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Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors

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Abstract

Birds have four spectrally distinct types of single cones that they use for colour vision. It is often desirable to be able to model the spectral sensitivities of the different cone types, which vary considerably between species. However, although there are several mathematical models available for describing the spectral absorption of visual pigments, there is no model describing the spectral absorption of the coloured oil droplets found in three of the four single cone types. In this paper, we describe such a model and illustrate its use in estimating the spectral sensitivities of single cones. Furthermore, we show that the spectral locations of the wavelengths of maximum absorbance (λmax) of the short- (SWS), medium- (MWS) and long- (LWS) wavelength-sensitive visual pigments and the cut-off wavelengths (λcut) of their respective C-, Y- and R-type oil droplets can be predicted from the λmax of the ultraviolet- (UVS)/violet- (VS) sensitive visual pigment.

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Abbreviations

α:

Absorptivity (naperian)

B mid :

Gradient of line tangent to absorbance spectrum at λmid

B(λ):

Derivative of T(λ)

c :

Oil droplet carotenoid pigment concentration

D(λ):

Measured absorptance

D max :

Maximum measured absorptance

D min :

Minimum measured absorptance

D 0 :

Real absorptance

l :

Length of light path

LWS:

Long-wavelength-sensitive

MWS:

Medium-wavelength-sensitive

MSP:

Microspectrophotometer

SWS:

Short-wavelength-sensitive

T(λ):

Transmittance

UVS:

Ultraviolet-sensitive

VS:

Violet-sensitive

λ:

Wavelength

λ0:

Wavelength at which oil droplet transmittance is 1/e

λcut:

Cut-off wavelength (oil droplets)

λmax:

Wavelength at maximum absorbance (visual pigments)

λmid:

Wavelength at half-maximum absorptance (oil droplets)

λs:

A wavelength shorter than the wavelengths at which the absorptivity of the oil droplet can be described by an exponential function

λT0.5:

Wavelength at 0.5 transmittance (ocular media)

References

  • Barlow HB (1982) What causes trichromacy? A theoretical analysis using comb-filtered spectra. Vision Res 22:635–643

    Google Scholar 

  • Bennett ATD, Cuthill IC, Norris KJ (1994) Sexual selection and the mismeasure of color. Am Nat 144:848–860

    Article  Google Scholar 

  • Bowmaker JK (1977) The visual pigments, oil droplets and spectral sensitivity of the pigeon. Vision Res 17:1129–1138

    Google Scholar 

  • Bowmaker JK, Knowles A (1977) The visual pigments and oil droplets of the chicken retina. Vision Res 17:755–764

    Google Scholar 

  • Bowmaker JK, Martin GR (1978) Visual pigments and colour vision in a nocturnal bird, Strix aluco (tawny owl). Vision Res 18:1125–1130

    Google Scholar 

  • Bowmaker JK, Martin GR (1985) Visual pigments and oil droplets in the penguin, Spheniscus humboldti. J Comp Physiol A 156:71–77

    Google Scholar 

  • Bowmaker JK, Kovach JK, Whitmore AV, Loew ER (1993) Visual pigments and oil droplets in genetically manipulated and carotenoid deprived quail: a microspectrophotometric study. Vision Res 33:571–578

    Google Scholar 

  • Bowmaker JK, Heath LA, Wilkie SE, Hunt DM (1997) Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds. Vision Res 37:2183–2194

    Google Scholar 

  • Chiao C-C, Vorobyev M, Cronin TW, Osorio D (2000) Spectral tuning of dichromats to natural scenes. Vision Res 40:3257–3271

    Google Scholar 

  • Das D, Wilkie SE, Hunt DM, Bowmaker JK (1999) Visual pigments and oil droplets in the retina of a passerine bird, the canary Serinus canaria: microspectrophotometry and opsin sequences. Vision Res 39:2801–2815

    Google Scholar 

  • Davies BH (1979) Solved and unsolved problems of carotenoid formation. Pure Appl Chem 51:623–630

    Google Scholar 

  • Duke-Elder S (1958) System of ophthalmology. The eye in evolution, vol 1. CV Mosby, St Louis

  • Endler JA, Basolo AL (1998) Sensory ecology, receiver biases and sexual selection. Trends Ecol Evol 13:415–420

