Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-10T17:00:46.688Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparative visual function in elasmobranchs: Spatial arrangement and ecological correlates of photoreceptor and ganglion cell distributions

Published online by Cambridge University Press:  01 July 2008

LENORE LITHERLAND  and
SHAUN P. COLLIN
LENORE LITHERLAND*
Affiliation:
Sensory Neurobiology Group, School of Biomedical Science, The University of Queensland, Brisbane, Australia
SHAUN P. COLLIN
Affiliation:
Sensory Neurobiology Group, School of Biomedical Science, The University of Queensland, Brisbane, Australia
*
*Address correspondence and reprint requests to: Lenore Litherland, Sensory Neurobiology Group, School of Biomedical Science, The University of Queensland, Brisbane 4072, Australia. E-mail: l.litherland@uq.edu.au
Get access Rights & Permissions [Opens in a new window]

Abstract

The topographic analysis of retinal ganglion and photoreceptor cell distributions yields valuable information for assessing the visual capabilities and behavioral ecology of vertebrates. This study examines whole-mounted retinas of four elasmobranch species, the ornate wobbegong, Orectolobus ornatus; the whitetip reef shark, Triaenodon obesus; the epaulette shark, Hemiscyllium ocellatum; and the east Australia shovelnose ray, Aptychotrema rostrata, for regional specializations mediating zones of improved visual ability. These species represent a range of lifestyles: benthic, mid-water, diurnal, and nocturnal. Both photoreceptors (visualized using differential interference contrast optics) and ganglion cells (stained with cresyl violet) in the retina are extensively sampled, and their spatial distribution is found to be nonuniform, exhibiting areae or “visual streaks.” In general, the topographic distributions of both cell populations are in register and match well with respect to the location of regions of high density. However, the location of peaks in rod and cone densities can vary within a retina, indicating that preferential sampling of different regions of the visual field may occur in photopic and scotopic vision. Anatomical measures of the optical limits of resolving power, indicated by intercone spacing, range from 3.8 to 13.1 cycles/deg. Spatial limits of resolving power, calculated from ganglion cell spacing, range from 2.6 to 4.3 cycles/deg. Summation ratios, assessed by direct comparison of cell densities of photoreceptors (input cells) and ganglion cells (output cells), at more than 150 different loci across the retina, show topographic differences in signal convergence (ranging from 25:1 to over 70:1). Species-specific retinal specializations strongly correlate to the habitat and feeding behavior of each species.

Keywords

Visual ecologyRetinal topographyPhotoreceptorsGanglion cellsElasmobranchs
Type
Research Articles
Information
Visual Neuroscience , Volume 25 , Issue 4 , July 2008 , pp. 549 - 561
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ali, M.A. & Anctil, M. (1974). Retinas of the electric ray (Narcine brasiliensis) and the freshwater stingray (Paratrygon motoro). Vision Research 14, 587–588.CrossRefGoogle ScholarPubMed
Ali, M.A. & Klyne, M.A. (1985). Phylogeny and functional morphology of the vertebrate retina. In Vertebrate Morphology, ed. Duncker, H.R. & Fleischer, G. pp. 633–648. Stuttgart, Germany: Gustav Fischer Verlag.Google Scholar
Bozzano, A. (2004). Retinal specialisations in the dogfish, Centroscymnus coelolepis from the Mediterranean deep-sea. Scientia Marina 68, 185–195.CrossRefGoogle Scholar
Bozzano, A. & Collin, S.P. (2000). Retinal ganglion cell topography in elasmobranchs. Brain, Behaviour and Evolution 55, 191–208.CrossRefGoogle ScholarPubMed
