625
Views
10
CrossRef citations to date
0
Altmetric
The H Barry Collin Research Medal Lecture

Scene through the eyes of an apex predator: a comparative analysis of the shark visual system

, PhD MSc BSc (Hons)
Pages 624-640 | Received 30 Apr 2018, Accepted 09 Jul 2018, Published online: 15 Apr 2021

REFERENCES

  • Walls GL. The Vertebrate Eye and its Adaptive Radiation. Bloomfield Hills, Michigan: Hafner Publishing Company, 1942.
  • Polyak SL. The Retina. Oxford: University Chicago Press, 1941.
  • Duke ES. System of Ophthalmology the Eye in Evolution, Vol. 1. London: Henry Kimpton, 1958.
  • Rodieck RW. The Vertebrate Retina: Principles of Structure and Function. San Francisco, California: W.H. Freeman and Company, 1973.
  • Rodieck RW. The First Steps in Seeing. Sunderland, Massachusetts: Sinauer Associates Inc, 1998.
  • Crescitelli F. The visual pigments of geckos and other vertebrates: an essay in comparative biology. In: Crescitelli F, ed. Handbook of Sensory Physiology. The Visual System in Vertebrates. Berlin: Springer‐Verlag, 1977. pp. 391–449.
  • Schwab IR. Evolution's Witness: How Eyes Evolved. Oxford: Oxford University Press, 2012.
  • Collin SP. Specialisations of the teleost visual system: adaptive diversity from shallow‐water to deep‐sea. Acta Physiol Scand 1997; 161: 5–24.
  • Collin SP, Shand J. Retinal sampling and the visual field in fishes. In: Collin SP, Marshall NJ, eds. Sensory Processing in Aquatic Environments. New York, New York: Springer‐Verlag, 2003. pp. 139–169.
  • Moore BA, Tyrell LP, Kamilar JM et al. Structure and function of regional specializations in the vertebrate retina. In: Kaas J, ed. Evolution of Nervous Systems, Vol. 1, 2nd ed. Oxford: Elsevier Publishers, 2017. pp. 351–372.
  • Hughes A. The topography of vision in mammals of contrasting life style: comparative optics and retinal organization. In: Crescitelli F, ed. The Visual System of Vertebrates, Handbook of Sensory Physiology Vol 7/5. Berlin, Heidelberg: Springer, 1977. pp. 613–756.
  • Harkness L, Bennett‐clark HC. The deep fovea as a focus indicator. Nature 1978; 272: 814–816.
  • Stone J, Halasz P. Topography of the retina in the elephant Loxodonta africana. Brain Behav Evol 1989; 34: 84–95.
  • Coimbra JP, Hart NS, Collin SP et al. Scene from above: retinal ganglion cell topography and spatial resolving power in the giraffe (Giraffa camelopardalis). J Comp Neurol 2013; 15: 2042–2057.
  • Coimbra JP, Collin SP, Hart NS. Topographic specialisations in the retinal ganglion cell layer correlate with lateralized visual behaviour, ecology and evolution in cockatoos. J Comp Neurol 2014; 522: 3363–3385.
  • Coimbre JP, Kaswera‐kyamakya C, Gilissen E et al. The topographic organisation of retinal ganglion cell density in an unusual arboreal and slow‐moving strepsirhine primate, the potto (Periodicticus potto). Brain Behav Evol 2016; 87: 4–18.
  • Compagno L, Dando M, Fowler S. Sharks of the World. London: Harper Collins Publishers Ltd., 2004.
  • Kelley J, Chapuis L, Davies WIL et al. Sensory system responses to human‐induced environmental change. Front Ecol Evol 2018; https://doi.org/10.3389/fevo.2018.00095.
  • Westbrook V, Collin SP, Crawford D et al. Sharks in the Arts: From Feared to Revered. Abingdon: Routledge, 2018.
  • Compagno LJV. Alternative life‐history styles of cartilaginous fishes in time and space. Environ Biol Fishes 1990; 28: 33–75.
  • Cortes E. Standardised diet composition and trophic levels of sharks. ICES J Mar Sci 1999; 56: 707–717.
  • Myers RA, Baum JK, Shepherd TD et al. Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 2007; 315: 1846–1850.
  • Carrier JC, Musick JA, Heithaus MR. Biology of Sharks and their Relatives. London: CRC Press, 2004.
  • Emde G, Mogdans J, Kapoor BG. The Senses of Fish. Adaptations for the Reception of Natural Stimuli. Dordrecht: Kluwer Academic Publishers, 2004.
  • Yopak KE, Lisney TJ, Collin SP. Not all sharks are “swimming noses”: variation in olfactory bulb size in cartilaginous fishes. Brain Struct Funct 2014; 220: 1127–1143.
