Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-19T11:50:06.819Z Has data issue: false hasContentIssue false
  • English
  • Français

Eye growth in sharks: Ecological implications for changes in retinal topography and visual resolution

Published online by Cambridge University Press:  24 August 2009

LENORE LITHERLAND ,
SHAUN P. COLLIN  and
KERSTIN A. FRITSCHES
LENORE LITHERLAND*
Affiliation:
Sensory Neurobiology Group, School of Biomedical Sciences, The University of Queensland, Brisbane, Queensland, Australia
SHAUN P. COLLIN
Affiliation:
Sensory Neurobiology Group, School of Biomedical Sciences, The University of Queensland, Brisbane, Queensland, Australia
KERSTIN A. FRITSCHES
Affiliation:
Sensory Neurobiology Group, School of Biomedical Sciences, The University of Queensland, Brisbane, Queensland, Australia
*
*Address correspondence and reprint requests to: Lenore Litherland, Sensory Neurobiology Group, School of Biomedical Sciences, The University of Queensland, Brisbane, Queensland 4072, Australia. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The visual abilities of sharks show substantial interspecific variability. In addition, sharks may change their habitat and feeding strategy throughout life. As the eyes of sharks continue to grow throughout the animal’s lifetime, ontogenetic variability in visual ability may also occur. The topographic analysis of the photoreceptor and ganglion cell distributions can identify visual specializations and assess changes in visual abilities that may occur concurrently with eye growth. This study examines an ontogenetic series of whole-mounted retinas in two elasmobranch species, the sandbar shark, Carcharhinus plumbeus, and the shortspine spurdog, Squalus mitsukurii, to identify regional specializations mediating zones for improved spatial resolution. The study examines retinal morphology and presents data on summation ratios between photoreceptor and ganglion cell layers, anatomically determined peak spatial resolving power, and the angular extent of the visual field. Peak densities of photoreceptors and ganglion cells occur in similar retinal locations. The topographic distribution of neurons in the ganglion cell layer does not differ substantially with eye growth. However, predicted peak spatial resolution increases with eye growth from 4.3 to 8.9 cycles/deg in C. plumbeus and from 5.7 to 7.2 cycles/deg in S. mitsukurii. The topographic distribution of different-sized ganglion cells is also mapped in C. plumbeus, and a population of large ganglion cells (soma area 120–350 μm2) form a narrow horizontal streak across the retinal meridian, while the spatial distribution of ordinary-sized ganglion cells (soma area 30–120 μm2) forms an area in the central retina. Species-specific retinal specializations highlight differences in visually mediated behaviors and foraging strategies between C. plumbeus and S. mitsukurii.

Keywords

Spatial resolving powerVisual fieldCarcharhinidaeSqualidaeVisual ecology
Type
Research Articles
Information
Visual Neuroscience , Volume 26 , Issue 4 , July 2009 , pp. 397 - 409
Copyright
Copyright © Cambridge University Press 2009

