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Basic mechanisms in pinniped vision

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Abstract

Pinnipeds are amphibious mammals. The amphibious lifestyle is challenging for all sensory systems including vision, and specific adaptations of the eyes have evolved in response to the changed requirements concerning vision in two optically very different media, water and air. The present review summarizes the information available on pinniped eyes with an emphasis on harbour seal vision for which most information is available to date. Recent studies in this species have improved the understanding of amphibious vision by reanalysing refraction, by studying corneal topography, and by measuring visual acuity as a function of ambient luminance. The harbour seal eye can be characterized as an eye that balances high resolution, supported by data on ganglion cell density and topography, and sensitivity. Furthermore, it was shown that seals have multifocal lenses, broad visual fields, and distinct eye movement abilities. The mechanisms described here form the basis for future research on visually guided behaviour.

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References

  • Bernholz CD, Matthews ML (1975) Critical flicker frequency in a harp seal: evidence for duplex retinal organization. Vis Res 15:733–736

    Article  CAS  PubMed  Google Scholar 

  • Bisti S, Maffei L (1974) Behavioural contrast sensitivity of the cat in various visual meridians. J Physiol 241:201–210

    CAS  PubMed  Google Scholar 

  • Bowmaker JK (1995) The visual pigments of fish. Prog Retin Eye Res 15:1–31

    Article  Google Scholar 

  • Busch H, Dücker G (1987) Das visuelle Leistungsvermögen der Seebären (Arctocephalus pusillus und Arctocephalus australis). Zool Anz 219(3/4):197–224

    Google Scholar 

  • Campbell FW, Maffei L, Piccolino M (1973) The contrast sensitivity of the cat. J Physiol 229:719–731

    CAS  PubMed  Google Scholar 

  • Carpenter RHS (1988) Movements of the eyes. Pion Limited, London

    Google Scholar 

  • Cornsweet TN, Pinsker HM (1965) Luminance discrimination of brief flashes under various conditions of adaptation. J Physiol 176:294–310

    CAS  PubMed  Google Scholar 

  • Crescitelli F (1958) Natural history of visual pigments. Ann N Y Acad Sci 74:230–255

    Article  CAS  Google Scholar 

  • Crognale MA, Levenson DH, Ponganis PJ et al (1998) Cone spectral sensitivity in the harbor seal (Phoca vitulina) and implications for color vision. Can J Zool 76:2114–2118

    Article  Google Scholar 

  • Dawson WW, Schroeder JP, Sharpe SN (1987) Corneal surface properties of two marine mammal species. Mar Mamm Sci 3(2):186–197

    Article  Google Scholar 

  • Dehnhardt G (2002) Sensory systems. In: Hoelzel R (ed) Marine mammal biology—an evolutionary approach. Blackwell, Oxford, pp 116–141

    Google Scholar 

  • Fasick JI, Robinson PR (1998) Mechanisms of spectral tuning in the dolphin visual pigments. Biochemistry 37:433–438

    Article  CAS  PubMed  Google Scholar 

  • Fasick JI, Robinson PR (2000) Spectral-tuning mechanisms of marine mammal rhodpsins and correlations with foraging depth. Vis Neurosci 17:781–788

    Article  CAS  PubMed  Google Scholar 

  • Fasick JI, Cronin TW, Hunt DM, Robinson PR (1998) The visual pigments of the bottlenose dolphin (Tursiops truncatus). Vis Neurosci 15:1–9

    Article  Google Scholar 

  • Geisbauer G, Griebel U, Schmid A, Timney B (2004) Brightness discrimination and neutral point testing in the horse. Can J Zool 82:660–670

    Article  Google Scholar 

  • Grasse KL, Cynader MS (1988) The effect of visual cortex lesions on vertical optokinetic nystagmus in the cat. Brain Res 455:385–389

    Article  CAS  PubMed  Google Scholar 

  • Griebel U, Peichl L (2003) Color vision in aquatic mammals—facts and open questions. Aquat Mamm 29(1):18–30

    Article  Google Scholar 

  • Griebel U, Schmid A (1992) Color vision in the California sea lion (Zalophus californianus). Vis Res 32(1):477–482

    Article  CAS  PubMed  Google Scholar 

  • Griebel U, Schmid A (1997) Brightness discrimination ability in the West Indian manatee (Trichechus manatus). J Exp Biol 200:1587–1592

    CAS  PubMed  Google Scholar 

  • Hanke FD, Dehnhardt G (2009) Aerial visual acuity in harbor seals (Phoca vitulina) as a function of luminance. J Comp Physiol A. doi:10.1007/s00359-009-0439-2

  • Hanke FD, Dehnhardt G, Schaeffel F, Hanke W (2006) Corneal topography, refractive state, and accommodation in harbor seals (Phoca vitulina). Vis Res 46:837–847