  • Collin SP, Kempster R, Yopak KE. How elasmobranchs sense their environment. In: Shadwick RE, Farrell AP, Brauner CJ, eds. Physiology of Elasmobranch Fishes: Structure and Interaction with Environment. Vol 34A, 1st ed. New York, New York: Elsevier, 2015. pp. 19–99.
  • Collin SP, Hart NS. Vision and photoentrainment in fishes: the effects of natural and anthropogenic perturbation. Integr Zool 2015; 10: 15–28.
  • Jerlov NG. Marine Optics. Amsterdam: Elsevier Scientific Publishers, 1976.
  • Levine JS, Macnicol EF. Colour vision in fishes. Sci Am 1982; 246: 140–149.
  • Bonfil R, Meÿer M, Scholl MC et al. Transoceanic migration, spatial dynamics, and population linkages of white sharks. Science 2005; 310: 100–103.
  • Knip DM, Heupel MR, Simpfendorfer CA. Sharks in nearshore environments: models, importance, and consequences. Mar Ecol Prog Ser 2010; 402: 1–11.
  • Warrant E. The eyes of deep‐sea fishes and the changing nature of visual sciences with depth. Philos Trans R Soc B 2000; 355: 1155–1159.
  • Johnsen S. The Optics of Light: A Biologists Guide to Light in Nature. Princeton, New Jersey: Princeton University Press, 2012.
  • Carey FG, Scharold JV. Movements of blue sharks (Prionace glauca) in depth and course. Mar Biol 1990; 106: 329–342.
  • Cohen JL. Vision in elasmobranchs. In: Douglas RH, Djamgoz MBA, eds. The Visual System of Fish. London: Chapman and Hall, 1990. pp. 465–490.
  • Litherland L, Collin SP, Fritsches KA. Visual optics and ecomorphology of the growing shark eye: a comparison between deep and shallow water species. J Exp Biol 2009; 212: 3583–3594.
  • Grubbs RD. Ontogenetic shifts in movement and habitat use. In: Carrier JC, Musick JA, Heithaus MR, eds. Sharks and Their Relatives, Vol. II. Boca Raton, Florida: CRC Press, 2010. pp. 319–350.
  • Warrant E, Collin SP, Locket NA. Eye design and vision in deep‐sea fishes. In: Collin SP, Marshall NJ, eds. Sensory Processing in Aquatic Environments. New York, New York: Springer Verlag, 2003. pp. 303–322.
  • Claes JM, Nilsson D‐E, Straube N et al. Iso‐luminance counterillumination drove bioluminescent shark radiation. Sci Rep 2014; 4: 4328.
  • Lisney TJ, Collin SP. Brain morphology in large pelagic fishes: a comparison between sharks and teleosts. J Fish Biol 2006; 68: 532–554.
  • Gilbert PW. The visual apparatus of sharks. In: Gilbert PW, ed. Sharks and Survival. Boston, Massachusetts: D.C. Health and Co, 1963. pp. 283–326.
  • Hueter RE, Mann DA, Maruska KP et al. Sensory biology of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR, eds. Biology of Sharks and their Relatives. Boca Raton, Florida: CRC Press, 2004. pp. 325–368.
  • Mccomb DM, Tricas TC, Kajiura SM. Enhanced visual fields in hammerhead sharks. J Exp Biol 2009; 212: 4010–4018.
  • Kajiura SM. Pupil dilation and visual field in the piked dogfish, Squalus acanthias. Environ Biol Fishes 2010; 88: 133–141.
  • Litherland L, Collin SP, Fritsches KA. Eye growth in sharks: ecological implications for changes in retinal topography and visual resolution. Vis Neurosci 2006; 26: 397–409.
  • Hart NS, Lisney TJ, Collin SP. Visual communication in elasmobranchs. In: Ladich F, Collin SP, Moller P, Kapoor BG, eds. Communication in Fishes. Plymouth: Science Publishers, 2006. pp. 337–372.
  • Lisney TJ, Theiss SM, Collin SP, et al. Vision in elasmobranchs and their relatives: 21st century advances. J Fish Biol 2012; 80: 2024–2054.
  • Lisney TJ, Collin SP. Relative eye size in elasmobranchs. Brain Behav Evol 2007; 69: 266–279.
  • Newman A, Marshall NJ, Collin SP. Visual‐eyes: a quantitative analysis of the photoreceptor layer in deep‐sea sharks. Brain Behav Evol 2013; 82: 237–249.
  • Collin SP. The neuroecology of cartilaginous fishes: sensory strategies for survival. Brain Behav Evol 2012; 80: 80–96.
  • Lythgoe JN. The Ecology of Vision. Oxford: Oxford University Press, 1979.
  • Mcfarland WN. Light in the sea: the optical world of elasmobranchs. J Exp Zool 1990; 256: 3–12.
  • Tubbesing VA, Block BA. Orbital rete and red muscle vein anatomy indicate a high degree of endothermy in the brain and eye of the salmon shark. Acta Zool 2001, 2001; 81: 49–56.
