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The optics of the growing lungfish eye: Lens shape, focal ratio and pupillary movements in Neoceratodus forsteri (Krefft, 1870)

Published online by Cambridge University Press:  06 September 2007

HELENA J. BAILES ,
ANN E.O. TREZISE  and
SHAUN P. COLLIN
HELENA J. BAILES
Affiliation:
School of Biomedical Sciences, The University of Queensland, St Lucia, Brisbane, QLD 4072, Australia
ANN E.O. TREZISE
Affiliation:
School of Biomedical Sciences, The University of Queensland, St Lucia, Brisbane, QLD 4072, Australia
SHAUN P. COLLIN
Affiliation:
School of Biomedical Sciences, The University of Queensland, St Lucia, Brisbane, QLD 4072, Australia
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Abstract

Lungfish (order Dipnoi) evolved during the Devonian period and are believed to be the closest living relatives to the land vertebrates. Here we describe the previously unknown morphology of the lungfish eye in order to examine ocular adaptations present in early sarcopterygian fish. Unlike many teleosts, the Australian lungfish Neoceratodus forsteri possesses a mobile pupil with a slow pupillary response similar to amphibians. The structure of the eye changes from juvenile to adult, with both eye and lens becoming more elliptical in shape with growth. This change in structure results in a decrease in focal ratio (the distance from lens center to the retina divided by the lens radius) and increased retinal illumination in adult fish. Despite a degree of lenticular correction for spherical aberration, there is considerable variation across the lens. A re-calculation of spatial resolving power using measured focal ratios from cryosectioning reveals a low ability to discriminate fine detail. The dipnoan eye shares more features with amphibian eyes than with most teleost eyes, which may echo the visual needs of this living fossil.

Keywords

DipnoiOpticsDevelopmentLongitudinal spherical aberration of the lensMatthiessen's ratio
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 3 , May 2007 , pp. 377 - 387
Copyright
© 2007 Cambridge University Press