    Article  PubMed  Google Scholar 

  • Hanke W, Römer R, Dehnhardt G (2006) Visual fields and eye movements in a harbor seal (Phoca vitulina). Vis Res 46:2804–2814

    Article  PubMed  Google Scholar 

  • Hanke FD, Hanke W, Hoffmann K-P, Dehnhardt G (2008a) Optokinetic nystagmus in harbor seals (Phoca vitulina). Vis Res 48(2):304–315

    Article  PubMed  Google Scholar 

  • Hanke FD, Kröger RHH, Siebert U, Dehnhardt G (2008b) Multifocal lenses in a monochromat, the harbour seal. J Exp Biol 211:3315–3322

    Article  PubMed  Google Scholar 

  • Hobson ES (1966) Visual orientation and feeding in seals and sea lions. Nature 210:326–327

    Article  Google Scholar 

  • Hughes A (1975) A quantitative analysis of the cat retinal ganglion cell topography. J Comp Neurol 163:107–128

    Article  CAS  PubMed  Google Scholar 

  • Hughes A (1976) A supplement to the cat schematic eye. Vis Res 16(2):149–154

    Article  CAS  PubMed  Google Scholar 

  • Hughes A (1977) Topography of vision in mammals. In: Crescitelli F (ed) Handbook of sensory physiology. Springer, Berlin

    Google Scholar 

  • Jacobs GH, Degan JFII, Neitz J, Crognale MA, Neitz M (1993) Photopigments and color vision in the nocturnal monkey Aotus. Vis Res 33:1773–1783

    Article  CAS  PubMed  Google Scholar 

  • Jamieson GS (1970) The eye of the harbour seal, Phoca vitulina. PhD thesis, The University of British Columbia, Vancouver

  • Jamieson GS (1971) The functional significance of corneal distortion in marine mammals. Can J Zool 49:421–423

    Article  CAS  PubMed  Google Scholar 

  • Jamieson GS, Fisher HD (1970) Visual discrimination in the harbour seal Phoca vitulina, above and below water. Vis Res 10:1175–1180

    Article  CAS  PubMed  Google Scholar 

  • Jamieson GS, Fisher HD (1971) The retina of the harbour seal, Phoca vitulina. Can J Zool 49:19–23

    Article  Google Scholar 

  • Jamieson GS, Fisher HD (1972) The pinniped eye: a review. In: Harrison RJ (ed) Functional anatomy of marine mammals. Academic Press, London, pp 245–261

    Google Scholar 

  • Johnson GL (1893) Observations on the refraction and vision of the seal’s eye. Proc Zool Soc Lond 719–723

  • Johnson GL (1901) Contributions to the comparative anatomy of the mammalian eye, chiefly based on ophthalmoscopic examination. Philos Trans R Soc Biol Charact 194:1–82

    Article  Google Scholar 

  • Kröger RHH (2008) The physics of light in air and water. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold—adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, pp 113–119

    Google Scholar 

  • Kröger RHH, Katzir G (2008) Comparative anatomy and physiology of vision in aquatic tetrapods. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold—adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, pp 121–147

    Google Scholar 

  • Kröger RHH, Campbell MCW, Fernald RD, Wagner H-J (1999) Multifocal lenses compensate for chromatic defocus in vertebrate eyes. J Comp Physiol A 184:361–369

    Article  PubMed  Google Scholar 

  • Land MF, Nilsson D-E (2002) Animal eyes. Oxford University Press, Oxford

    Google Scholar 

  • Landau D, Dawson WW (1970) The histology of retinas from the pinnipedia. Vis Res 10:691–702

    Article  CAS  PubMed  Google Scholar 

  • Lavigne DM, Ronald K (1975a) Evidence of duplicity in the retina of the California sea lion (Zalophus californianus). Comp Biochem Physiol 50:65–70

    Article  CAS  Google Scholar 

  • Lavigne DM, Ronald K (1975b) Pinniped visual pigments. Comp Biochem Physiol 52(B):325–329

    CAS  Google Scholar 

  • Lavigne DM, Ronald K (1977) Functional aspects of pinniped vision. In: Harrison RJ (ed) Functional anatomy of marine mammals. Academic Press, London, pp 135–173

    Google Scholar 

  • Levenson DH, Schusterman RJ (1997) Pupillometry in seals and sea lions: ecological implications. Can J Zool 75:2050–2057

    Article  Google Scholar 

  • Levenson DH, Schusterman RJ (1999) Dark adaptation and visual sensitivity in shallow and deep-diving pinnipeds. Mar Mamm Sci 15(4):1303–1313