  • Alexander RL. Blood supply to the eyes and brain of laminiform sharks (Lamniformes). J Zool 1998; 245: 363–369.
  • Weng KC, O'sullivan JB, Lowe CG et al. Movements, behavior and habitat preferences of juvenile white sharks Carcharodon carcharias in the eastern Pacific. Mar Ecol Prog Ser 2007; 338: 211–224.
  • Fritsches KA, Brill RW, Warrant EJ. Warm eyes provide superior vision in swordfishes. Curr Biol 2005; 15: 55–58.
  • Janvier P. Early Vertebrates. Oxford: Oxford University Press, 1996.
  • Hildebrand M, Goslow G. Analysis of Vertebrate Structure. New York, New York: John Wiley & Sons Inc, 2001.
  • Harris AJ. Eye movements of the dogfish Squalus acanthias L. J Exp Biol 1965; 43: 107–138.
  • Land MF. Eye movements of vertebrates and their relation to eye form and function. J Comp Physiol A 2015; 201: 195.
  • Neil DM. Compensatory eye movements. In: Sandeman DC, Atwood HL, eds. Neural Integration and Behaviour. New York, New York: Academic, 1982. pp. 133–163.
  • Land MF. 1995. The function of eye movements in animals remote from man. In: Findlay JM, Walker R, Kentridge RW, eds. Eye Movement Research. Mechanisms, Processes and Application. Amsterdam: Elsevier, 1995. pp. 63–76.
  • Fritsches KA. Eye Movement Strategies and Vision in Teleost Fish. PhD Thesis. The University of Queensland. 1999.
  • Collewijn H. The normal range of horizontal eye movements in the rabbit. Exp Neurol 1970; 28: 132–143.
  • Collewijn H. The Oculomotor System of the Rabbit and its Plasticity. Berlin: Springer‐Verlag, 1981.
  • Lisberger SG, Miles FA, Optican LM et al. Optokinetc response in monkey: underlying mechanisms and their sensitivity to long‐term adaptive changes in vestibuloocular reflex. J Neurophysiol 1981; 45: 869–890.
  • Keng MJ, Anastasio TJ. The horizontal optokinetic response of the goldfish. Brain Behav Evol 1997; 49: 214–229.
  • Fritsches KA, Marshall NJ. A new category of eye movements in a small fish. Curr Biol 1999; 9: R272–R273.
  • Maxwell SS. Labyrinth and equilibrium : iii. The mechanism of the static functions of the labyrinth. J Gen Physiol 1920; 3: 157–162.
  • Ryan LA, Hart NS, Collin SP et al. Visual resolution and contrast sensitivity in two benthic sharks. J Exp Biol 2016; 219: 3971–3980.
  • Harahush BK, Hart NS, Green K et al. Retinal neurogenesis and ontogenetic changes in the visual system of the brown banded bamboo shark, Chiloscyllium punctatum (Hemiscyllidae, Elasmobranchii). J Comp Neurol 2009; 513: 83–97.
  • Schieber NL, Collin SP, Hart NS. Comparative retinal anatomy in four species of elasmobranch. J Morphol 2012; 273: 423–440.
  • Ryan LA, Hemmi JM, Collin SP et al. Electrophysiological measures of temporal resolution, contrast sensitivity and spatial resolving power in sharks. J Comp Physiol A 2017; 203: 197–210.
  • Davson H, Grant CT. Osmolarities of some body fluids in the elasmobranch and teleost. Biol Bull 1960; 119: 293.
  • Bunt SM. Evolution of vision in fishes. In: Gregory RL, ed. Evolution of the Eye and Visual System, Vol. 2. Basingstoke, London: Macmillan Press Ltd, 1991. pp. 398–420.
  • Gruber SH, Cohen JL. Visual system of the elasmobranchs: State of the art 1960‐1975. In: Hodgson ES, Mathweson RF, eds. Sensory Biology of Sharks, Skates and Rays. Arlington, Virginia: Office of Naval Research. Department of the Navy, 1978. pp. 11–105.
  • Bozzano A, Murgia R, Vallerga S et al. The photoreceptor system in the retinae of two dogfishes, Scyliorhinus canicula and Galeus melastomus: possible relationship with depth distribution and predatory lifestyle. J Fish Biol 2001; 59: 1258–1278.
  • Charman WN. The vertebrate dioptric apparatus. In: Cronly‐dillon JR, Gregory RL, eds. Vision and Visual Dysfunction: Evolution of the Eye and Visual System, Vol. 2. London: The Macmillan Press Ltd, 1991. pp. 82–117.
  • Kuchnow KP. Elasmobranch pupillary response. Vision Res 1971; 11: 1395–1406.
  • Gilbert PW, Sivak JG, Pelham RE. Rapid pupil change in selachians. Can J Zool 1981; 59: 560–564.