    Google Scholar 

  • Goldsmith TH, Butler BK (2003) The roles of receptor noise and cone oil droplets in the photopic spectral sensitivity of the budgerigar, Melopsittacus undulatus. J Comp Physiol A 189:135–142

    Google Scholar 

  • Goldsmith TH, Collins JS, Licht S (1984) The cone oil droplets of avian retinas. Vision Res 24:1661–1671

    Google Scholar 

  • Govardovskii VI (1983) On the role of oil drops in colour vision. Vision Res 23:1739–1740

    Google Scholar 

  • Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17:509–528

    Google Scholar 

  • Hart NS (2001a) The visual ecology of avian photoreceptors. Prog Retin Eye Res 20:675–703

    Google Scholar 

  • Hart NS (2001b) Variations in cone photoreceptor abundance and the visual ecology of birds. J Comp Physiol A 187:685–697

    Google Scholar 

  • Hart NS (2002) Vision in the peafowl (Aves: Pavo cristatus). J Exp Biol 205:3925–3935

    Google Scholar 

  • Hart NS (2004) Microspectrophotometry of visual pigments and oil droplets in a marine bird, the wedge-tailed shearwater Puffinus pacificus: topographic variations in photoreceptor spectral characteristics. J Exp Biol 207:1229–1240

    Google Scholar 

  • Hart NS, Partridge JC, Cuthill IC (1998) Visual pigments, oil droplets and cone photoreceptor distribution in the European starling (Sturnus vulgaris). J Exp Biol 201:1433–1446

    Google Scholar 

  • Hart NS, Partridge JC, Cuthill IC (1999) Visual pigments, cone oil droplets, ocular media and predicted spectral sensitivity in the domestic turkey (Meleagris gallopavo). Vision Res 39:3321–3328

    Google Scholar 

  • Hart NS, Partridge JC, Bennett ATD, Cuthill IC (2000a) Visual pigments, cone oil droplets and ocular media in four species of estrildid finch. J Comp Physiol A 186:681–694

    Google Scholar 

  • Hart NS, Partridge JC, Cuthill IC, Bennett AT (2000b) Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L) and the blackbird (Turdus merula L). J Comp Physiol A 186:375–387

    Google Scholar 

  • Jane SD, Bowmaker JK (1988) Tetrachromatic colour vision in the duck (Anas platyrhynchos L): microspectrophotometry of visual pigments and oil droplets. J Comp Physiol A 162:225–235

    Google Scholar 

  • Lamb TD (1995) Photoreceptor spectral sensitivities: common shape in the longwave region. Vision Res 35:3083–3091

    Google Scholar 

  • 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. Vision Res 24:597–604

    Google Scholar 

  • Lovy D (1996) WinDig 2.5. Department of Physical Chemistry, University of Geneva, Switzerland. Freeware available from the author at dominique.lovy@chiphy.unige.ch or by download from: http://www.unige.ch/sciences/chifi/cpb/windig.html (verified May 2004)

  • Maier EJ, Bowmaker JK (1993) Colour vision in the passeriform bird, Leothrix lutea: correlation of visual pigment absorbance and oil droplet transmission with spectral sensitivity. J Comp Physiol A 172:295–301

    Google Scholar 

  • Meyer DB, Stuckey SR, Hudson RA (1971) Oil droplet carotenoids of avian cones. I. Dietary exclusion: models for biochemical and physiological studies. Comp Biochem Physiol B 40:61–70

    Google Scholar 

  • Morris VB, Shorey CD (1967) An electron microscope study of types of receptor in the chick retina. J Comp Neurol 129:313–340

    Google Scholar 

  • Ödeen A, Håstad O (2003) Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Mol Biol Evol 20:855–861

    Google Scholar 

  • Osorio D, Vorobyev M, Jones CD (1999) Colour vision of domestic chicks. J Exp Biol 202:2951–2959

    Google Scholar 

  • Partridge JC (1986) Microspectrophotometry of vertebrate photoreceptors. PhD Thesis, University of Bristol, Bristol, UK

  • Partridge JC (1989) The visual ecology of avian cone oil droplets. J Comp Physiol A 165:415–426

