Experimental Brain Research

, 199:299 | Cite as

Basic mechanisms in pinniped vision

  • Frederike D. Hanke
  • Wolf Hanke
  • Christine Scholtyssek
  • Guido Dehnhardt


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.


Pinnipeds Visual system Amphibious vision Resolution Sensitivity 



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.


  1. Bernholz CD, Matthews ML (1975) Critical flicker frequency in a harp seal: evidence for duplex retinal organization. Vis Res 15:733–736CrossRefPubMedGoogle Scholar
  2. Bisti S, Maffei L (1974) Behavioural contrast sensitivity of the cat in various visual meridians. J Physiol 241:201–210PubMedGoogle Scholar
  3. Bowmaker JK (1995) The visual pigments of fish. Prog Retin Eye Res 15:1–31CrossRefGoogle Scholar
  4. Busch H, Dücker G (1987) Das visuelle Leistungsvermögen der Seebären (Arctocephalus pusillus und Arctocephalus australis). Zool Anz 219(3/4):197–224Google Scholar
  5. Campbell FW, Maffei L, Piccolino M (1973) The contrast sensitivity of the cat. J Physiol 229:719–731PubMedGoogle Scholar
  6. Carpenter RHS (1988) Movements of the eyes. Pion Limited, LondonGoogle Scholar
  7. Cornsweet TN, Pinsker HM (1965) Luminance discrimination of brief flashes under various conditions of adaptation. J Physiol 176:294–310PubMedGoogle Scholar
  8. Crescitelli F (1958) Natural history of visual pigments. Ann N Y Acad Sci 74:230–255CrossRefGoogle Scholar
  9. 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 76:2114–2118CrossRefGoogle Scholar
  10. Dawson WW, Schroeder JP, Sharpe SN (1987) Corneal surface properties of two marine mammal species. Mar Mamm Sci 3(2):186–197CrossRefGoogle Scholar
  11. Dehnhardt G (2002) Sensory systems. In: Hoelzel R (ed) Marine mammal biology—an evolutionary approach. Blackwell, Oxford, pp 116–141Google Scholar
  12. Fasick JI, Robinson PR (1998) Mechanisms of spectral tuning in the dolphin visual pigments. Biochemistry 37:433–438CrossRefPubMedGoogle Scholar
  13. Fasick JI, Robinson PR (2000) Spectral-tuning mechanisms of marine mammal rhodpsins and correlations with foraging depth. Vis Neurosci 17:781–788CrossRefPubMedGoogle Scholar
  14. Fasick JI, Cronin TW, Hunt DM, Robinson PR (1998) The visual pigments of the bottlenose dolphin (Tursiops truncatus). Vis Neurosci 15:1–9CrossRefGoogle Scholar
  15. Geisbauer G, Griebel U, Schmid A, Timney B (2004) Brightness discrimination and neutral point testing in the horse. Can J Zool 82:660–670CrossRefGoogle Scholar
  16. Grasse KL, Cynader MS (1988) The effect of visual cortex lesions on vertical optokinetic nystagmus in the cat. Brain Res 455:385–389CrossRefPubMedGoogle Scholar
  17. Griebel U, Peichl L (2003) Color vision in aquatic mammals—facts and open questions. Aquat Mamm 29(1):18–30CrossRefGoogle Scholar
  18. Griebel U, Schmid A (1992) Color vision in the California sea lion (Zalophus californianus). Vis Res 32(1):477–482CrossRefPubMedGoogle Scholar
  19. Griebel U, Schmid A (1997) Brightness discrimination ability in the West Indian manatee (Trichechus manatus). J Exp Biol 200:1587–1592PubMedGoogle Scholar
  20. 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
  21. Hanke FD, Dehnhardt G, Schaeffel F, Hanke W (2006) Corneal topography, refractive state, and accommodation in harbor seals (Phoca vitulina). Vis Res 46:837–847CrossRefPubMedGoogle Scholar
  22. Hanke W, Römer R, Dehnhardt G (2006) Visual fields and eye movements in a harbor seal (Phoca vitulina). Vis Res 46:2804–2814CrossRefPubMedGoogle Scholar
  23. Hanke FD, Hanke W, Hoffmann K-P, Dehnhardt G (2008a) Optokinetic nystagmus in harbor seals (Phoca vitulina). Vis Res 48(2):304–315CrossRefPubMedGoogle Scholar
  24. Hanke FD, Kröger RHH, Siebert U, Dehnhardt G (2008b) Multifocal lenses in a monochromat, the harbour seal. J Exp Biol 211:3315–3322CrossRefPubMedGoogle Scholar
  25. Hobson ES (1966) Visual orientation and feeding in seals and sea lions. Nature 210:326–327CrossRefGoogle Scholar
  26. Hughes A (1975) A quantitative analysis of the cat retinal ganglion cell topography. J Comp Neurol 163:107–128CrossRefPubMedGoogle Scholar
  27. Hughes A (1976) A supplement to the cat schematic eye. Vis Res 16(2):149–154CrossRefPubMedGoogle Scholar
  28. Hughes A (1977) Topography of vision in mammals. In: Crescitelli F (ed) Handbook of sensory physiology. Springer, BerlinGoogle Scholar