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References

REFERENCES

Ali, M.A. & Anctil, M. (1973). Retina of the South American lungfish Lepidosiren paradoxa Fitzinger. Canadian Journal of Zoology 51, 969–972.Google Scholar
Appleby, S.J. & Muntz, W.R.A. (1979). Occlusable yellow corneas in tetraodontidae. Jounral of Experimental Biology 83, 249–259.Google Scholar
Bailes, H.J., Robinson, S.R., Trezise, A.E.O. & Collin, S.P. (2006a). Morphology, characterization and distribution of retinal photoreceptors in the Australian lungfish Neoceratodus forsteri (Krefft, 1870). The Journal of Comparative Neurology 494, 381–397.Google Scholar
Bailes, H.J., Trezise, A.E.O. & Collin, S.P. (2006b). The number, morphology and distribution of retinal ganglion cells and optic axons in the Australian lungfish Neoceratodus forsteri (Krefft 1870). Visual Neuroscience 23, 257–273.Google Scholar
Bancroft, T.L. (1911). On a weak point in the life-history of Neoceratodus forsteri, Krefft. Proceedings of the Royal Society of Queensland 23, 251–256.Google Scholar
Bantseev, K.L., Moran, K.L., Dixon, D.G., Trevithick, J.R. & Sivak, J.G. (2004). Optical properties, mitochondria, and sutures of lenses of fishes: A comparative study of nine species. Canadian Journal of Zoology 82, 86–93.Google Scholar
Barr, L. & Alpern, M. (1963). Photosensitivity of the frog iris. Journal of General Physiology 46, 1249–1265.Google Scholar
Bateson, W. (1890). Contractility of the iris in fishes and cephalopods. Journal of the Marine Biological Association of the UK 1, 215–216.Google Scholar
Brinkmann, H., Venkatesh, B., Brenner, S. & Meyer, A. (2004). Nuclear protein-coding genes support lungfish and not the coelacanth as the closest living relatives of land vertebrates. Proceedings of the National Academy of Sciences of the USA 101, 4899–4905.Google Scholar
Brooks, S. (1995). Short-term study of the breeding requirements of lungfish (Neoceratodus forsteri) in the Burnett River with specific reference to the possible effects of the proposed Walla Weir. Queensland Department of Primary Industries Report, Brisbane.
Brooks, S. & Kind, P. (2001). Ecology and demographics of lungfish (Neoceratodus forsteri) and general fish communities in the Burnett River, Queensland, with reference to the impacts of Walla Weir and future infrastructure development. Queensland Department of Primary Industries Report, Brisbane.
Brown-Séquard, E. (1859). Recherches experimentales sur l'influence excitaire de la lumière, du froid et de la chaleur sur l'iris, dans les cinq classes d'animaux vertébrés. Journal de Physiologie et Pathologie Générale 2, 281–294.Google Scholar
Collin, H.B. & Collin, S.P. (2000). The corneal surface of aquatic vertebrates: Microstructures with optical and nutritional function? Philosophical Transactions of the Royal Society of London, Series B 355, 1171–1176.Google Scholar
Collin, S.P. & Collin, H.B. (2006). The corneal epithelial surface in the eyes of vertebrates: Environmental and evolutionary influences on structure and function. Journal of Morphology 267, 273–291.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, 34–41.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 optical specialisations and the characterisation and phylogeny of photoreceptor types. Brain, Behavior, and Evolution 54, 96–118.Google Scholar
Cornell, E.A. & Hailman, J.P. (1984). Pupillary responses of two Rana pipiens-complex anuran species. Herpetologica 40, 356–366.Google Scholar
Douglas, R.H., Collett, T.S. & Wagner, H.-J. (1986). Accommodation in anuran Amphibia and its role in depth vision. Journal of Comparative Physiology A 158, 133–143.Google Scholar
Douglas, R.H., Collin, S.P. & Corrigan, J. (2002). The eyes of suckermouth armoured catfish (Loricariidae, subfamily Hypostpmus): Pupil response, lenticular longitudinal spherical aberration and retinal topography. Journal of Experimental Biology 205, 3425–3433.Google Scholar
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, 2697–2710.Google Scholar
Douglas, R.H. & McGuigan, C.M. (1989). The spectral transmission of freshwater teleost ocular media—an interspecific comparison and a guide to potential ultraviolet sensitivity. Vision Research 29, 871–897.Google Scholar
Duke-Elder, S. (1958). The Eye in Evolution, vol. II. London: Henry Kimpton.
Easter, S.S.-J. & Nicola, G.N. (1996). The development of vision in the zebrafish Danio rerio. Developmental Biology 180, 646–663.Google Scholar
Fernald, R.D. (1988). Aquatic adaptations in fish eyes. In Sensory Biology of Aquatic Animals, ed. Atema, J., Fay, R.R., Popper, A.N. & Tavolga, W.N., pp. 435–466. Berlin: Springer.
Gilbert, P.W. (1963). The visual apparatus in sharks. In Sharks and Survival, ed. Gilbert, P.W., pp. 283–326. Boston: Heath.
Günther, A. (1871). Description of Ceratodus, a genus of ganoid fishes. Philosophical Transactions of the Royal Society of London 161, 511.Google Scholar
Hart, N.S. (2002). Vision in the peafowl (Aves:Pavo cristatus). Journal of Experimental Biology 205, 3925–3935.Google Scholar