  • Douglas RH, Harper RD, Case JF. The pupil response of a teleost fish, Porichthys notatus: description and comparison to other species. Vision Res 1998; 38: 2697–2710.
  • Zigman S, Munro G, Lerman S. A study of the DNA of dogfish corneal epithelium. Invest Ophthalmol 1965; 4: 222–225.
  • Collin SP, Collin HB. The fish cornea: adaptations for different aquatic environments. In: Kapoor BG, Hara TJ, eds. Sensory Biology of Jawed Fishes ‐ New Insights. Enfield, Connecticut: Science Publishers Inc, 2001. pp. 57–96.
  • Collin HB, Collin SP. The corneal surface structure in aquatic vertebrates: microprojections with optical and nutritional function? Philos Trans R Soc B 2000; 355: 1171–1176.
  • Keller N, Pouliquen Y. Ultrastructural study of posterior cornea in cartilaginous fishes. In: Cavanagh HD, ed. The Cornea: Transactions of the World Congress on the Cornea III. New York, New York: Raven Press, 1988. pp. 153–158.
  • Yee RW, Edelhauser HF, Stern ME. Specular microscopy of vertebrate corneal endothelium: a comparative study. Exp Eye Res 1987; 44: 703–714.
  • Ranvier L. Lecons d'Anatomie Generale Faites au College de France 9th Lecon, la Cornee. Paris: Librairie J.B. Baillere et fils, 1878.
  • Poscai AN, de Sousa rangel B, da Silva casas A et al. Microscopic aspects of the nictitating membrane in Carcharinidae and Sphyrnidae sharks: a preliminary study. Zoomorphology 2017; 136: 359–364.
  • Ritter EK, Godknecht AJ. Agonistic displays in the blacktip shark (Carcharhinus limbatus). Copeia 2000; 2000: 282–284.
  • Fernald RD. The optical system of fishes. In: Douglas RH, Mba D, eds. The Visual System of Fish. London: Chapman and Hall, 1990. pp. 45–61.
  • Sivak JG. Refraction and accommodation of the elasmobranch eye. In: Hodgson ES, Mathewson MF, eds. Sensory Biology of Elasmobranchs. U.S. Government Printing Office, Sensory Biology of Sharks, Skates and Rays. Arlington, Virginia: Office of Naval Research. Department of the Navy, 1976. pp. 107–116.
  • Lisney TJ, Collin SP. Retinal ganglion cell distribution and spatial resolving power in elasmobranchs. Brain Behav Evol 2008; 72: 59–77.
  • Matthiessen L. Untersuchungen über dem Aplanatismus und die Periscopie der Kristallinsen in den Augen der Fische. Pflüg Arch 1880; 21: 287–307.
  • Matthiessen L. 1882. Über den physikalisch‐optischen Bau des Auges der Cetacean und der Fische. Pflug Arch Ges Phys 1882; 38: 521–528.
  • Hueter RE. Adaptations for spatial vision in sharks. J Exp Zool 1991; 1991: 130–141.
  • Hueter RE, Gruber SH. Retinoscopy of aquatic eyes. Vision Res 1980; 20: 197–200.
  • Sivak JG, Luer CA. Optical development of the ocular lens of an elasmobranch, Raja eglanteria. Vision Res 1991; 31: 373–382.
  • Clayton RM. Comparative aspects of lens proteins. In: Davson H, Graham LT, eds. The Eye, Vol. 5. New York, New York: Academic Press, 1974. pp. 399–494.
  • Sivak JG. Elasmobranch visual optics. J Exp Zool 1990; 256: 13–21.
  • Land MF, Nilsson DE. Animal Eyes. Oxford: Oxford University Press, 2002.
  • Sivak JG. A survey of vertebrate strategies for vision in air and water. In: Ali MA, ed. Sensory Ecology. NATO Advanced Study Institutes Series (Series A: Life Sciences), Vol. 18. Boston, Massachusetts: Springer, 1978. pp. 503–519.
  • Siebeck UE, Marshall NJ. Ocular media transmission in coral reef fish ‐ can coral reef fish see ultraviolet light? Vision Res 2001; 41: 133–149.
  • Losey GS, Mcfarland WN, Loew ER et al. Visual biology of Hawaiian coral reef fishes. I. Ocular transmission and visual pigments. Copeia 2003; 2003: 433–454.
  • Thorpe A, Douglas RH. Spectral transmission and short‐wave absorbing pigments in the fish lens – II. Effects of age. Vision Res 1993; 33: 301–307.
  • Franz V. Die Akkommodation des Selachierauges und seine Abbledungs apparate nebst Befunden an der Retina. Zool Jb Abt Allg Zool Physiol Tiere 1931; 19: 323–462.
  • Sivak JG, Gilbert PW. Refractive and histological study of accommodation in two species of sharks (Ginglymostoma cirratum and Carcharhinus milberti). Can J Zool 1976; 54: 1811–1817.
