspis. Visual Neuroscience 4, 533545.Google Scholar
Fröhlich, E., Negishi, K., & Wagner, H.-J. (1995). Patterns of rod proliferation in deep-sea fish retinae. Vision Research 35, 17991811.Google Scholar
Gill, H.S., Renaud, C.B., Chapleau, F., Mayden, R.L., & Potter, I.C. (2003). Phylogeny of living parasitic lampreys (Petromyzontiformes) based on morphological data. Copeia 2003, 687703.Google Scholar
Govardovskii, V.I. & Lychakov, D.V. (1984). Visual cells and visual pigments of the lamprey, Lampetra fluviatilis L. Journal of Comparative Physiology A 154, 279286.Google Scholar
Govardovskii, V.I., Fyhrquist, N., Reuter, T., Kuzmin, D.G., & Donner, K. (2000). In search of the visual pigment template. Visual Neuroscience 17, 509528.Google Scholar
Hárosi, F.I. (1975). Absorption spectrum and linear dichroism of some amphibian photoreceptors. Journal of General Physiology 66, 357382.Google Scholar
Hárosi, F.I. & Kleinschmidt, J. (1993). Visual pigments in the sea lamprey, Petromyzon marinus. Visual Neuroscience 10, 711715.Google Scholar
Hart, N.S. (2002). Vision in the peafowl (Aves: Pavo cristatus). Journal of Experimental Biology 205, 39253935.Google Scholar
Holmberg, K. (1977). The cyclostome retina. In Handbook of Sensory Physiology: The Visual System in Vertebrates, ed. Mackay, D.M. & Teuber, H.L., pp. 4766. New York: Springer-Verlag.
Holmberg, K. & Öhman, P. (1976). Fine structure of retinal synaptic organelles in lamprey and hagfish photoreceptors. Vision Research 16, 237239.Google Scholar
Land, M.F. (1981). Optics and vision in invertebrates. In Handbook of Sensory Physiology, Vol. VII/B, ed. Crescitelli, F., pp. 471591. Berlin: Springer-Verlag.
Land, M.F. & Nilsson, D.E. (2002). Animal Eyes. Oxford, UK: Oxford University Press.
Locket, N.A. (1977). Adaptations to the deep-sea environment. In The Visual System in Vertebrates. Handbook of Sensory Physiology, Vol. VII/5, ed. Crescitelli, F., pp. 67192. Berlin: Springer-Verlag.
Lowenfeld, I.E. (1993). The Pupil: Anatomy, Physiology and Clinical Applications. Detroit, Michigan: Wayne State University Press.
Mathis, U., Schaeffel, F., & Howland, H.C. (1988). Visual optics in toads (Bufo americanus). Journal of Comparative Physiology A 163, 201213.Google Scholar
Matthiessen, L. (1882). Über die Beziehung, welche zwischen dem Brechungsindex des Kernzentrums der Kristallinse und den Dimensionen des Auges bestehen. Pflügers Archiv für die gesamte Physiologie des Menschen und der Tiere 27, 510523.Google Scholar
Munk, O. (1966). Ocular anatomy of some deepsea teleosts. Dana Report 70, 162.Google Scholar
Munk, O. (1986). A multifocal lens in the eyes of the mesopelagic teleosts Trachipterus trachypterus (Gmelin, 1789) and T. arcticus (Brünnich, 1771). Archiv fuer Fishereiwissenschaft 37, 4357.Google Scholar
Munz, F.W. & McFarland, W.N. (1973). The significance of spectral position in the rhodopsins of tropical marine fishes. Vision Research 13, 18291874.Google Scholar
Nakamura, E.L. (1968). Visual acuity of two tunas, Katsuwonus pelamis and Euthynnus affinis. Copeia 1968, 4149.Google Scholar
Öhman, P. (1971). The photoreceptor outer segments of the river lamprey (Lampetra fluviatilis). An electron-fluorescence and light microscopic study. Acta Zoologica Stockholm 52, 287297.Google Scholar
Öhman, P. (1976). Fine structure of photoreceptors and associated neurons of Lampetra fluviatilis (Cyclostomi). Vision Research 16, 659662.Google Scholar
Partridge, J.C. (1990). The colour sensitivity and vision of fishes. In Life and Light in the Sea, ed. Herring, P.J., Campbell, A.K., Whitfield, M. & Maddock, L., pp. 167184. Cambridge: Cambridge University Press.