  29. Jacobs GH, Degan JFII, Neitz J, Crognale MA, Neitz M (1993) Photopigments and color vision in the nocturnal monkey Aotus. Vis Res 33:1773–1783CrossRefPubMedGoogle Scholar
  30. Jamieson GS (1970) The eye of the harbour seal, Phoca vitulina. PhD thesis, The University of British Columbia, VancouverGoogle Scholar
  31. Jamieson GS (1971) The functional significance of corneal distortion in marine mammals. Can J Zool 49:421–423CrossRefPubMedGoogle Scholar
  32. Jamieson GS, Fisher HD (1970) Visual discrimination in the harbour seal Phoca vitulina, above and below water. Vis Res 10:1175–1180CrossRefPubMedGoogle Scholar
  33. Jamieson GS, Fisher HD (1971) The retina of the harbour seal, Phoca vitulina. Can J Zool 49:19–23CrossRefGoogle Scholar
  34. Jamieson GS, Fisher HD (1972) The pinniped eye: a review. In: Harrison RJ (ed) Functional anatomy of marine mammals. Academic Press, London, pp 245–261Google Scholar
  35. Johnson GL (1893) Observations on the refraction and vision of the seal’s eye. Proc Zool Soc Lond 719–723Google Scholar
  36. Johnson GL (1901) Contributions to the comparative anatomy of the mammalian eye, chiefly based on ophthalmoscopic examination. Philos Trans R Soc Biol Charact 194:1–82CrossRefGoogle Scholar
  37. 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 113–119Google Scholar
  38. 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 121–147Google Scholar
  39. Kröger RHH, Campbell MCW, Fernald RD, Wagner H-J (1999) Multifocal lenses compensate for chromatic defocus in vertebrate eyes. J Comp Physiol A 184:361–369CrossRefPubMedGoogle Scholar
  40. Land MF, Nilsson D-E (2002) Animal eyes. Oxford University Press, OxfordGoogle Scholar
  41. Landau D, Dawson WW (1970) The histology of retinas from the pinnipedia. Vis Res 10:691–702CrossRefPubMedGoogle Scholar
  42. Lavigne DM, Ronald K (1975a) Evidence of duplicity in the retina of the California sea lion (Zalophus californianus). Comp Biochem Physiol 50:65–70CrossRefGoogle Scholar
  43. Lavigne DM, Ronald K (1975b) Pinniped visual pigments. Comp Biochem Physiol 52(B):325–329Google Scholar
  44. Lavigne DM, Ronald K (1977) Functional aspects of pinniped vision. In: Harrison RJ (ed) Functional anatomy of marine mammals. Academic Press, London, pp 135–173Google Scholar
  45. Levenson DH, Schusterman RJ (1997) Pupillometry in seals and sea lions: ecological implications. Can J Zool 75:2050–2057CrossRefGoogle Scholar
  46. Levenson DH, Schusterman RJ (1999) Dark adaptation and visual sensitivity in shallow and deep-diving pinnipeds. Mar Mamm Sci 15(4):1303–1313CrossRefGoogle Scholar
  47. 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):833–843CrossRefGoogle Scholar
  48. Lythgoe JP (1975) Problems of seeing colors underwater. In: Ali MA (ed) Vision in fishes: new approaches in research. Plenum Press, New York, pp 619–634Google Scholar
  49. Lythgoe JN, Dartnall HJA (1970) A ‘deep sea rhodopsin’ in a marine mammal. Nature 227:995–996CrossRefGoogle Scholar
  50. 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 39:69–76CrossRefPubMedGoogle Scholar
  51. Mass AM, Supin AY (2003) Retinal topography of the harp seal Pagophilus groenlandicus. Brain Behav Evol 62:212–222CrossRefPubMedGoogle Scholar
  52. Mass AM, Supin AY (2005) Ganglion cell topography and retinal resolution of the Steller sea lion (Eumetobias jubatus). Aquat Mamm 31(4):393–402CrossRefGoogle Scholar
  53. Mauck B, Dehnhardt G (1997) Mental rotation in a California sea lion (Zalophus californianus). J Exp Biol 200:1309–1316PubMedGoogle Scholar
  54. McFarland WN (1971) Cetacean visual pigments. Vis Res 11:1065–1076CrossRefPubMedGoogle Scholar
  55. 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):23–32CrossRefPubMedGoogle Scholar
  56. Nagy AR, Ronald K (1970) The harp seal, Pagophilus groenlandicus (Erxleben 1777). VI. Structure of the retina. Can J Zool 48:367–370CrossRefPubMedGoogle Scholar
  57. Newman LA, Robinson PR (2005) Cone visual pigments of aquatic mammals. Vis Neurosci 22:873–879CrossRefPubMedGoogle Scholar
  58. Peichl L (1992) Topography of ganglion cells in the dog and wolf retina. J Comp Neurol 324:603–620CrossRefPubMedGoogle Scholar