Heinermann, P.H. (1984). Yellow intraocular filters in fishes. Journal of Experimental Biology 43, 127–147.Google Scholar
Henning, J., Henning, P.A. & Himstedt, J.P. (1991). Peripheral and central contribution to the pupillary reflex control in amphibians: Pupillographic and theoretical considerations. Biological Cybernetics 64, 511–518.Google Scholar
Howland, H.C., Merola, S. & Basarab, J.R. (2004). The allometry and scaling of the size of vertebrate eyes. Vision Research 44, 2043–2065.Google Scholar
Hughes, A. (1977). The topography of vision in mammals of contrasting lifestyles: Comparative optics and retinal organization. In Handbook of Sensory Physiology: The Visual System in Vertebrates, ed. Crescitelli, F., pp. 615–756. Berlin: Springer-Verlag.
Illidge, T. (1893). On Ceratodus forsteri. Proceedings of the Royal Society of Queensland 10, 40–44.Google Scholar
Jamieson, G.S. (1971). The functional significance of corneal distortion in marine mammals. Canadian Journal of Zoology 49, 421–423.Google Scholar
Joss, J.M.P. (1998). Are extant lungfish neotenic? Clinical and Experimental Pharmacology and Physiology 25, 733–735.Google Scholar
Kemp, A. (1977). Patterns of tooth plate formation in the Australian lungfish Neoceratodus forsteri Krefft. Zoological Journal of The Linnean Society 60, 223–258.Google Scholar
Kemp, A. (1984). Spawning of the Australian lungfish, Neoceratodus forsteri (Krefft) in the Brisbane River and in Enoggera Reservoir, Queensland. Memoirs of the Queensland Museum 21, 391–399.Google Scholar
Kemp, A. (1986). The Biology of the Australian Lungfish, Neoceratodus forsteri (Krefft 1870). Journal of Morphology, Supplement 1, 181–198.Google Scholar
Kemp, A. & Molnar, R.E. (1981). Neoceratodus forsteri from the lower Cretaceous of New South Wales, Australia. Journal of Palaeontology 55, 211–217.Google Scholar
Kerr, J.G. (1902). The development of Lepidosiren paradoxa. III. Development of the skin and its derivatives. Quarterly Journal of Microscopical Sciences 46, 417–406.Google Scholar
Krefft, G. (1870). Description of a giant amphibian allied to the genus Lepidosiren from the Wide Bay district, Queensland. Proceedings of The Zoological Society of London 1870, 221–224.Google Scholar
Kreuzer, R.O. & Sivak, J.G. (1984). Spherical aberration of the fish lens: interspecies variation and age. Journal of Comparative Physiology 154, 415–422.Google Scholar
Kreuzer, R.O. & Sivak, J.G. (1985). Chromatic aberration of the vertebrate lens. Ophthalmic & Physiological Optics 5, 33–41.Google Scholar
Krizaj, D., Gabriel, R., Owen, W.G. & Witkovsky, P. (1998). Dopamine D2 receptor-mediated modulation of rod-cone coupling in the Xenopus retina. Journal of Comparative Neurology 398, 529–538.Google Scholar
Kröger, R.H.H, Campbell, M.C.W., Fernald, R.D. & Wagner, H.J. (1999). Multifocal lenses compensate for chromatic defocus in vertebrate eyes. Journal of Comparative Physiology 184, 361–369.Google Scholar
Lisney, T.J. & Collin, S.P. (2007). Eye size and neuroethology in elasmobranchs. Brain Behavior and Evolution 69, 266–279.Google Scholar
Malkki, P.E. & Kröger, R.H.H. (2005). Visualization of chromatic correction of fish lenses by multiple focal lengths. Journal of Optics A: Pure and Applied Optics 7, 691–700.Google Scholar
Mathis, U., Schaeffel, F. & Howland, H.C. (1988). Visual optics in toads (Bufo americanus). Journal of Comparative Physiology 163, 201–213.Google Scholar
Matthiessen, L. (1880). Untersuchungen über Aplanatismus und die Periscopie der Kristallinsen in den Augen der Fische. Pflügers Archives 21, 287–307.Google Scholar
Möller, A. (1951). Die struktur des auges bei urodelen verschiedener korpergrosse. Zoologische Jahrbücher Abteilung für allgemeine Zoologie und Physiologie der Tiere 62, 138–182.Google Scholar
Munk, O. (1964). The eye of Calamoichthyes calabaricus Smith, 1865 (Polypteridae, Pisces) compared with the eye of other fishes. Videnskabelige Meddelellserr naturhistorisk Forening 127, 113–125.Google Scholar
Munk, O. (1984). Non-spherical lenses in the eyes of some deep-sea teleosts. Archiv für Fischereiwissenschaft 34, 145–153.Google Scholar
Munk, O. (1986). A multifocal lens in the eyes of mesopelagic teleosts Tracipterus tracypterus (Gmelin, 1789) and T. arcticus (Brunich, 1771). Archiv für Fischereiwissenschaft 37, 43–57.Google Scholar
Munk, O. & Frederiksen, R.D. (1974). On the function of aphakic apertures in teleosts. Videnskabelige Meddelellser Dansk Naturhistorisk Forening 137, 65–94.Google Scholar
Muntz, W.R.A. (1972). Inert absorbing and reflecting pigments. In Handbook of Sensory Physiology, ed. Dartnall, H.J.A., pp. 529–565. Berlin: Springer.
Muntz, W.R.A. (1975). The visual consequences of yellow filtering pigments in the eyes of fishes occupying different habitats. In Light as an ecological factor—II, eds. Evans, G.C., Bainbridge, R. & Rackham, O. pp. 271–287. New York: Halstead Press.
Muntz, W.R.A. (1982). Visual adaptations to different light environments in Amazonian fishes. Revue Canadienne de Biologie Experimentale 41, 35–46.Google Scholar