    Google Scholar 

  • Partridge JC, DeGrip WJ (1991) A new template for rhodopsin (vitamin A1 based) visual pigments. Vision Res 31:619–630

    Google Scholar 

  • Polyak S (1957) The vertebrate visual system. University of Chicago Press, Chicago

    Google Scholar 

  • Pumphrey RJ (1948) The sense organs of birds. Ibis 90:171–199

    Google Scholar 

  • Rochon-Duvigneaud A (1943) Les yeux et la vision des vertébrés. Masson, Paris

    Google Scholar 

  • Rodieck RW (1973) The vertebrate retina. WH Freeman, San Francisco

    Google Scholar 

  • Siddiqi A, Cronin TW, Loew ER, Vorobyev M, Summers K (2004) Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. J Exp Biol 207:2471–2485

    Google Scholar 

  • Stavenga DG, Smits RP, Hoenders BJ (1993) Simple exponential functions describing the absorbance bands of visual pigment spectra. Vision Res 33:1011–1017

    Article  CAS  PubMed  Google Scholar 

  • Vorobyev M (1997) Costs and benefits of increasing the dimensionality of colour vision system. In: Taddei-Ferretti C (ed) Biophysics of photoreception: molecular and phototransductive events. World Scientific, Singapore, pp 280–289

    Google Scholar 

  • Vorobyev M (2003) Coloured oil droplets enhance colour discrimination. Proc R Soc Lond B 270:1255–1261

    Google Scholar 

  • Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B 265:351–358

    Article  CAS  PubMed  Google Scholar 

  • Vorobyev M, Osorio D, Bennett AT, Marshall NJ, Cuthill IC (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183:621–633

    Google Scholar 

  • Vorobyev M, Brandt R, Peitsch D, Laughlin SB, Menzel R (2001) Colour thresholds and receptor noise: behaviour and physiology compared. Vision Res 41:639–653

    Google Scholar 

  • Wald G, Zussman H (1937) Carotenoids of the chicken retina. Nature 140:197

    Google Scholar 

  • Wilkie SE, Vissers PM, Das D, DeGrip WJ, Bowmaker JK, Hunt DM (1998) The molecular basis for UV vision in birds: spectral characteristics, cDNA sequence and retinal localization of the UV-sensitive visual pigment of the budgerigar (Melopsittacus undulatus). Biochem J 330:541–547

    Google Scholar 

  • Wilkie SE, Robinson PR, Cronin TW, Poopalasundaram S, Bowmaker JK, Hunt DM (2000) Spectral tuning of avian violet- and ultraviolet-sensitive visual pigments. Biochemistry 39:7895–7901

    Google Scholar 

  • Wortel JF, Nuboer JFW (1986) The spectral sensitivity of blue-sensitive pigeon cones: evidence for complete screening of the visual pigment by the oil-droplets. Vision Res 26:885–886

    Google Scholar 

  • Wright MW, Bowmaker JK (2001) Retinal photoreceptors of paleognathous birds: the ostrich (Struthio camelus) and rhea (Rhea americana). Vision Res 41:1–12

    Google Scholar 

  • Yokoyama S (2000) Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res 19:385–419

    Google Scholar 

  • Yokoyama S, Radlwimmer FB, Kawamura S (1998) Regeneration of ultraviolet pigments of vertebrates. FEBS Lett 423:155–158

    Google Scholar 

  • Yokoyama S, Blow NS, Radlwimmer FB (2000a) Molecular evolution of color vision of zebra finch. Gene 259:17–24

    Google Scholar 

  • Yokoyama S, Radlwimmer FB, Blow NS (2000b) Ultraviolet pigments in birds evolved from violet pigments by a single amino acid change. Proc Natl Acad Sci USA 97:7366–7371

    Google Scholar 

Download references

Acknowledgements

N.S.H was funded primarily by a University of Queensland Postdoctoral Research Fellowship and partly by an NHMRC Project Grant awarded to David Vaney (UQ). M.V was also funded by the University of Queensland. The authors would like to thank the two anonymous referees for their helpful comments.

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Correspondence to Nathan S. Hart.

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Hart, N.S., Vorobyev, M. Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors. J Comp Physiol A 191, 381–392 (2005). https://doi.org/10.1007/s00359-004-0595-3

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