  • Hueter RE, Murphy CJ, Howland M et al. Refractive state and accommodation in the eyes of free‐swimming versus restrained juvenile lemon sharks (Negaprion brevirostris). Vision Res 2001; 41: 1885–1889.
  • Dowling JE. The Retina: An Approachable Part of the Brain. Cambridge: Harvard University Press, 1987.
  • Wagner HJ. Retinal structure of fishes. In: Douglas RH, Djamgoz MBA, eds. The Visual System of Fish, Vol. 1990. London: Chapman and Hall, 1990. pp. 109–157.
  • Archer SN. Light and photoreception: visual pigments and photoreception. In: Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S, eds. Adaptive Mechanisms in the Ecology of Vision. Dordrecht: Kluwer Academic Publishers, 1999. pp. 25–41.
  • Cohen JL. Functional Organization of the Retina of the Lemon Shark (Negaprion brevirostris, Poey): An Anatomical and Electrophysiological Approach. PhD Thesis, University of Miami, Miami, Florida. 1980.
  • Stell WK, Witkovsky P. Retinal structure in the smooth dogfish, Mustelus canis: light microscopy of photoreceptor and horizontal cells. J Comp Neurol 1973; 148: 33–46.
  • Collin SP, Potter IC. 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 Behav Evol 2000; 55: 120–138.
  • Collin SP. Behavioural ecology and retinal cell topography. In: Archer SN, Djamgoz MBA, Loew E, Partridge JC, Vallerga S, eds. Adaptive Mechanisms in the Ecology of Vision. Great Britain: Kluwer Academic Publishers, 1999. pp. 509–535.
  • Hart NS, Theiss SM, Harahush BK et al. Microspectrophotometic evidence for cone monochromacy in sharks. Naturwissenschaften 2011; 98: 193–201.
  • Gruber SH. Duplex vision in the elasmobranchs: histological, electrophysiological and psychophysical evidence. In: Ali MA, ed. Vision in Fishes: New Approaches in Research. New York, New York: Plenum Press, 1975. pp. 525–540.
  • Kohbara J, Niwa H, Oguri M. Comparative light microscopic studies on the retina of some elasmobranch fishes. Bull Jpn Soc Sci Fish 1987; 53: 2117–2125.
  • Stell WK, Detwiler PB, Wagner HG et al. Giant retinal ganglion cells in dogfish (Mustelus): electrophysiology of single on‐centre units. V. In: Ali MA, ed. Vision in Fishes. NATO Advanced Study Institutes Series (Series A: Life Sciences), Vol. 1. Boston, Massachusetts: Springer, 1975. pp. 99–112.
  • Bozzano A, Collin SP. Retinal ganglion cell topography in elasmobranchs. Brain Behav Evol 2000; 55: 191–208.
  • Anctil M, Ali MA. Giant ganglion cells in the retina of the hammerhead shark (Sphyrna lewini). Vision Res 1974; 14: 903–904.
  • Bridges CDB. The rhodopsin–porphyropsin visual system. In: Dartnall HJA, ed. Handbook of Sensory Physiology, Vol. VII. Berlin: Springer‐Verlag, 1972. pp. 417–480.
  • Whitmore AV, Bowmaker JK. Seasonal variation in cone sensitivity and shortwave absorbing visual pigments in the rudd, Scardinius erythrophthalmus. J Comp Physiol A 1989; 166: 103–115.
  • Parry JW, Bowmaker JK. Visual pigment reconstitution in intact goldfish retina using synthetic retinaldehyde isomers. Vision Res 2000; 40: 2241–2247.
  • Cohen JL, Hueter RE, Organisiak DT. The presence of a porphyropsin‐based visual pigment in the juvenile lemon shark (Negaprion brevirostris). Vision Res 1990; 30: 1949–1953.
  • Yokoyama S. Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 2000; 19: 385–419.
  • Denton EJ, Shaw TI. The visual pigments of some deep‐sea elasmobranchs. J Mar Biol Assoc UK 1963; 43: 65–70.
  • Denton EJ, Nicol JAC. The choroidal tapeta of some cartilaginous fishes. J Mar Biol Assoc UK 1964; 44: 219–258.
  • Mcfarland WN, Munz FW. Part II. The photic environment of clear tropical seas during the day. Vision Res 1975; 15: 1063–1070.
  • Munz FW, Mcfarland WN. The significance of spectral position in the rhodopsins of tropical marine fishes. Vision Res 1973; 13: 1829–1874.
  • Frank TM, Widder EA. Comparative study of the spectral sensitivities of mesopelagic crustaceans. J Comp Physiol A 1999; 185: 255–265.
  • Douglas RH, Marshall NJ. A review of vertebrate and invertebrate ocular filters. In: Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S, eds. Adaptive Mechanisms in the Ecology of Vision. Dordrecht: Kluwer Academic Publishers, 1999. pp. 95–162.
