Journal of Comparative Physiology A

, Volume 196, Issue 2, pp 91–96 | Cite as

Pollinating birds differ in spectral sensitivity

  • Anders Ödeen
  • Olle HåstadEmail author
Original Paper


Pollinating animals and their angiosperm hosts often show strong co-adaptation in traits that increase the likelihood of a successful transfer of pollen and nutrient rewards. One such adaptation is the reported colour difference caused by unequal distribution of anthocyanidin pigments amongst plant species visited by hummingbirds and passerines. This phenomenon has been suggested to reflect possible differences in the colour vision of these pollinating birds. The presence of any such difference in colour vision would arguably affect the ecological and evolutionary interactions between flowers and their visitors, accentuating differences in floral displays and attractiveness of plants to the favoured avian pollinators. We have tested for differences in colour vision, as indicated by the amino acid present at certain key positions in the short-wavelength-sensitive type 1 (SWS1) visual pigment opsin, between the major groups of pollinating birds: the non-passerine Trochilidae (hummingbirds), the passerine Meliphagidae (honeyeaters) and Nectariniidae (sunbirds) plus five other Passerida passerine families. The results reveal gross spectral sensitivity differences between hummingbirds and honeyeaters, on the one hand, and the Passerida species, on the other.


Colour vision Pollination SWS1 pigment opsin UV sensitivity Ornithophily 

List of abbreviations


Base pair


Wavelength of maximum absorbance




Polymerase chain reaction


Short-wavelength-sensitive type one


Ultraviolet sensitive


Violet sensitive



Australian Museum, Sydney, Burke Museum, University of Washington, Seattle, the Field Museum, Chicago and the Swedish Museum of Natural History, Stockholm, kindly provided the tissue samples. We would like to thank Julian Partridge, Jon Ågren and the two anonymous reviewers for constructive comments on earlier versions of the manuscript. This study was financially supported by the Swedish Research Council FORMAS to AÖ, the Swedish Research Council (VR) to OH, and by Stiftelsen för Zoologisk Forskning and the Royal Swedish Academy of Sciences (sequencing). It complies with the “Principles of animal care”, publication No. 86-23, revised 1985, of the National Institute of Health, and also with current Swedish laws.