Bozzano, A., Murgia, R., Vallerga, S., Hirano, J. & Archer, S. (2001). The photoreceptor system in the retinae of two dogfishes, Scyliorhinus canicula and Galeus malastomus: Possible relationship with the depth distribution and predatory lifestyle. Journal of Fish Biology 59, 1258–1278.CrossRefGoogle Scholar
Braekevelt, C.R. (1992). Photoreceptor fine structure in the southern fiddler ray (Trygonorhina fasciata). Histology and Histopathology 7, 283–289.Google ScholarPubMed
Braekevelt, C.R. (1994). Retinal photoreceptor fine structure in the short-tailed stingray (Dasyatis brevicaudata). Histology and Histopathology 9, 507–514.Google ScholarPubMed
Carraro, R. & Gladstone, W. (2006). Habitat preference and site fidelity of the ornate wobbegong shark (Orectolobus ornatus) on rocky reefs of New South Wales. Pacific Science 60, 207–223.CrossRefGoogle Scholar
Cohen, J.L. & Gruber, S.H. (1985). Spectral input to lemon shark (Negaprion brevirostris) ganglion cells. Journal of Comparative Physiology 156, 579–586.CrossRefGoogle Scholar
Collin, S.P. (1988). The retina of the shovel-nosed ray, Rhinobatos batillum (Rhinobatidae): Morphology and quantitative analysis of the ganglion, amacrine and bipolar cell populations. Journal of Experimental Biology 47, 195–207.Google ScholarPubMed
Collin, S.P. (2008). A web-based archive for topographic maps of retinal distribution in vertebrates. Clinical and Experimental Optometry 91, 85–95.CrossRefGoogle ScholarPubMed
Collin, S.P. & Pettigrew, J.D. (1988 a). Retinal ganglion cell topography in teleosts: A comparison between Nissl-stained material and retrograde labelling from the optic nerve. Journal of Comparative Neurology 276, 412–422.CrossRefGoogle ScholarPubMed
Collin, S.P. & Pettigrew, J.D. (1988 b). Retinal topography in reef teleosts I: Some species with well-developed areae but poorly-developed streaks. Brain, Behaviour and Evolution 31, 269–282.CrossRefGoogle ScholarPubMed
Collin, S.P. & Pettigrew, J.D. (1988 c). Retinal topography in reef teleosts II: Some species with prominent horizontal streaks and high-density areae. Brain, Behaviour and Evolution 31, 283–295.CrossRefGoogle ScholarPubMed
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, Behaviour and Evolution 34, 184–192.CrossRefGoogle ScholarPubMed
Compagno, L.J.V. (1984). Sharks of the world: Carcharhiniformes. FAO Fish Synopsis 4, 251–655.Google Scholar
Compagno, L.J.V. (1990). Alternative life-history styles of cartilaginous fishes in time and space. Environmental Biology of Fishes 28, 33–75.CrossRefGoogle Scholar
Cortes, E. (1999). Standardized diet composition and trophic levels of sharks. ICES Journal of Marine Science 56, 707–717.CrossRefGoogle Scholar
Curcio, A.C., Packer, O. & Kalina, R.E. (1987). A whole mount method for sequential analysis of photoreceptor and ganglion cell topography in a single retina. Vision Research 27, 9–15.CrossRefGoogle Scholar
Fern, D. (2004). Optics and retinal anatomy of the brown banded bamboo shark, Chiloscyllium punctatum. Hons. Thesis. The University of Queensland, Brisbane, Australia.Google Scholar
Fernald, R.D. (1988). Aquatic adaptations of fish eyes. In Sensory Biology of Aquatic Animals, ed. Atema, J.F., Fay, R.R., Popper, A.N. & Tavolga, W.N., pp. 435–466. New York: Springer-Verlag.CrossRefGoogle Scholar
Fouts, W.R. & Nelson, D.R. (1999). Prey capture by the Pacific angel shark, Squatina californica: Visually mediated strikes and ambush-site characteristics. Copeia 1999, 304–312.CrossRefGoogle Scholar
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, 333–341.CrossRefGoogle Scholar
Gilbert, P.W. (1963). The visual apparatus of sharks. In Sharks and Survival, ed. Gilbert, P.W., pp. 283–326. Boston, MA: D.C. Health and Co.Google Scholar
