Abstract
Intraspecific variation in photoreceptor physiology is known in several vertebrate taxa, but is currently unknown in birds, despite many avian traits varying intraspecifically, and avian visual ecology encompassing a wide range of environments and visual stimuli, which might influence spectral sensitivity. Avian retinal photoreceptors contain light absorbing carotenoid-rich oil droplets that affect vision. Carotenoids are also important plumage components. However, our understanding of the regulation of carotenoids in oil droplets remains rudimentary. Among birds, Melopsittacus undulatus has probably the best-studied colour vision, shows profound intraspecific variation in plumage colour, and increased plasma carotenoids during moult. We used microspectrophotometry to determine whether a relationship exists between oil droplet carotenoid concentration and plumage pigmentation, and tested for sex and spatial variation in droplet absorbance across the retina. Absorbance of one variety of P-type droplets was higher in males. No relationship was found between droplet absorbance and plumage colour. We found a spatial pattern of droplets absorbance across the retina that matched a pattern found in another parrot, and other avian species. Our work provides insights into the development and maintenance of retinal oil droplets and suggests a common mechanism and function for carotenoid deposition in the retina across bird species.
Similar content being viewed by others
Abbreviations
- AIC:
-
Akaike’s information criterion
- λcut :
-
Cut-off wavelength
- ICC:
-
Intraclass coefficient
- LWS:
-
Longwave sensitive
- MWS:
-
Mediumwave sensitive
- MSP:
-
Microspectrophotometry
- SWS:
-
Shortwave sensitive
- UVS:
-
Ultraviolet sensitive
- VS:
-
Violet sensitive
- λmax :
-
Wavelength of maximum sensitivity
References
Arnold KE, Owens IPF, Marshall NJ (2002) Fluorescent signaling in parrots. Science 295(5552):92
Bennett ATD, Cuthill IC, Norris KJ (1994) Sexual selection and the mismeasure of color. Am Nat 144(5):848–860
Bennett ATD, Cuthill IC, Partridge JC, Maier EJ (1996) Ultraviolet vision and mate choice in zebra finches. Nature 380(6573):433–435
Bennett ATD, Thery M (2007) Avian color vision and coloration: multidisciplinary evolutionary biology. Am Nat 169(1):S1–S6
Berg ML, Bennett ATD (2010) The evolution of plumage colouration in parrots: a review. Emu 110(1):10–20. doi:10.1071/mu09076
Blas J, Perez-Rodriguez L, Bortolotti GR, Vinuela J, Marchant TA (2006) Testosterone increases bioavailability of carotenoids: insights into the honesty of sexual signaling. Proc Natl Acad Sci USA 103(49):18633–18637
Boughman JW (2002) How sensory drive can promote speciation. Trends Ecol Evol 17(12):571–577
Bowmaker JK (1977) Visual pigments, oil droplets and spectral sensitivity of pigeon. Vision Res 17(10):1129–1138
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(16):2183–2194
Campenhausen MV, Kirschfeld K (1998) Spectral sensitivity of the accessory optic system of the pigeon. J Comp Physiol A 183(1):1–6
Carvalho LS, Knott B, Berg ML, Bennett ATD, Hunt DM (2011) Ultraviolet-sensitive vision in long-lived birds. Proc R Soc B 278(1702):107–114. doi:10.1098/rspb.2010.1100
Cassey P, Honza M, Grim T, Hauber ME (2008) The modelling of avian visual perception predicts behavioural rejection responses to foreign egg colours. Biol Lett 4(5):515–517. doi:10.1098/rsbl.2008.0279
Chen DM, Goldsmith TH (1986) Four spectral classes of cone in the retinas of birds. J Comp Physiol A 159(4):473–479
Cherry MI, Bennett ATD, Moskat C (2007) Host intra-clutch variation, cuckoo egg matching and egg rejection by great reed warblers. Naturwissenschaften 94(6):441–447
Church SC, Bennett ATD, Cuthill IC, Partridge JC (1998) Ultraviolet cues affect the foraging behaviour of blue tits. Proc R Soc B 265(1405):1509–1514
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(17):2801–2815
Endler JA (1992) Signals, signal conditions, and the direction of evolution. Am Nat 139:S125–S153