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

Anctil, M. & Ali, M.A. (1974). Giant ganglion cells in the retina of the hammerhead shark (Sphyrna lewini). Vision Research 14, 903–905.CrossRefGoogle ScholarPubMed
Archer, S.N. (1999). Light and photoreception: Visual pigments and photoreception. In Adaptive Mechanisms in the Ecology of Vision, ed. Archer, S.N., Djamgoz, B.A., Loew, E.R., Partridge, J.C. & Vallerga, S., pp. 413–437. London: Kluwer Academic Publishers.CrossRefGoogle Scholar
Barbour, H.R., Archer, M.A., Ghart, N.S., Thomas, N., Dunlop, S.A., Beazley, L.D. & Shand, J. (2002). Retinal characteristics of the ornate dragon lizard, Ctenophorus ornatus. The Journal of Comparative Neurology 450, 334–344.CrossRefGoogle ScholarPubMed
Beaudet, L. & Hawryshyn, C.W. (1999). Ecological Aspects of Vertebrate Visual Ontogeny. Dordrecht, The Netherlands: Kluwer.Google Scholar
Bozzano, A. (2004). Retinal specialisations in the dogfish, Centroscymnus coelolepis from the Mediterranean deep-sea. Scientia Marina 68, 185–195.Google Scholar
Bozzano, A. & Collin, S.P. (2000). Retinal ganglion cell topography in elasmobranchs. Brain, Behavior and Evolution 55, 191–208.Google Scholar
Calderone, J.B., Reese, B.E. & Jacobs, G.H. (2003). Topography of photoreceptors and retinal ganglion cells in the spotted hyena (Crocuta crocuta). Brain, Behavior and Evolution 62, 182–192.Google Scholar
Cocker, J.E. (1978). Adaptations of deep sea fishes. Environmental Biology of Fishes 3, 389–399.Google Scholar
Coggeshall, R.E. & Lekan, H.A. (1996). Methods for determining numbers of cells and synapses: A case study for more uniform standards of review. The Journal of Comparative Neurology 364, 6–15.Google 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. The Journal of Experimental Biology 47, 195–207.Google Scholar
Collin, S.P. (1997). Specializations of the teleost visual system: Adaptive diversity from shallow-water to deep-sea. Acta Physiologica Scandinavica 161 (Suppl. 638), 5–24.Google Scholar
Collin, S.P. (1999). Behavioural ecology and retinal cell topography. In Adaptive Mechanisms in the Ecology of Vision, ed. Archer, S.N., Djamgoz, M.B.A., Loew, E.R., Partridge, J.C. & Vallerga, S., pp. 509–535. London: Kluwer Accademic Publishers.CrossRefGoogle Scholar
Collin, S.P., Hoskins, R.V. & Partridge, J.C. (1998). Seven retinal specializations in the tubular eye of the deep-sea pearleye, Scopelarchus michaelsarsi: A case study in visual optimization. Brain, Behavior and Evolution 51, 291–314.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, Behavior and Evolution 34, 184–192.Google Scholar
Collin, S.P. & Shand, J. (2003). Retinal sampling and the visual field in fish. In Sensory Processing of the Aquatic Environment, ed. Collin, S.P. & Marshall, N.J., pp. 139–169. New York: Springer.CrossRefGoogle Scholar
Compagno, L.J.V., Dando, M. & Fowler, S. (2005). A Field Guide to the Sharks of the World. London: Collins.Google Scholar
Denton, E.J. & Nicol, J.A.C. (1964). The choroidal tapeta of some cartilaginous fishes (Chondrichthyes). Journal of the Marine Biological Association of the United Kingdom 44, 219–258.CrossRefGoogle Scholar
Dunlop, S.A. & Beazley, L.D. (1981). Changing retinal ganglion cell distribution in the frog Heleioporus eyrei. The Journal of Comparative Neurology 202, 221–236.CrossRefGoogle ScholarPubMed
Easter, S.S.J., Johns, P.R. & Baumann, L.R. (1977). Growth of the adult goldfish eye—I: Optics. Vision Research 17, 469–477.Google Scholar
Ellis, J.K. & Musick, J.A. (2007). Ontogenetic changes in the diet of the sandbar shark, Carcharhinus plumbeus, in the lower Chesapeake Bay and Virginia (USA) coastal waters. Environmental Biology of Fishes 80, 51–67.CrossRefGoogle Scholar
Fernald, R.D. (1985). Growth of the teleost eye: Novel solutions to complex constraints. Environmental Biology of Fishes 13, 113–123.CrossRefGoogle Scholar
Fernald, R.D. (1988). Aquatic adaptations of fish eyes. In Sensory Biology of Aquatic Animals, ed. Atema, J., Fay, R.R., Popper, A.N. & Tavolga, W.N., pp. 435–466. New York: Springer-Verlag.CrossRefGoogle Scholar