Gilbert, P.W., Sivak, J.G. & Pelham, R.E. (1981). Rapid pupil change in selachians. Canadian Journal of Zoology 59, 560–564.CrossRefGoogle Scholar
Gruber, S.H. & Cohen, J.L. (1985). Visual system of the white shark, Carcharodon carcharias, with emphasis on retinal structure. Memoir #9: The Southern California Academy of Sciences 9, 61–72.Google Scholar
Gruber, S.H., Gulley, R.L. & Brandon, J. (1975). Duplex retina in 7 elasmobranch species. Bulletin of Marine Science 25, 353–358.Google Scholar
Gruber, S.H., Hamasaki, D.H. & Bridges, C.D.B. (1963). Cones in the retina of the lemon shark (Negaprion brevicaudatus). Vision Research 3, 397–399.CrossRefGoogle Scholar
Guthrie, D.M. & Muntz, W.R.A. (1993). Role of vision in fish behaviour. In Behaviourof teleost fishes, ed. Pitcher, T.J., 2nd edition, pp. 89–128. London: Chapman & Hall.CrossRefGoogle Scholar
Hamasaki, D.I. & Gruber, S.H. (1965). The photoreceptors of the nurse shark, Ginglymostoma cirratum and the sting ray, Dasyatis sayi. Bulletin of Marine Science 15, 1051–1059.Google Scholar
Hart, N.S., Lisney, T.J., Marshall, N.J. & Collin, S.P. (2004). Multiple cone visual pigments and the potential for trichromatic colour vision in two species of elasmobranch. Journal of Experimental Biology 207, 4587–4594.CrossRefGoogle ScholarPubMed
Hart, S.N., Lisney, T.J. & Collin, S.P. (2006). Visual communication in elasmobranchs. In Communication in Fishes, ed. Ladich, F., Collin, S.P., Moller, P. & Kapoor, B.G., pp. 337–372. Plymouth, UK: Science Publishers.Google Scholar
Heupel, M.R. & Bennett, M.B. (1998). Observations on the diet and feeding habits of the epaulette shark, Hemiscyllium ocellatum (Bonnaterre), on Heron Island Reef, Great Barrier Reef, Australia. Marine and Freshwater Research 49, 753–756.CrossRefGoogle Scholar
Hobson, E.S. (1963). Feeding behaviour in three different species of sharks. Pacific Science 17, 171–194.Google Scholar
Hueter, R.E. (1991). Adaptations for spatial vision in sharks. Journal of Experimental Zoology Supplement 5, 130–141.Google Scholar
Hughes, A. (1977). The topography of vision in mammals of contrasting life style: Comparative optics and retinal organisation. In The Visual System in Vertebrates, Vol. VII/5, ed. Crescitelli, F., pp. 613–756. Berlin: Springer Verlag.CrossRefGoogle Scholar
Hughes, A. (1981). One brush tailed possum can browse as much pasture as a 0.06 sheep which may indicate why this “arboreal” animal has a visual streak: Some comments on the “terrain” theory. Vision Research 21, 957–958.CrossRefGoogle Scholar
Kato, S. (1962). Histology if the retinas of the pacific sharks Carcharhinus melanopterus and Triaenodon obesus. Masters Thesis. The University of Hawaii, Ohau, Hawaii.Google Scholar
Kuchnow, K.P. (1971). Elasmobranch pupillary response. Vision Research 11, 1395–1397.CrossRefGoogle ScholarPubMed
Kyne, P.M. (2000). Aspects of the reproductive biology and diet of the eastern shovelnose ray, Aptychotrema rostrata (Shaw & Nodder, 1794), from Moreton Bay, Queensland. Hons. Thesis. The University of Queensland, Brisbane, Australia.Google Scholar
Last, P.R. & Stevens, J.D. (1994). Sharks and Rays of Australia. Hobart, Australia: CSIRO.Google Scholar
Lisney, T.J. (2004). Neuroethology and vision in elasmobranchs. Doctorate Thesis. The University of Queensland, Brisbane, Australia.Google Scholar
Litherland, L. (2001). Retinal topography in elasmobranchs: Interspecific and ontogenetic variations. Hons. Thesis. The University of Queensland, Brisbane, Australia.Google Scholar
Logiudice, F.T. & Laird, R.J. (1994). Morphology and density distribution of cone photoreceptors in the retina of the Atlantic stingray, Dasyatis sabina. Journal of Morphology 221, 277–289.CrossRefGoogle ScholarPubMed