Endler JA (1993) The color of light in forests and its implications. Ecol Monogr 63(1):1–27
Fuller RC, Carleton KL, Fadool JM, Spady TC, Travis J (2004) Population variation in opsin expression in the bluefin killifish, lucania goodei: a real-time pcr study. J Comp Physiol A 190(2):147–154
Goldsmith TH (1990) Optimization, constraint, and history in the evolution of eyes. Q Rev Biol 65(3):281–322
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(2):135–142
Goldsmith TH, Butler BK (2005) Color vision of the budgerigar (Melopsittacus undulatus): hue matches, tetrachromacy, and intensity discrimination. J Comp Physiol A 191(10):933–951
Goldsmith TH, Collins JS, Licht S (1984) The cone oil droplets of avian retinas. Vision Res 24(11):1661–1671
Hart NS (2001) The visual ecology of avian photoreceptors. Prog Retin Eye Res 20(5):675–703
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(7):1229–1240
Hart NS, Hunt DM (2007) Avian visual pigments: characteristics, spectral tuning, and evolution. Am Nat 169(1):S7–S26
Hart NS, Lisney TJ, Collin SP (2006) Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity. J Exp Biol 209(23):4776–4787
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(7–8):681–694
Hart NS, Partridge JC, Cuthill IC, Bennett ATD (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(4):375–387
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(9):1433–1446
Heath LA, Wilkie SE, Bowmaker JK, Hunt DM (1997) The rod and green cone opsins of two avian species, the budgerigar, Melopsittacus undulatus, and the mallard duck, Anas platyrhynchus. Gene 204(1–2):121–126
Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350(6316):337–339
Hill GE, Montgomerie R, Inouye CY, Dale J (1994) Influence of dietary carotenoids on plasma and plumage color in the house finch—intrasexual and intersexual variation. Funct Ecol 8(3):343–350
Jacobs GH (1977) Visual sensitivity—significant within-species variations in a nonhuman primate. Science 197(4302):499–500
Jacobs GH, Neitz M, Deegan JF, Neitz J (1996) Trichromatic colour vision in new world monkeys. Nature 382(6587):156–158
Joseph L, Dolman G, Donnellan S, Saint KM, Berg ML, Bennett ATD (2008) Where and when does a ring start and end? Testing the ring-species hypothesis in a species complex of australian parrots. Proc R Soc B 275(1650):2431–2440
Knott B, Berg ML, Morgan ER, Buchanan KL, Bowmaker JK, Bennett ATD (2010) Avian retinal oil droplets: dietary manipulation of avian colour vision? Proc R Soc B 277:953–962. doi:10.1098/rspb.2009.1805
Liebman PA, Granda AM (1975) Super dense carotenoid spectra resolved in single cone oil droplets. Nature 253(5490):370–372
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(6):597–604
Maier EJ, Bowmaker JK (1993) Color-vision in the passeriform bird, leiothrix-lutea—correlation of visual pigment absorbency and oil droplet transmission with spectral sensitivity. J Comp Physiol A 172(3):295–301
Martin GR, Muntz WRA (1978) Spectral sensitivity of red and yellow oil droplet fields of pigeon (Columba livia). Nature 274(5671):620–621
McGraw KJ, Adkins-Regan E, Parker RS (2002a) Anhydrolutein in the zebra finch: a new, metabolically-derived carotenoid in birds. Comp Biochem Physiol B 132(4):811–818
McGraw KJ, Hill GE, Stradi R, Parker RS (2002b) The effect of dietary carotenoid access on sexual dichromatism and plumage pigment composition in the American goldfinch. Comp Biochem Physiol B 131(2):261–269
McGraw KJ, Gregory AJ, Parker RS, Adkins-Regan E (2003) Diet, plasma carotenoids, and sexual coloration in the zebra finch (Taeniopygia guttata). Auk 120(2):400–410
McGraw KJ, Nogare MC (2004) Carotenoid pigments and the selectivity of psittacofulvin-based coloration systems in parrots. Comp Biochem Physiol B 138(3):229–233
McGraw KJ, Nogare MC (2005) Distribution of unique red feather pigments in parrots. Biol Lett 1(1):38–43
Mollon JD, Bowmaker JK, Jacobs GH (1984) Variations of color-vision in a new world primate can be explained by polymorphism of retinal photopigments. Proc R Soc B 222(1228):373–399