    Article  Google Scholar 

  • Levenson DH, Ponganis PJ, Crognale MA et al (2006) Visual pigments of marine carnivores: pinnipeds, polar bear, and sea otter. J Comp Physiol A 192(8):833–843

    Article  CAS  Google Scholar 

  • Lythgoe JP (1975) Problems of seeing colors underwater. In: Ali MA (ed) Vision in fishes: new approaches in research. Plenum Press, New York, pp 619–634

    Google Scholar 

  • Lythgoe JN, Dartnall HJA (1970) A ‘deep sea rhodopsin’ in a marine mammal. Nature 227:995–996

    Article  Google Scholar 

  • Mass AM, Supin AY (1992) Peak density, size and regional distribution of ganglion cells in the retina of the fur seal Callorhinuns ursinus. Brain Behav Evol 39:69–76

    Article  CAS  PubMed  Google Scholar 

  • Mass AM, Supin AY (2003) Retinal topography of the harp seal Pagophilus groenlandicus. Brain Behav Evol 62:212–222

    Article  PubMed  Google Scholar 

  • Mass AM, Supin AY (2005) Ganglion cell topography and retinal resolution of the Steller sea lion (Eumetobias jubatus). Aquat Mamm 31(4):393–402

    Article  Google Scholar 

  • Mauck B, Dehnhardt G (1997) Mental rotation in a California sea lion (Zalophus californianus). J Exp Biol 200:1309–1316

    CAS  PubMed  Google Scholar 

  • McFarland WN (1971) Cetacean visual pigments. Vis Res 11:1065–1076

    Article  CAS  PubMed  Google Scholar 

  • Murphy CJ, Bellhorn RW, Williams T et al (1990) Refractive state, ocular anatomy, and accommodative range of the sea otter (Enhydra lutris). Vis Res 30(1):23–32

    Article  CAS  PubMed  Google Scholar 

  • Nagy AR, Ronald K (1970) The harp seal, Pagophilus groenlandicus (Erxleben 1777). VI. Structure of the retina. Can J Zool 48:367–370

    Article  CAS  PubMed  Google Scholar 

  • Newman LA, Robinson PR (2005) Cone visual pigments of aquatic mammals. Vis Neurosci 22:873–879

    Article  PubMed  Google Scholar 

  • Peichl L (1992) Topography of ganglion cells in the dog and wolf retina. J Comp Neurol 324:603–620

    Article  CAS  PubMed  Google Scholar 

  • Peichl L, Moutairou K (1998) Absence of short-wavelength sensitive cones in the retinae of seals (Carnivora) and African giant rats (Rodentia). Eur J Neurosci 10:2586–2594

    Article  CAS  PubMed  Google Scholar 

  • Peichl L, Behrmann G, Kröger RHH (2001) For whales and seals the ocean is not blue: a visual pigment loss in marine mammals. Eur J Neurosci 13:1520–1528

    Article  CAS  PubMed  Google Scholar 

  • Piggins DJ (1970) Refraction of the harp seal, Pagophilus groenlandicus (Erxleben 1777). Nature 227:78–79

    Article  CAS  PubMed  Google Scholar 

  • Pütter A (1903) Die Augen der Wassersäugetiere. Zool Jahrb Anat Ontogenie 17:99–402

    Google Scholar 

  • Rahmann H (1967) Die Sehschärfe bei Wirbeltieren. Nat Rundsch 1:10–14

    Google Scholar 

  • Reitner A, Sharpe LT, Zrenner E (1991) Is colour vision possible with only rods and blue-sensitive cones? Nature 352:798–800

    Article  CAS  PubMed  Google Scholar 

  • Renouf D (1991) Sensory reception and processing in Phocidae and Otariidae. In: Renouf D (ed) Behaviour in pinnipeds. University Press, Cambridge

    Google Scholar 

  • Reuter T, Peichl L (2008) Structure and function of the retina in aquatic tetrapods. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold—adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, pp 149–172

    Google Scholar 

  • Schaeffel F, Farkas L, Howland HC (1987) Infrared photoretinoscope. Appl Opt 26(8):1505–1508

    Article  Google Scholar 

  • Schieber F (1992) Aging and the senses. In: Birren JE, Sloan R, Cohen G (eds) Handbook of mental health and aging. Academic Press, New York, pp 251–306

    Google Scholar 

  • Scholtyssek C, Kelber A, Dehnhardt G (2008) Brightness discrimination in the harbor seal (Phoca vitulina). Vis Res 48:96–103

    Article  PubMed  Google Scholar 

  • Schor CM (1993) Development of OKN. In: Miles FA, Wallman J (eds) Visual motion and its role in the stabilization of gaze. Elsevier, Amsterdam, pp 301–320

    Google Scholar 

  • Schusterman RJ, Balliet RF (1970) Visual acuity of the harbour seal and the Steller sea lion under water. Nature 226:563–564