Partridge, J.N., Shand, J., Archer, S.N., Lythgoe, J.N., & Van Groningen-Luyben, W.A.H.M. (1989). Interspecific variation in the visual pigments of deep-sea fishes. Journal of Comparative Physiology A 164, 513529.Google Scholar
Pedler, C. & Tilly, R. (1964). The nature of the gecko visual cells. A light and electron microscopic study. Vision Research 4, 499510.Google Scholar
Potter, I.C. & Strahan, R. (1968). The taxonomy of the lampreys Geotria and Mordacia and their distribution in Australia. Proceedings of the Linnean Society of London 179, 229240.Google Scholar
Potter, I.C., Lanzing, W.J.R., & Strahan, R. (1968). Morphometric and meristic studies on populations of Australian lampreys of the genus Mordacia. Journal of the Linnean Society (Zoology) 47, 533546.Google Scholar
Potter, I.C., Hilliard, R.W., & Bird, D.J. (1982). Stages in metamorphosis. In The Biology of Lampreys, Vol. 4B, ed. Hardisty, M.W. & Potter, I.C., pp. 137164. London, UK: Academic Press.
Ripps, H. & Dowling, J.E. (1991). Structural features and adaptive properties of photoreceptors in the skate retina. The Journal of Experimental Zoology Supplement 5, 4654.Google Scholar
Shand, J., Hart, N.S., Thomas, N., & Partridge, J.C. (2002). Developmental changes in the cone visual pigments of black bream, Acanthopagrus butcheri. Journal of Experimental Biology 205, 36613667.Google Scholar
Shu, D.-G., Luo, H.-L., Conway Morris, S., Zuang, X.-L., Hu, S.-X., Chen, L., Han, J., Zhu, M., Li, Y., & Chen, L.-Z. (1999). Lower Cambrian vertebrates from south China. Nature 402, 4246.Google Scholar
Snyder, A.W. & Miller, W.H. (1977). Photoreceptor diameter and spacing for highest resolving power. Journal of the Optical Society of America 67, 696698.Google Scholar
Stell, W.K. (1972). The morphological organization of the vertebrate retina. In Handbook of Sensory Physiology Vol. II/2, Physiology of Photoreceptor Organs, ed. Fuortes, M.G.F., pp. 111213, New York: Springer-Verlag.
Tamura, T. (1957). A study of visual perception in fish, especially on resolving power and accommodation. Bulletin of the Japanese Society of Scientific Fisheries 22, 536557.Google Scholar
Tamura, T. & Wisby, W.J. (1963). The visual sense of pelagic fishes, especially the visual axis and accommodation. Bulletin of Marine Science of the Gulf and Caribbean 13, 433448.Google Scholar
Tonosaki, A., Washioka, H., Hara, M., Ishikawa, M., & Watanabe, H. (1989). Photoreceptor disc membranes of Lampetra japonica. Neuroscience Research 6, 340349.Google Scholar
Van Der Meer, H.J. (1995). Visual resolution during growth in a cichlid fish: A morphological and behavioural case study. Brain Behavior and Evolution 45, 2533.Google Scholar
Walls, G.L. (1928). An experimental study of the retina of the brook lamprey, Entosphenus appendix (DeKay). Journal of Comparative Neurology 46, 465473.Google Scholar
Walls, G.L. (1942). The Vertebrate Eye and its Adaptive Radiation. Bloomfield Hills, Michigan: Cranbrook Institute of Science, Cranbrook Press.
Warrant, E.J. & McIntyre, P.D. (1990). Screening pigment, aperture and sensitivity in the dung beetle superposition eye. Journal of Comparative Physiology A 167, 805815.Google Scholar
Warrant, E.J. & Nilsson, D.-E. (1998). Absorption of white light in photoreceptors. Vision Research 38, 195207.Google Scholar
Williamson, M. & Keast, A. (1988). Retinal structure relative to feeding in the rock bass (Ambloplites rupestris) and bluegill (Lepomis macrochirus). Canadian Journal of Zoology 66, 28402846.Google Scholar
Wong, R.O.L. (1989). Morphology and distribution of neurons in the retina of the American garter snake Thamnophis sirtalis. Journal of Comparative Neurology 283, 587601.Google Scholar
Xian-Guang, H., Aldridge, R.J., Siveter, D.J., Siveter, D.J., & Xiang-Hong, F. (2002). New evidence on the anatomy and phylogeny of the earliest vertebrates. Proceedings of the Royal Society B (London) 269, 18651869.Google Scholar
Yamada, E. & Ishikawa, T. (1967). The so-called “synaptic ribbon” in the inner segment of the lamprey retina. Archivum Histologicum Japonicum 28, 411417.Google Scholar
Yamanouchi, T. (1956). The visual acuity of the coral fish Microcanthus strigatus (Cuvier and Valenciennes). Publication of the Seto Marine Biology Laboratory 5, 133156.Google Scholar
Young, R.W. & Martin, G.R. (1984). Optics of retinal oil droplets: A model of light collection and polarization detection in the avian retina. Vision Research 24, 129137.Google Scholar