Advertisement

Journal of Comparative Physiology A

, Volume 191, Issue 10, pp 925–932 | Cite as

The cone photoreceptors and visual pigments of chameleons

  • James K. BowmakerEmail author
  • Ellis R. Loew
  • Matthias Ott
Original Paper
First Online:

Abstract

Visual pigments, oil droplets and photoreceptor types in the retinas of four species of true chameleons have been examined by microspectrophotometry. The species occupy different photic environments: two species of Chamaeleo are from Madagascar and two species of Furcifer are from Africa and the Arabian Peninsula. In addition to double cones, four spectrally distinct classes of single cone were identified. No rod photoreceptors were observed. The visual pigments appear to be mixtures of rhodopsins and porphyropsins. Double cones contained a pale oil droplet in the principle member and both outer segments contained a long-wave-sensitive visual pigment with a spectral maximum between about 555 nm and 610 nm, depending on the rhodopsin/porphyropsin mixture. Long-wave-sensitive single cones contained a visual pigment spectrally identical to the double cones, but combined with a yellow oil droplet. The other three classes of single cone contained visual pigments with maxima at about 480–505, 440–450 and 375–385 nm, combined with yellow, clear and transparent oil droplets respectively. The latter two classes were sparsely distributed. The transmission of the lens and cornea of C. dilepis was measured and found to be transparent throughout the visible and near ultraviolet, with a cut off at about 350 nm.

Keywords

Visual pigment Photoreceptor Oil droplet Chameleon Colour vision 

Abbreviations

MSP

Microspectrophotometry

λmax

Wavelength on maximum absorbance of visual pigment

λcut

Cut-off wavelength of oil droplet

LWS

Long-wave-sensitive

MWS

Middle-wave-sensitive

SWS

Short-wave-sensitive

UVS

Ultraviolet sensitive

This is a preview of subscription content, log in to check access.