  • Sparks JS, Schelly RC, Smith WL et al. The covert world of fish biofluorescence: a phylogenetically widespread and phenotypically variable phenomenon. PLoS ONE 2014; 9: e83259.
  • Gruber DF, Loew ER, Deheyn DD et al. Biofluorescence in catsharks (Scyliorhinidae): fundamental description and relevance for elasmobranch visual ecology. Sci Rep 2016; 6: 24751.
  • Schluessel V, Rick I, Plischke K. No rainbow for grey bamboo sharks: evidence for the absence of colour vision in sharks from behavioural discrimination experiments. J Comp Physiol A 2014; 200: 939–947.
  • Marshall NJ, Vorobyev M. The design of color signals and color vision in fishes. In: Collin SP, Marshall NJ, eds. Sensory Processing in Aquatic Environments. New York, New York: Springer, 2003. pp. 194–222.
  • Hart NS, Lisney TJ, Marshall NJ et al. Multiple cone visual pigments and the potential for trichromatic colour vision in two species of elasmobranch. J Exp Biol 2004; 207: 4587–4594.
  • Theiss SM, Lisney TJ. Collin SP, et al. Colour vision and visual ecology of the blue‐spotted maskray, Dasyatis kuhlii (Müller and Henle, 1814). J Comp Physiol A 2007; 193: 67–79.
  • Van‐eyk SM, Siebeck UE, Champ CM et al. Behavioural evidence for colour vision in an elasmobranch. J Exp Biol 2011; 214: 4186–4192.
  • Peichl L, Behrmann G, Kröger RHH. For whales and seals the ocean is not blue: a visual pigment loss in marine mammals. Eur J Neurosci 2001; 13: 1520–1528.
  • Theiss SM, Davies WL, Hart NS et al. Cone monochromacy and visual pigment spectral tuning in wobbegong sharks. Biol Lett 2012; 8: 1019–1022.
  • Davies WL, Carvalho LS, Tay BH et al. Into the blue: gene duplication and loss underlie color vision adaptations in a deep‐sea chimaera, the elephant shark Callorhinchus milii. Genome Res 2009; 19: 415–426.
  • Van‐eyk S, Champ C, Hart NS et al. Is blue the new black? Colour vision in elasmobranchs. Front Behav Neurosci 2012; https://doi.org/10.3389/conf.fnbeh.2012.27.00376.
  • Collin SP. A web‐based archive for topographic maps of retinal distribution in vertebrates. Clin Exp Optom 2008; 91: 85–95.
  • Claes JM, Partridge JC, Hart NS et al. Photon hunting in the twilight zone: visual adaptations of mesopelagic bioluminescent sharks. PLoS ONE 2014; 9: e104213.
  • Collin SP, Pettigrew JD. Retinal topography in reef teleosts. 1. Some species with well developed areae but poorly developed streaks. Brain Behav Evol 1988; 31: 269–282.
  • Fritsches KA, Marshall NJ, Warrant EJ. Retinal specializations in the blue marlin: eyes designed for sensitivity to low light levels. Mar Freshw Res 2003; 54: 333–341.
  • Collin SP, Pettigrew JD. Retinal topography in reef teleosts. II. Some species with prominent horizontal streaks and high density areae. Brain Behav Evol 1988; 31: 283–295.
  • Bozzano A. Retinal specialisations in the dogfish, Centroscymnus coelolepis from the Mediterranean deep‐sea. Sci Mar 2004; 68: 185–195.
  • Litherland L, Collin SP. Comparative visual function in elasmobranchs: spatial arrangement and ecological correlates of photoreceptor and ganglion cell distributions. Vis Neurosci 2008; 25: 549–561.
  • Strong WR. Shape discrimination and visual predatory tactics in white sharks. In: Klimley P, Ainley DG, eds. Great White Sharks: The Biology of Carcharodon carcharias. New York, New York: Academic Press, 1996. pp. 229–240.
  • Litherland L. Retinal Topography in Elasmobranchs: Interspecific and Ontogenetic Variations. Honours Thesis. The University of Queensland. 2001.
  • Claes JM, Aksnes DL, Mallefet J. Phantom hunter of the fjords: camouflage by counterillumination in a shark (Etmopterus spinax). J Exp Mar Biol Ecol 2010; 388: 28–32.
  • Collin SP, Pettigrew JD. Quantitative comparison of the limits on visual spatial resolution set by the ganglion cell layer in twelve species of reef teleosts. Brain Behav Evol 1989; 34: 184–192.
  • Snyder AW, Miller WH. Photoreceptor diameter and spacing for highest resolving power. J Opt Soc Am 1977; 67: 696–698.
  • Wässle H, Riemann HJ. The mosaic of nerve cells in the mammalian retina. Proc R Soc Lond B 1978; 200: 441–461.