Muntz WRA (1972) Inert absorbing and reflecting pigments. In: Dartnall HJA (ed) Handbook of sensory physiology, vol 7. Springer, Berlin, pp 529–565
Osorio D, Vorobyev M, Jones CD (1999) Colour vision of domestic chicks. J Exp Biol 202(21):2951–2959
Parry JWL, Carleton KL, Spady T, Carboo A, Hunt DM, Bowmaker JK (2005) Mix and match color vision: tuning spectral sensitivity by differential opsin gene expression in lake malawi cichlids. Curr Biol 15(19):1734–1739
Partridge JC (1989) The visual ecology of avian cone oil droplets. J Comp Physiol A 165(3):415–426
Pearn SM, Bennett ATD, Cuthill IC (2001) Ultraviolet vision, fluorescence and mate choice in a parrot, the budgerigar Melopsittacus undulatus. Proc R Soc B 268(1482):2273–2279
Pearn SM, Bennett ATD, Cuthill IC (2003a) The role of ultraviolet-a reflectance and ultraviolet-a-induced fluorescence in budgerigar mate choice. Ethology 109(12):961–970
Pearn SM, Bennett ATD, Cuthill IC (2003b) The role of ultraviolet-a reflectance and ultraviolet-a induced fluorescence in the appearance of budgerigar plumage: Insights from spectrofluorometry and reflectance spectrophotometry. Proc R Soc B 270(1517):859–865
Pryke SR (2007) Fiery red heads: female dominance among head color morphs in the gouldian finch. Behav Ecol 18(3):621–627
Pryke SR, Andersson S, Lawes MJ, Piper SE (2002) Carotenoid status signaling in captive and wild red-collared widowbirds: independent effects of badge size and color. Behav Ecol 13(5):622–631
Ribot RFH, Berg ML, Buchanan KL, Komduer J, Joseph L, Bennett ATD (2009) Does the ring species concept predict vocal variation in the crimson rosella, Platycercus elegans, complex? Anim Behav 77(3):581–593
Schaefer HM, Levey DJ, Schaefer V, Avery ML (2006) The role of chromatic and achromatic signals for fruit detection by birds. Behav Ecol 17(5):784–789
Schiedt K, Bischof S, Glinz E (1991) Recent progress on carotenoid metabolism in animals. Pure Appl Chem 63(1):89–100
Slifka KA, Bowen PE, Stacewicz-Sapuntzakis M, Crissey SD (1999) A survey of serum and dietary carotenoids in captive wild animals. J Nutr 129(2):380–390
Stradi R, Pini E, Celentano G (2001) The chemical structure of the pigments in Ara macao plumage. Comp Biochem Physiol B 130(1):57–63
Tabachnick BG, Fidell LS (2007) Using multivariate statistics, 5th edn. Pearson, Boston
Taylor T, Warner C (1986) Genetics for budgerigar breeders, 2nd edn. The Budgerigar Society, UK
Toomey MB, McGraw KJ (2009) Seasonal, sexual, and quality related variation in retinal carotenoid accumulation in the house finch (Carpodacus mexicanus). Funct Ecol 23(2):321–329
Völker O (1937) Ueber fluoreszierende, gelbe federpigmente bei papageien, eine neue klasse von federfarbstoffen. J Ornithol 85(1):136–146
Vorobyev M (2003) Coloured oil droplets enhance colour discrimination. Proc R Soc B 270(1521):1255–1261
Vorobyev M, Osorio D, Bennett ATD, Marshall NJ, Cuthill IC (1998) Tetrachromacy, oil droplets and bird plumage colours. J Comp Physiol A 183(5):621–633
Wilkie SE, Vissers P, Das D, de Grip WJ, Bowmaker JK, Hunt DM (1997) Short-wave sensitive visual pigments from birds: The ultraviolet-sensitive opsin from budgerigar (Melopsittacus undulatus). Invest Ophthalmol Vis Sci 38(4):1046
Acknowledgments
B. Knott was funded by a Biotechnology and Biological Sciences Research Council (BBSRC) strategic studentship no. BBS/S/H/2005/11891. A. T. D. Bennett was funded by BBSRC grant B01568, and by a Leverhulme Trust Fellowship, Bristol University and Deakin University. The authors declare that all experiments comply with the laws of the United Kingdom. All animal procedures were approved by the University of Bristol ethical review group (UIN:UB/06/002).
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Knott, B., Bowmaker, J.K., Berg, M.L. et al. Absorbance of retinal oil droplets of the budgerigar: sex, spatial and plumage morph-related variation. J Comp Physiol A 198, 43–51 (2012). https://doi.org/10.1007/s00359-011-0684-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00359-011-0684-z