Muntz, W.R.A. & Wainwright, A.W. (1977). Seasonal changes in the environmental light and visual pigments of the rudd Scardinius erythrophthalmus. Vision Research 17, 75–83.Google Scholar
Orlov, O.Y. & Gamburtzeva, A.G. (1976). Changeable colouration of cornea in the fish Hexagrammos octogrammus. Nature 263, 405–407.Google Scholar
Pankhurst, P.M., Pankhurst, N.W. & Montgomery J.C. (1993). Comparison of Behavioral and Morphological Measures of Visual-Acuity During Ontogeny in a Teleost Fish, Forsterygion-Varium, Tripterygiidae (Forster, 1801). Brain, Behavior and Evolution 42, 178–188.Google Scholar
Pettigrew, P. & Collin, S.P. (1995). Terrestrial optics in an aquatic eye: The sandlance Limnichthyes fasciatus (Creeidae, Teleostei). Journal of Comparative Physiology A. 177, 397–408.Google Scholar
Robinson, S.R. (1994). Early vertebrate color-vision. Nature 367, 121–121.Google Scholar
Rochon-Duvigneaud, A. (1943). Les yeux et la vision des vertébrés. Paris: Masson et Cie.
Rubin, L. & Nolte, J. (1982). Autonomic innervation and photosensitivity of the sphincter pupillae muscle of two teleosts: Lophius piscatorius and Opsanus tau. Current Eye Research 1, 543–551.Google Scholar
Shand, J. (1994). Changes in the visual system of teleost fishes during growth and settlement: an ecological perspective. James Cook University, Townsville.
Shand, J., Døving, K.B. & Collin, S.P. (1999). Optics of the developing fish eye: Comparisons of Matthiessen's ratio and the focal length of the lens in the black bream. Vision Research 39, 1071–1078.Google Scholar
Siebeck, U.E., Collin, S.P., Ghoddussi, M. & Marshall, N.J. (2003). Occlusable corneas in toadfishes: Light transmission, movement and ultrastructure of pigment during light and dark adaptation. Journal of Experimental Biology 206, 2177–2190.Google Scholar
Sivak, J.G. (1974). The refractive error of the fish eye. Vision Research 14, 209–213.Google Scholar
Sivak, J.G. (1978). Optical characteristics of the eye of the spiny dogfish (Squalus acanthias). Revue Canadienne de Biologie Experimentale 37, 209–217.Google Scholar
Sivak, J.G. (1980). Accommodation in vertebrates: a contemporary survey. In Current Topics in Eye Research, ed. Zadunaisky, J.A. & Davson, H., pp. 281–330. New York: Academic Press.
Sivak, J.G. (1982). Optical characteristics of the eye of the flounder. Journal of Comparative Physiology 146, 345–349.Google Scholar
Sivak, J.G. (1988). Optics of amphibious eyes in vertebrates. In Sensory Biology of Aquatic Animals, eds. Atema, J., Fay, R.R., Popper, A.N. & Tavolga, W.N., pp. 467–486. New York: Springer-Verlag.
Sivak, J.G. (1990). The optical variability of the fish lens. In The Visual System of Fish, eds. Douglas, R.H. & Djamgoz, M.B.A., pp. 63–80. London: Chapman & Hall.
Sivak, J.G., Herbert, K.L., Peterson, K.L. & Kuszak, J.R. (1994). The interrelationship of lens anatomy and optical quality I. Non-primate lenses. Experimental Eye Research 59, 505–520.Google Scholar
Sivak, J.G. & Kreuzer, R.O. (1983). Spherical aberration of the crystalline lens. Vision Research 23, 59–70.Google Scholar
Sivak, J.G., Levy, B., Weber, A.P. & Glover, R.F. (1985). Environmental influence on shape of the crystalline lens: The amphibian example. Experimental Biology 44, 29–40.Google Scholar
Sivak, J.G. & Luer, C.A. (1991). Optical development of the ocular lens of an elasmobranch (Raja elanteria). Vision Research 31, 373–382.Google Scholar
Somiya, H. (1987). Dynamic mechanism of visual accommodation in teleosts: structure of the lens muscle and its nerve control. Proceedings of the Royal Society of London, series B 230, 77–91.Google Scholar
Steinach, E. (1890). Untersuchungen zur vergleichenden physiologie der Iris. Pflügers Archiv für die Gesamte Physiologie des Menschen und der Tiere 47, 289–340.Google Scholar
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, 536–557.Google Scholar
Tansley, K. (1965). Vision in Vertebrates. London: Chapman and Hall.
Tohyama, Y., Ichimiya, T., Kasama-Yoshida, H., Cao, Y., Hasegawa, M., Kojima, H., Tamai, Y. & Kurihara, T. (2000). Phylogentic relation of lungfish indicated by the amino acid sequence of myelin DM20. Molecular Brain Research 80, 256–259.Google Scholar
Venkatesh, B., Mark, E.V. & Brenner, S. (2001). Molecular synapomorphies resolve evolutionary relationships of extant jawed vertebrates. Proceedings of the National Academy of Sciences of the USA 98, 11382–11387.Google Scholar
Walls, G. (1942). The Vertebrate Eye and its Adaptive Radiation. New York: Hafner Publishing Company.
Walls, G.L. & Judd, H.D. (1933). The intra-ocular colour filters of vertebrates. British Journal of Ophthalmology 17, 641–675; 705–725.Google Scholar
Yokobori, S., Hasegawa, M., Ueda, T., Okada, N., Nishikawa, K. & Watanabe, K. (1994). Relationship among coelacanths, lungfishes, and tetrapods—a phylogenetic analysis based on mitochondrial cytochrome-oxidaseI gene sequences. Journal of Molecular Evolution 38, 602–609.Google Scholar
Young, J.Z. (1933). Comparative studies on the physiology of the iris. II. Uranoscopus and Lophius. Proceedings of the Royal Society of London, series B 112, 242–249.Google Scholar