Fernald, R.D. (1991). Teleost vision: Seeing while growing. Journal of Experimental Zoology Supplement 6, 167–180.Google 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
Grubbs, R.D., Musick, J.A., Conrath, C. & Romine, J.G. (2007). Long-term movements, migrations, and temporal delineation of a summer nursery for juvenile sandbar sharks in the Chesapeake Bay region. In Shark Nursery Grounds of the Gulf of Mexico and East Coast Waters of the United States, ed. McCandless, T., Kohler, N.E. & Pratt, H.L., American Fisheries Society Symposium 50, 63–86. Bethesda MD: American Fisheries Society.Google Scholar
Gruber, S.H. & Cohen, J.L. (1985). Visual system of the white shark, Carcharodon carcharias, with emphasis on retinal structure. The Southern California Academy of Sciences 9, 61–72.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.Google 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
Harahush, B.K., Hart, N.S., Green, K. & Collin, S.P. (2009). Retinal neurogenesis and ontogenetic changes in the visual system of the brown banded bamboo shark, Chiloscyllium punctatum (Hemiscyllidae, Elasmobranchii). The Journal of Comparative Neurology 513, 83–97.Google Scholar
Harris, A.J. (1965). Eye movements of the dogfish Squalus acanthias L. The Journal of Experimental Biology 43, 107–130.Google Scholar
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
Hayes, B.P. & Brooke, M.d.L. (1990). Retinal ganglion cell distribution and behaviour in procellariiform seabirds. Vision Research 30, 1277–1290.CrossRefGoogle ScholarPubMed
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, ed. Crescitelli, F., pp. 613–756. Berlin: Springer Verlag.Google Scholar
Kajiura, S.M. (2001). Head morphology and electrosensory pore distribution of carcharhinid and sphyrnid sharks. Environmental Biology of Fishes 61, 125–133.Google Scholar
Kato, S. (1962). Histology of the retinas of the pacific sharks Carcharhinus melanopterus and Triaenodon obesus. Masters Thesis. The University of Hawaii, Oahu, Hawaii.Google Scholar
Kohbara, J., Niwa, H. & Oguri, M. (1987). Comparative light microscopic studies on the retina of some elasmobranch fishes. Nippon Suisan Gakkaishi 53, 2117–2125.CrossRefGoogle Scholar
Lisney, T.J. & Collin, S.P. (2008). Retinal ganglion cell distribution and spatial resolving power in elasmobranchs. Brain, Behavior and Evolution 72, 59–77.CrossRefGoogle ScholarPubMed
Litherland, L. (2001). Retinal topography in elasmobranchs: Interspecific and ontogenetic variations. Hons. Thesis. The University of Queensland, Brisbane, Australia.Google Scholar
Litherland, L. (2009). Neuroethological studies on shark vision. PhD. Thesis. The University of Queensland, Brisbane, Australia.Google Scholar
Litherland, L. & Collin, S.P. (2008). Comparative visual function in elasmobranchs: Spatial arrangement and ecological correlates of photoreceptor and ganglion cell distributions. Visual Neuroscience 25, 549–561.CrossRefGoogle ScholarPubMed
Litherland, L., Collin, S.P. & Fritsches, K.A. (in press). Visual optics and ecomorphology of the growing shark eye: a Comparison between deep and shallow water species. Journal of Experimental Biology.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
Malchow, R.P., Qian, H., Ripps, H. & Dowling, J.E. (1990). Structural and functional properties of two types of horizontal cell in the skate retina. The Journal of General Physiology 95, 177–198.Google Scholar
Mass, A.M. & Supin, A.Y. (2000). Ganglion cells density and retinal resolution in the sea otter, Enhydra lutris. Brain, Behavior and Evolution 55, 111–119.Google Scholar
McAuley, R.B., Lenanton, R., Chidlow, J., Allison, R. & Heist, E.J. (2005). Biology and stock assessment of the thickskin (sandbar) shark, Carcharhinus plumbeus, in Western Australia and further refinement of the dusky shark, Carcharhinus obscurus, stock assessment. Department of Fisheries Government of Western Australia, Perth, Australia.Google Scholar
McElroy, W.D., Wetherbee, B.M., Mostello, C.S., Lowe, C.G., Crow, G.L. & Wass, R.C. (2006). Food habits and ontogenetic changes in the diet of the sandbar shark, Carcharhinus plumbeus, in Hawaii. Environmental Biology of Fishes 76, 81–92.CrossRefGoogle Scholar