  • Hart NS. Vision in the peafowl (Aves: Pavo cristatus). J Exp Biol 2002; 205: 3925–3935.
  • Theiss SM, Collin SP, Hart NS. Interspecific visual adaptations among wobbegong sharks (Orectolobidae). Brain Behav Evol 2010; 76: 248–260.
  • Mcelroy WD, Wetherbee BM, Mostello CS et al. Food habits and ontogenetic changes in the diet of the sandbar shark, Carcharhinus plumbeus, in Hawaii. Environ Biol Fishes 2006; 76: 81–92.
  • Ellis JK, Musick JA. Ontogenetic changes in the diet of the sandbar shark, Carcharhinus plumbeus, in the lower Chesapeake Bay and Virginia (USA) coastal waters. Environ Biol Fishes 2007; 80: 51–67.
  • Harahush BK, Hart NS, Collin SP. Ontogenetic changes in retinal ganglion cell distribution and spatial resolving power in the brown banded bamboos shark, Chiloscyllium punctatum (Elasmobranchii). Brain Behav Evol 2014; 83: 286–300.
  • Stell WK, Witkovsky P. Retinal structure in the smooth dogfish, Mustelus canis: general description and light microscopy of giant ganglion cells. J Comp Neurol 1973; 148: 1–32.
  • Kobayashi H. A comparative study on electroretinogram in fish, with special reference to ecological aspects. J Shimonoseki Coll Fish 1962; 11: 17–148.
  • Mccomb DM, Frank TM, Hueter RE et al. Temporal resolution and spectral sensitivity of the visual system of three coastal shark species from different light environments. Physiol Biochem Zool 2010; 83: 299–307.
  • Kalinoski M, Hirons A, Horodysky A et al. Spectral sensitivity, luminous sensitivity and temporal resolution of the visual systems in three sympatric temperate coastal shark species. J Comp Physiol A 2014; 200: 997–1013.
  • Nicol JAC. The tapetum in Scyliorhinus canicula. J Mar Biol Assoc UK 1961; 41: 271–277.
  • Best ACG, Nicol JAC. Eye‐shine in fishes: a review of ocular reflectors. Can J Zool 1980; 58: 945–956.
  • Kuchnow KP, Gilbert PW. Preliminary in vivo studies on pupillary and tapetal pigment responses in the lemon shark, Negaprion brevirostris. In: Gilbert PW, Mathewson RF, Rall DP, eds. Sharks, Skates and Rays. Baltimore, Maryland: John Hopkins University Press, 1967. pp. 465–477.
  • Heath AR, Hindman HM. The role of cyclic AMP in the control of elasmobranch ocular tapetum lucidum pigment granule migration. Vision Res 1988; 28: 1277–1285.
  • Nicol JAC, van Baalen C. Studies on the reflecting layers of fishes. Contrib Mar Sci 1968; 13: 65–88.
  • Somiya H. Fishes with eyeshine: functional morphology of guanine type tapetum lucidum. Mar Ecol Prog Ser 1980; 2: 9–26.
  • Northcutt RG. Visual pathways in elasmobranchs: organization and phylogenetic implications. J Exp Zool 1991; 5: 97–107.
  • Smeets WJAJ. Cartilaginous fishes. In: Nieuwenhuys R, ten Donkelaar HJ, Nicholson C, eds. The Central Nervous System of Vertebrates, Vol. 1. Berlin: Springer, 1998. pp. 551–654.
  • Repérant J, Miceli D, Rio JP et al. The anatomical organization of retinal projections in the shark Scyliorhinous canicula with special reference to the evolution of the selachian primary visual system. Brain Res Rev 1986; 11: 227–248.
  • Hueter RE. The organization of spatial vision in the juvenile lemon shark (Negaprion brevirostris): Retinotectal projection, retinal topography and implications for the visual ecology of sharks. Ph.D. Thesis. University of Florida, Gainesville, Florida. 1988.
  • Lisney TJ, Collin SP, Bennett MB. Volumetric analysis of sensory brain areas indicates ontogenetic shifts in the relative importance of sensory systems in elasmobranchs. Raffles Bull Zool 2007; 14: 7–15.
  • Graeber RC. Telencephalic function in elasmobranch: a behavioral perspective. In: Ebbesson SOE, ed. Comparative Neurology of the Telencephalon. New York, New York: Plenum Press, 1980. pp. 17–39.
  • Graeber RC, Schoeder DM, Jane JA et al. Visual discrimination following partial telencephalic ablations in nurse sharks (Ginglymostoma cirratum). J Comp Neurol 1978; 180: 325–344.
  • Graeber RC. Behavioral studies correlated with central nervous system integration of vision in sharks. In: Hodgson ES, Mathewson RF, eds. Sensory Biology of Sharks, Skates and Rays. Washington DC: US Govt. Printing Office, 1978. pp. 195–225.