References

  1. Armengol JA, Prada F, Ambrosiani J, Genis-Galvez JM (1988) The photoreceptors of the chameleon retina (Chamaleo chamaleo). A Golgi study. J Hirnforsch 29:403–409PubMedGoogle Scholar
  2. Bowmaker JK (1991) Visual pigments, oil droplets and photoreceptors. In: Gouras P (ed) The perception of colour. Macmillan, London, pp 108–127Google Scholar
  3. Bowmaker JK, Astell S, Hunt DM, Mollon JD (1991) Photosensitive and photostable pigments in the retinae of Old World monkeys. J Exp Biol 156:1–19PubMedGoogle Scholar
  4. Bowmaker JK, Kovach JK, Whitmore AV, Loew ER (1993) Visual pigments and oil droplets in genetically manipulated and carotenoid deprived quail: a microspectrophotometric study. Vis Res 33:571–578PubMedCrossRefGoogle Scholar
  5. Bowmaker JK, Heath LA, Wilkie SE, Hunt DM (1997) Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds. Vis Res 37:2183–2194PubMedCrossRefGoogle Scholar
  6. Carpenter CC, Ferguson GW (1977) Variation and evolution of stereotyped behavior in reptiles. In: Gans C, Tinkle DW (eds) Biology of the Reptilia. Academic, London, pp 335–554Google Scholar
  7. Douglas RH, McGuigan CM (1989) The spectral transmission of freshwater teleost ocular media—an interspecific comparison and a guide to potential ultraviolet sensitivity. Vis Res 29:871–879CrossRefPubMedGoogle Scholar
  8. Ellingson JM, Fleishman LJ, Loew ER (1995) Visual pigments and spectral sensitivity of the diurnal gecko Gonatodes albogularis. J Comp Physiol A 177:559–567CrossRefPubMedGoogle Scholar
  9. Fleishman LJ, Loew ER, Leal M (1993) Ultraviolet vision in lizards. Nature 365:397CrossRefGoogle Scholar
  10. Fleishman LJ, Bowman M, Saunders D, Miller WE, Rury MJ, Loew ER (1997) The visual ecology of Puerto Rican anoline lizards: habitat light and spectral sensitivity. J Comp Physiol A 181:446–460CrossRefGoogle Scholar
  11. Goldsmith TH, Collins JS, Licht S (1984) The cone oil droplets of avian retinas. Vis Res 24:1661–1671CrossRefPubMedGoogle Scholar
  12. Govardovskii VI (1983) On the role of oil drops in colour vision. Vis Res 23:1739–1740CrossRefPubMedGoogle Scholar
  13. Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17:509–528CrossRefPubMedGoogle Scholar
  14. Harkness L (1977) Chameleons use accommodation cues to judge distance. Nature 267:346–349CrossRefPubMedGoogle Scholar
  15. Hart NS (2001a) Variations in cone photoreceptor abundance and the visual ecology of birds. J Comp Physiol A 187:685–697CrossRefPubMedGoogle Scholar
  16. Hart NS (2001b) The visual ecology of avian photoreceptors. Prog Ret Eye Res 20:675–703CrossRefGoogle Scholar
  17. Kawamura S, Yokoyama S (1997) Expression of visual and nonvisual opsins in American chameleon. Vis Res 37:1867–1871PubMedCrossRefGoogle Scholar
  18. Kawamura S, Yokoyama S (1998) Functional characterization of visual and nonvisual pigments of American chameleon (Anolis carolinensis). Vis Res 38:37–44CrossRefPubMedGoogle Scholar
  19. LeBas NR, Marshall NJ (2000) The role of colour in signalling and male choice in the agamid lizard Ctenophorus ornatus. Proc R Soc Lond B 267:445–452CrossRefGoogle Scholar
  20. Liebman PA, Entine G (1964) Sensitive low-light-level microspectrophotometer: detection of photosensitive pigments of retinal cones. J Opt Soc Am A 54:1451–1459Google Scholar
  21. Liebman PA, Granda AM (1971) Microspectrophotometric measurements of visual pigments of two species of turtle, Pseudemys scripta and Chelonia mydas. Vis Res 11:105–114CrossRefPubMedGoogle Scholar
  22. Lipetz LE (1984) A new method for determining peak absorbance of dense pigment samples and its application to the cone oil droplets of Emydoidea blandingii. Vis Res 24:567–604PubMedGoogle Scholar
  23. Lipetz LE, Cronin TW (1988) Application of an invariant spectral form to the visual pigments of crustaceans: implications regarding the binding of the chromophore. Vis Res 28:1083–1093CrossRefPubMedGoogle Scholar
  24. Loew ER (1994) A third, ultraviolet-sensitive visual pigment in the tokay gecko (Gekko gekko). Vis Res 34:1427–1431CrossRefPubMedGoogle Scholar
  25. Loew ER, Fleishman LJ, Foster RG, Provencio I (2002) Visual pigments and oil droplets in diurnal lizards: a comparative study of Caribbean anoles. J Exp Biol 205:927–938PubMedGoogle Scholar
  26. Macedonia JM, Husak JF, Brandt YM, Lappin AK, Baird T (2004) Sexual dichromatism and color conspicuousness in three populations of collared lizards (Crotaphytus collaris) from Oklahoma. J Herpetol 38:340–354CrossRefGoogle Scholar
  27. Maier EJ, Bowmaker JK (1993) Colour vision in a passeriform bird, Leiothrix lutea: correlation of visual pigment absorbance and oil droplet transmission with spectral sensitivity. J Comp Physiol A 172:295–301CrossRefGoogle Scholar
  28. Mollon JD, Bowmaker JK, Jacobs GH (1984) Variations of colour vision in a New World primate can be explained by polymorphism of retinal photopigments. Proc R Soc Lond B 222:373–399PubMedCrossRefGoogle Scholar
  29. Osorio D, Vorobyev M, Jones CD (1999) Colour vision of domestic chicks. J Exp Biol 202:2951–2959PubMedGoogle Scholar
  30. Ott M, Schaeffel F (1995) A negatively powered lens in the chameleon. Nature 373:692–694CrossRefPubMedGoogle Scholar
  31. Ott M, Schaeffel F, Kirmse W (1998) Binocular vision and accommodation in prey-catching chameleons. J Comp Physiol A 182:319–330CrossRefGoogle Scholar
  32. Parry JWL, Bowmaker JK (2000) Visual pigment reconstitution in intact goldfish retina using synthetic retinaldehyde isomers. Vis Res 40:2241–2247CrossRefPubMedGoogle Scholar
  33. Persons MH, Fleishman LJ, Frye MA, Stimphil ME (1999) Sensory response patterns and the evolution of visual signal design in anoline lizards. J Comp Physiol A 184:585–607CrossRefGoogle Scholar
  34. Provencio I, Loew ER, Foster RG (1992) Vitamin A2-based visual pigments in fully terrestrial vertebrates. Vis Res 32:2201–2208CrossRefPubMedGoogle Scholar
  35. Raxworthy CJ, Forstner MRJ, Nussbaum RA (2002) Chameleon radiation by oceanic dispersal. Nature 415:784–787PubMedGoogle Scholar
  36. Röll B (2000) Carotenoid and retinoid—two pigments in a gecko eye lens. Comp Biochem Physiol A 125:105–112CrossRefGoogle Scholar
  37. Sándor PS, Frens MA, Henn V (2001) Chameleon eye position obeys Listing’s law. Vis Res 41:2245–2251CrossRefPubMedGoogle Scholar
  38. Schleich HH, Küstle W, Kabisch K (1996) Amphibians and Reptiles of North Africa. Koeltz Scientific Books, KoenigsteinGoogle Scholar
  39. Thorpe A, Douglas RH, Truscott RJW (1993) Spectral transmission and short-wave absorbing pigments in the fish lens—I. Phylogenetic distribution and identity. Vis Res 33:289–300CrossRefPubMedGoogle Scholar
  40. Vorobyev M (2003) Coloured oil droplets enhance colour discrimination. Proc R Soc Lond B 270:1255–1261CrossRefGoogle Scholar
  41. Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B 265:351–358CrossRefGoogle Scholar
  42. Vorobyev M, Osorio D, Bennett ATD, Marshall NJ, Cuthill IC (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183:621–633CrossRefPubMedGoogle Scholar
  43. Walls GL (1942) The vertebrate eye and its adaptive radiation. Cranbrook Institute of Science, MichiganGoogle Scholar
  44. Wright MW, Bowmaker JK (2001) Retinal photoreceptors of paleognathous birds: the ostrich (Struthio camelus) and rhea (Rhea americana). Vis Res 41:1–12CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • James K. Bowmaker
    • 1
    Email author
  • Ellis R. Loew
    • 2
  • Matthias Ott
    • 3
  1. 1.Division of Visual Science, Institute of OphthalmologyUniversity College LondonLondonUK
  2. 2.Department of Biomedical SciencesCornell UniversityIthacaUSA
  3. 3.Anatomisches InstitutUniversität TübingenTübingenGermany

Personalised recommendations

Cite article

Buy options