  59. 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 10:2586–2594CrossRefPubMedGoogle Scholar
  60. 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 13:1520–1528CrossRefPubMedGoogle Scholar
  61. Piggins DJ (1970) Refraction of the harp seal, Pagophilus groenlandicus (Erxleben 1777). Nature 227:78–79CrossRefPubMedGoogle Scholar
  62. Pütter A (1903) Die Augen der Wassersäugetiere. Zool Jahrb Anat Ontogenie 17:99–402Google Scholar
  63. Rahmann H (1967) Die Sehschärfe bei Wirbeltieren. Nat Rundsch 1:10–14Google Scholar
  64. Reitner A, Sharpe LT, Zrenner E (1991) Is colour vision possible with only rods and blue-sensitive cones? Nature 352:798–800CrossRefPubMedGoogle Scholar
  65. Renouf D (1991) Sensory reception and processing in Phocidae and Otariidae. In: Renouf D (ed) Behaviour in pinnipeds. University Press, CambridgeGoogle Scholar
  66. 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 149–172Google Scholar
  67. Schaeffel F, Farkas L, Howland HC (1987) Infrared photoretinoscope. Appl Opt 26(8):1505–1508CrossRefGoogle Scholar
  68. 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 251–306Google Scholar
  69. Scholtyssek C, Kelber A, Dehnhardt G (2008) Brightness discrimination in the harbor seal (Phoca vitulina). Vis Res 48:96–103CrossRefPubMedGoogle Scholar
  70. 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 301–320Google Scholar
  71. Schusterman RJ, Balliet RF (1970) Visual acuity of the harbour seal and the Steller sea lion under water. Nature 226:563–564CrossRefPubMedGoogle Scholar
  72. 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 188:37–46CrossRefPubMedGoogle Scholar
  73. Sivak JG (1980) Accommodation in vertebrates: a contemporary survey. Curr Top Eye Res 3:281–330PubMedGoogle Scholar
  74. 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 165:771–777CrossRefPubMedGoogle Scholar
  75. Southall KD, Oliver GW, Lewis JW et al (2002) Visual pigment sensitivity in three deep diving marine mammals. Mar Mamm Sci 18:275–281CrossRefGoogle Scholar
  76. Stich KP, Dehnhardt G, Mauck B (2003) Mental rotation of perspective stimuli in a California sea lion (Zalophus californianus). Brain Behav Evol 61:102–112CrossRefPubMedGoogle Scholar
  77. Supin AY, Popov VV, Mass AM (2001) The sensory physiology of aquatic mammals. Kluwer, BostonGoogle Scholar
  78. Walls GL (1942) The vertebrate eye and its adaptive radiation. Hafner Press, New YorkGoogle Scholar
  79. Walls GL (1962) The evolutionary history of eye movements. Vis Res 2:69–80CrossRefGoogle Scholar
  80. Warrant E, Locket NA (2004) Vision in the deep sea. Biol Rev 79:671–712CrossRefPubMedGoogle Scholar
  81. Wartzok D (1979) Phocid spectral sensitivity curves. In: Third biennial conference on the biology of marine mammals, Seattle. Society for Marine Mammals, Lawrence, p 62Google Scholar
  82. Wartzok D, Ketten DR (1999) Marine mammal sensory systems. In: Reynolds JEI, Rommel SA (eds) Biology of marine mammals. Smithsonian Press, Washington, pp 117–175Google Scholar
  83. Wartzok D, McCormick MG (1978) Color discrimination by a bering sea spotted seal, Phoca largha. Vis Res 18:781–784CrossRefPubMedGoogle Scholar
  84. 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 309:297–300CrossRefGoogle Scholar
  85. Weiffen M, Möller B, Mauck B, Dehnhardt G (2006) Effect of water turbidity on the visual acuity of harbor seals (Phoca vitulina). Vis Res 46:1777–1783CrossRefPubMedGoogle Scholar
  86. Welsch U, Ramdohr S, Riedelsheimer B et al (2001) Microscopic anatomy of the deep-diving Antarctic Weddell seal Leptonychotes weddelli. J Morphol 248:165–174CrossRefPubMedGoogle Scholar
  87. 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 23:57–63Google Scholar
  88. Wilson G (1970b) Vision of the Weddell seal (Leptonychotes weddelli). In: Holgate MW (ed) Antarctic ecology. Academic Press, LondonGoogle Scholar
  89. Yarbus AL (1967) Eye movements and vision. Plenum Press, New YorkGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Frederike D. Hanke
    • 1
  • Wolf Hanke
    • 2
  • Christine Scholtyssek
    • 2
  • Guido Dehnhardt
    • 2
  1. 1.General Zoology and NeurobiologyUniversity of BochumBochumGermany
  2. 2.Institute for Biosciences, Sensory and Cognitive EcologyUniversity of RostockRostockGermany

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