    Article  CAS  PubMed  Google Scholar 

  • Schusterman RJ, Balliet RF (1971) Aerial and underwater visual acuity in the California sea lion (Zalophus californianus) as a function of luminance. Ann N Y Acad Sci 188:37–46

    Article  CAS  PubMed  Google Scholar 

  • Sivak JG (1980) Accommodation in vertebrates: a contemporary survey. Curr Top Eye Res 3:281–330

    CAS  PubMed  Google Scholar 

  • Sivak JG, Howland HC, West J, Weerheim J (1989) The eye of the hooded seal, Cristophora cristata, in air and water. J Comp Physiol A 165:771–777

    Article  CAS  PubMed  Google Scholar 

  • Southall KD, Oliver GW, Lewis JW et al (2002) Visual pigment sensitivity in three deep diving marine mammals. Mar Mamm Sci 18:275–281

    Article  Google Scholar 

  • Stich KP, Dehnhardt G, Mauck B (2003) Mental rotation of perspective stimuli in a California sea lion (Zalophus californianus). Brain Behav Evol 61:102–112

    Article  CAS  PubMed  Google Scholar 

  • Supin AY, Popov VV, Mass AM (2001) The sensory physiology of aquatic mammals. Kluwer, Boston

    Google Scholar 

  • Walls GL (1942) The vertebrate eye and its adaptive radiation. Hafner Press, New York

    Google Scholar 

  • Walls GL (1962) The evolutionary history of eye movements. Vis Res 2:69–80

    Article  Google Scholar 

  • Warrant E, Locket NA (2004) Vision in the deep sea. Biol Rev 79:671–712

    Article  PubMed  Google Scholar 

  • Wartzok D (1979) Phocid spectral sensitivity curves. In: Third biennial conference on the biology of marine mammals, Seattle. Society for Marine Mammals, Lawrence, p 62

  • Wartzok D, Ketten DR (1999) Marine mammal sensory systems. In: Reynolds JEI, Rommel SA (eds) Biology of marine mammals. Smithsonian Press, Washington, pp 117–175

    Google Scholar 

  • Wartzok D, McCormick MG (1978) Color discrimination by a bering sea spotted seal, Phoca largha. Vis Res 18:781–784

    Article  CAS  PubMed  Google Scholar 

  • Watanabe Y, Bornemann H, Liebsch N et al (2006) Seal-mounted cameras detect invertebrate fauna on the underside of an Antarctic ice shelf. Mar Ecol Prog Ser 309:297–300

    Article  Google Scholar 

  • Weiffen M, Möller B, Mauck B, Dehnhardt G (2006) Effect of water turbidity on the visual acuity of harbor seals (Phoca vitulina). Vis Res 46:1777–1783

    Article  PubMed  Google Scholar 

  • Welsch U, Ramdohr S, Riedelsheimer B et al (2001) Microscopic anatomy of the deep-diving Antarctic Weddell seal Leptonychotes weddelli. J Morphol 248:165–174

    Article  CAS  PubMed  Google Scholar 

  • Wilson G (1970a) Some comments on the optical system of Pinnipedia as a result of observations on the Weddell seal (Leptonychotes weddelli). Br Antarc Surv Bull 23:57–63

    Google Scholar 

  • Wilson G (1970b) Vision of the Weddell seal (Leptonychotes weddelli). In: Holgate MW (ed) Antarctic ecology. Academic Press, London

    Google Scholar 

  • Yarbus AL (1967) Eye movements and vision. Plenum Press, New York

    Google Scholar 

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Acknowledgments

The authors would like to thank the numerous collaborators that accompanied and influenced their own work on harbour seal vision with new ideas, helpful comments, and advice as well as never-ending support of all kind. The authors’ research has been supported by grants of the Studienstiftung des deutschen Volkes to FDH, the Deutsche Forschungsgemeinschaft to WH and CS, and by grants of the VolkswagenStiftung and the Deutsche Forschungsgemeinschaft (SFB 509) to GD.

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  1. General Zoology and Neurobiology, University of Bochum, ND 6/33, 44780, Bochum, Germany

    Frederike D. Hanke

  2. Institute for Biosciences, Sensory and Cognitive Ecology, University of Rostock, Albert-Einstein-Strasse 3, 18059, Rostock, Germany

    Wolf Hanke, Christine Scholtyssek & Guido Dehnhardt

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  1. Frederike D. Hanke
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  2. Wolf Hanke
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  4. Guido Dehnhardt
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Correspondence to Guido Dehnhardt.

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Hanke, F.D., Hanke, W., Scholtyssek, C. et al. Basic mechanisms in pinniped vision. Exp Brain Res 199, 299–311 (2009). https://doi.org/10.1007/s00221-009-1793-6

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