McPherson, K. (2004). Retinal anatomy and optics in the mackeral tuna, Euthynnus affinis. Hons. Thesis. University of Queensland, Brisbane, Australia.Google Scholar
Murayama, T., Somiya, H., Aoki, I. & Ishii, T. (1995). Retinal ganglion cell size and distribution predict visual capabilities of Dall’s Porpoise. Marine Mammal Science 11, 136–149.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.Google Scholar
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.Google Scholar
Reymond, L. (1985). Spatial visual acuity of the eagle Aquila audax: A behavioural, optical and anatomical investigation. Vision Research 25, 1477–1491.Google Scholar
Reymond, L. (1987). Spatial visual acuity of the falcon Falco berigora: A behavioural, optical and anatomical investigation. Vision Research 27, 1859–1874.Google Scholar
Rodieck, R.W. (1973). The Vertebrate Retina: Principles of Structure and Function. San Francisco, CA: W.H. Freeman and Company.Google Scholar
Shand, J. (1997). Ontogenetic changes in retinal structure and visual acuity: A comparative study of coral-reef teleosts with different post-settlement lifestyles. Environmental Biology of Fishes 49, 307–322.Google Scholar
Shand, J., Chin, S.M., Harman, A.M. & Collin, S.P. (2000 a). The relationship between the position of the retinal area centralis and feeding behaviour in juvenile black bream Acanthopagrus butcheri (Sparidae: Teleostei). Philosophical Transactions of the Royal Society of London Series B 355, 1183–1186.Google Scholar
Shand, J., Chin, S.M., Harman, A.M., Moore, S. & Collin, S.P. (2000 b). Variability in the location of the retinal ganglion cell area centralis is correlated with ontogenetic changes in feeding behaviour in the black bream, Acanthopagrus butcheri (Sparidae, Teleostei). Brain, Behavior and Evolution 55, 176–190.Google Scholar
Stell, W.K. & Witkovsky, P. (1973 a). Retinal structure in the smooth dogfish, Mustelus canis: General description and light microscopy of giant ganglion cells. The Journal of Comparative Neurology 148, 1–32.Google Scholar
Stell, W.K. & Witkovsky, P. (1973 b). Retinal structure in the smooth dogfish, Mustelus canis: Light microscopy of photoreceptor and horizontal cells. The Journal of Comparative Neurology 148, 33–46.CrossRefGoogle ScholarPubMed
Theiss, S.M., Lisney, T.J., Collin, S.P. & Hart, N.S. (2007). Colour vision and visual ecology of the blue-spotted maskray, Dasyatis kuhlii Muller & Henle, 1814. Journal of Comparative Physiology A 193, 67–79.Google Scholar
Uemura, M., Somiya, H., Moku, M. & Kawaguchi, K. (2000). Temporal and mosaic distribution of large ganglion cells in the retina of a daggertooth aulopiform deep-sea fish (Anotopterus pharao). Philosophical Transactions of the Royal Society of London Series B 355, 1161–1166.CrossRefGoogle ScholarPubMed
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, 25–33.Google Scholar
Wagner, H.-J. (1978). Cell types and connectivity patterns in mosaic retinas. Advances in Anatomy, Embryology, and Cell Biology 55, 1–81.Google ScholarPubMed
Wagner, H.J. (1990). Retinal structure of fishes. In The Visual System of Fish, ed. Douglas, R.H. & Djamgoz, B.A., pp. 109–148. London: Chapman and Hall.CrossRefGoogle Scholar
Walls, G.L. (1942). The Vertebrate Eye and Its Adaptive Radiation. New York: Hafner.Google Scholar
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.Google Scholar
Warrant, E.J. (2000). The eyes of deep-sea fishes and the changing nature of visual scenes with depth. Philosophical Transactions of the Royal Society of London Series B 355, 1155–1159.CrossRefGoogle ScholarPubMed
Wässle, H., Peichl, L. & Boycott, B.B. (1981). Morphology and topography of on- and off-alpha ganglion cells in the cat retina. Proceedings of the Royal Society of London Series B 212, 157–175.Google Scholar
Wilson, C.D. & Seki, M.P. (1994). Biology and population characteristics of Squalus mitsukurii from a seamount in the Central North Pacific Ocean. Fishery Bulletin 92, 851–864.Google Scholar