  • Gardiner JM, Atema J, Hueter RE et al. Modulation of shark prey capture kinematics in response to sensory deprivation. Fortschr Zool 2017; 120: 42–52.
  • Gardiner JM, Atema J, Hueter RE et al. Multisensory integration and behavioral plasticity in sharks from different ecological niches. PLoS ONE 2014; 9: e93036.
  • Huveneers C, Holman D, Robbins R et al. White sharks exploit the sun during predatory approaches. Am Nat 2015; 185: 562–570.
  • Klimley AP, Ainley DG, eds. Great White Sharks: The Biology of Carcharodon carcharias. San Diego, California: Academic Press, 1996.
  • Fouts WR, Nelson DR. Prey capture by the Pacific angel shark, Squatina californica: visually mediated strikes and ambush‐site characteristics. Copeia 1999; 1999: 304–312.
  • Egeberg CA, Kempster RM, Theiss SM et al. The distribution and abundance of electrosensory pores in benthic sharks: a comparison of wobbegong (Orectolobus maculatus) and angel (Squatina australis) sharks (Elasmobranchii). Mar Freshw Res 2014; 65: 1003–1008.
  • Klimley AP. Schooling in Sphyrna lewini, a species with a low risk of predation: a nonegalitarian state. Z Tierpsychol 1985; 70: 297–319.
  • Johnson RH, Nelson DR. Agonistic display in the gray reef shark, Carcharhinus menisorrah, and its relationship to man. Copeia 1973; 1973: 76–84.
  • Gruber SH, Myrberg AA. Approaches to the study of the behavior of sharks. Am Zool 1977; 17: 471–486.
  • Pratt HL Jr, Carrier JC. A review of elasmobranch reproductive behaviour with a case study on the nurse shark, Ginglymostoma cirratum. Environ Biol Fishes 2001; 60: 157–188.
  • Sunday JM, Pecl GT, Frusher S et al. Species traits and climate velocity explain geographic range shifts in an ocean‐warming hotspot. Ecol Lett 2015; 18: 944–953.
  • Sequeira A, Mellin C, Rowat D et al. Ocean‐scale prediction of whale shark distribution. Divers Distrib 2012; 18: 504–518.
  • Baum J, Myers R, Kehler D et al. Collapse and conservation of shark populations in the Northwest Atlantic. Science 2003; 299: 389–392.
  • Clarke SC, Mcallister MK, Milner‐gulland EJ et al. Global estimates of shark catches using trade records from commercial markets. Ecol Lett 2006; 9: 1115–1126.
  • Robbins WD, Hisano M, Connolly SR et al. Ongoing collapse of coral‐reef shark populations. Curr Biol 2006; 16: 2314–2319.
  • Hisano M, Connolly SR, Robbins WD. Population growth rates of reef sharks with and without fishing on the great barrier reef: robust estimation with multiple models. PLoS ONE 2011; 6: e25028.
  • Kempster RN, Collin SP. Iconic species: Great white sharks, basking sharks and whale sharks. In: Techera E, Klein N, eds. Sharks: Conservation, Governance and Management. London and New York, New York: Earthscan Routledge, Taylor and Francis, 2014. pp. 213–235.
  • Hart NS, Collin SP. Shark senses and shark repellents. Integr Zool 2015; 10: 38–64.
  • O'connell CP, Andreotti S, Rutzen M et al. The use of permanent magnets to reduce elasmobranch encounter with a simulated beach net. 2. The great white shark (Carcharodon carcharias). Ocean Coast Manag 2014; 97: 20–28.
  • Sager DR, Hocutt CH, Stauffer JR Jr. Estuarine fish responses to strobe light, bubble curtains and strobe light/bubble‐curtain combinations as influenced by water flow rate and flash frequencies. Fish Res 1987; 5: 383–399.
  • Ryan LA, Chapuis L, Hemmi JM et al. Effects of auditory and visual stimuli on shark feeding behaviour: the disco effect. Mar Biol 2017; 165: 11.
  • Jarvik E. Basic Structure and Evolution of Vertebrates. London: Academic Press Inc, 1980.
  • Braekevelt CR. Retinal photoreceptor fine structure in the short‐tailed stingray (Dasyatis brevicaudata). Histol Histopathol 1994; 9: 507–514.
  • Weng KC, Block BA. Diel vertical migration of the bigeye thresher shark (Alopias superciliosus) a species possessing orbital retia mirabilia. Fish Bull, US 2004; 102: 221–229.
  • Gruber SH, Cohen JL. Visual system of the white shark, Carcharodon carcharias, with emphasis on retinal structure. Mem South Calif Acad Sci 1985; 9: 61–72.
  • Lisney TJ. Neuroethology and Vision in Elasmobranchs. PhD Thesis, The University of Queensland, Brisbane. 2004.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.