Lythgoe, J.N. (1979). The Ecology of Vision. Oxford: Oxford University Press.Google Scholar
van der Meer, H.J. (1991). Ecomorphology of Photoreception in Haplochromine Cichlid Fishes. Alblasserdam, The Netherlands: Haveka B.V.Google Scholar
van der Meer, H.J. & Anker, G.C. (1984). Retinal resolving power and sensitivity of the photopic system in seven haplochromine species (Teleostei, Cichlidae). Netherlands Journal of Zoology 34, 197–209.CrossRefGoogle Scholar
O’Connell, C.P. (1963). The structure of the eye of Sardinops caerulea, Engraulis mordax and four other pelagic marine teleosts. Journal of Morphology 113, 287–319.CrossRefGoogle ScholarPubMed
Peterson, E.H. & Rowe, M.H. (1980). Different regional specializations of neurons in the ganglion cell layer and inner plexiform layer of the Californian horned shark, Heterodontus francisci. Brain Research 201, 195–201.CrossRefGoogle Scholar
Pettigrew, J.D., Dreker, B., Hopkins, S. & Brown, M. (1988). The mosaic of the retinal ganglion cells in the echolocating of bats (Microchiroptera): Estimation of visual acuity. Brain, Behaviour and Evolution 32, 39–56.CrossRefGoogle Scholar
Rodieck, R.W. (1973). The Vertebrate Retina: Principles of Structure and Function. San Francisco, CA: W.H. Freeman and Company.Google Scholar
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and trans-species comparisons. Brain, Behaviour and Evolution 23, 121–164.CrossRefGoogle ScholarPubMed
Sivak, J.G. (1991). Elasmobranch visual optics. Journal of Experimental Zoology Supplement 5, 13–21.Google Scholar
Smith, K. (2006). Eye movement and visual field in elasmobranchs. Hons. Thesis. The University of Queensland, Brisbane, Australia.Google Scholar
Stell, W.K. (1972). The structure and morphologic relations of rods and cones in the retina of the spiny dogfish, Squalus. Comparative Biochemistry and Physiology A 42, 141–151.CrossRefGoogle ScholarPubMed
Stell, W.K. & Witkovsky, P. (1973 a). Retinal structure in the smooth dogfish, Mustelus canis: General description and light microscopy of giant ganglion cells. Journal of Comparative Neurology 148, 1–32.CrossRefGoogle ScholarPubMed
Stell, W.K. & Witkovsky, P. (1973 b). Retinal structure in the smooth dogfish, Mustelus canis: Light microscopy of photoreceptor and horizontal cells. Journal of Comparative Neurology 148, 33–46.CrossRefGoogle ScholarPubMed
Stone, J. (1981). The Wholemount Handbook: A Guide to the Preparation and Analysis of Retinal Wholemounts. Sydney, Australia: Maitland Publications Pty Ltd.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.CrossRefGoogle 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, 433–448.Google Scholar
Theiss, S.M., Lisney, T.J., Collin, S.P. & Hart, N.S. (2006). Colour vision and visual ecology of the blue-spotted maskray, Dasyatis kuhlii Muller & Henle, 1814. Journal of Comparative Physiology A 193, 67–79.CrossRefGoogle ScholarPubMed
Toyoda, J., Saito, T. & Kondo, H. (1978). Three types of horizontal cells in the stingray retina: Their morphology and physiology. Journal of Comparative Neurology 179, 569–580.CrossRefGoogle ScholarPubMed
Warrant, E.J. (1999). Seeing better at night: Life style, eye design and the optimum strategy of spatial and temporal summation. Vision Research 39, 1611–1630.CrossRefGoogle ScholarPubMed
Weissburg, M.J. & Browman, H.I. (2005). Sensory biology: Linking the internal and external ecologies of marine organisms. Marine Ecology Progress Series 287, 263–265.CrossRefGoogle Scholar
Yew, D.T., Chan, Y.W., Lee, M. & Lam, S. (1984). A biophysical, morphological and morphometrical survey of the eye of the small shark (Hemiscyllium plagiosum). Anatomischer Anzeiger 155, 355–363.Google ScholarPubMed