  1. Barker FK, Cibois A, Schikler P, Feinstein J, Cracraft J (2004) Phylogeny and diversification of the largest avian radiation. Proc Natl Acad Sci USA 101:11040–11045CrossRefPubMedGoogle Scholar
  2. Beason RC, Loew ER (2008) Visual pigment and oil droplet characteristics of the bobolink (Dolichonyx oryzivorus), a new world migratory bird. Vision Res 48:1–8CrossRefPubMedGoogle Scholar
  3. 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 37:2183–2194CrossRefPubMedGoogle Scholar
  4. Carvalho LS, Cowing JA, Wilkie SE, Bowmaker JK, Hunt DM (2007) The molecular evolution of avian ultraviolet- and violet-sensitive visual pigments. Mol Biol Evol 24:1843–1852CrossRefPubMedGoogle Scholar
  5. Chittka L (1996) Does bee color vision predate the evolution of flower color? Naturwissenschaften 83:136–138CrossRefGoogle Scholar
  6. Chittka L, Menzel R (1992) The evolutionary adaptation of flower colors and the insect pollinators color vision. J Comp Physiol A 170:533–543Google Scholar
  7. Cronk Q, Ojeda I (2008) Bird-pollinated flowers in an evolutionary and molecular context. J Exp Bot 59:715–727CrossRefPubMedGoogle Scholar
  8. Cuthill IC, Partridge JC, Bennett ATD, Church SC, Hart NS, Hunt S (2000) Ultraviolet vision in birds. Adv Study Behav 29:159–214CrossRefGoogle Scholar
  9. 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 39:2801–2815CrossRefPubMedGoogle Scholar
  10. Ericson PGP, Christidis L, Cooper L, Irestedt M, Jackson J, Johansson US, Norman JA (2002) A Gondwanan origin of passerine birds supported by DNA sequences of the endemic New Zealand wrens. Proc R Soc Lond B 269:235–241CrossRefGoogle Scholar
  11. Ericson PGP, Anderson CL, Britton T, Elzanowski A, Johansson US, Källersjö M, Ohlson JI, Parsons TJ, Zuccon D, Mayr D (2006) Diversification of Neoaves: integration of molecular sequence data and fossils. Biol Lett 2:543–547CrossRefPubMedGoogle Scholar
  12. Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun E, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harschman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Stedman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1767CrossRefPubMedGoogle Scholar
  13. Hart N (2001) The visual ecology of avian photoreceptors. Prog Retin Eye Res 20:675–703CrossRefPubMedGoogle Scholar
  14. Hart N (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 207:1229–1240CrossRefPubMedGoogle Scholar
  15. Hart NS, Hunt DM (2007) Avian visual pigments: characteristics, spectral tuning and evolution. Am Nat 169(Suppl):S7–S26CrossRefPubMedGoogle Scholar
  16. Hart N, Vorobyev M (2005) Modeling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors. J Comp Physiol A 191:381–392CrossRefGoogle Scholar
  17. Hart NS, Partridge JC, Cuthill IC (1998) Visual pigments, oil droplets and cone photoreceptor distribution in the European starling (Sturnus vulgaris). J Exp Biol 201:1433–1446PubMedGoogle Scholar
  18. 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 39:3321–3328CrossRefPubMedGoogle Scholar
  19. 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 186:681–694CrossRefPubMedGoogle Scholar
  20. 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 186:375–387CrossRefPubMedGoogle Scholar
  21. Håstad O, Ernstdotter E, Ödeen A (2005a) Ultraviolet vision and foraging in dip and plunge diving birds. Biol Lett 1:306–309CrossRefPubMedGoogle Scholar
  22. Håstad O, Victorsson J, Ödeen A (2005b) Differences in color vision make passerines less conspicuous in the eyes of their predators. Proc Natl Acad Sci USA 102:6391–6394CrossRefPubMedGoogle Scholar
  23. Herrera G, Zagal JC, Diaz M, Fernandez MJ, Vielma A, Cure M, Martinez J, Bozinovic F, Palacios AG (2008) Spectral sensitivities of photoreceptors and their role in colour discrimination in the green-backed firecrown hummingbird (Sephanoides sephaniodes). J Comp Physiol A 194:785–794CrossRefGoogle Scholar
  24. Lythgoe JN (1979) The ecology of vision. Oxford University Press, OxfordGoogle Scholar
  25. Maier EJ, Bowmaker JK (1993) Colour vision in the passeriform bird, Leiothrix lutea: correlation of visual pigment absorbance and oil droplet transmission with spectral sensitivity. J Comp Physiol A 172:295–301CrossRefGoogle Scholar
  26. McGuire JA, Witt CC, Altshuler DL, Remsen JV Jr (2007) Phylogenetic systematics and biogeography of hummingbirds: Bayesian and maximum likelihood analyses of partitioned data and selection of an appropriate partitioning strategy. Syst Biol 56:837–856CrossRefPubMedGoogle Scholar
  27. Meyer DB (1977) The avian eye and its adaptations. In: Crescitelli F (ed) The visual system in vertebrates, vol VII/5. Springer, Berlin, pp 549–611Google Scholar
  28. Ödeen A, Håstad O (2003) Complex distribution of avian color vision systems revealed by sequencing the SWS1 opsin from total DNA. Mol Biol Evol 20:855–861CrossRefPubMedGoogle Scholar
  29. Ödeen A, Hart NS, Håstad O (2009) Assessing the use of genomic DNA as a predictor of the maximum absorbance wavelength of avian SWS1 opsin visual pigments. J Comp Physiol A 195:167–173CrossRefGoogle Scholar
  30. Schaefer HM, Schaefer V, Vorobyev (2007) Are fruit colors adapted to consumer vision and birds equally efficient in detecting colourful signals? Am Nat 169:S159–S169CrossRefPubMedGoogle Scholar
  31. Scogin R (1988) Floral anthocyanidins of bird-visited flowers. Bot Gaz 149:437–442CrossRefGoogle Scholar
  32. Shi Y, Yokoyama S (2003) Molecular analysis of the evolutionary significance of ultraviolet vision in vertebrates. Proc Natl Acad Sci USA 100:8308–8313CrossRefPubMedGoogle Scholar
  33. Soltis DE, Bell CD, Kim S, Soltis PS (2008) Origin and evolution of angiosperms. Ann NY Acad Sci 1133:3–25CrossRefPubMedGoogle Scholar
  34. Walls GL (1942) The vertebrate eye and its adaptive radiation. Hafner, New YorkGoogle Scholar
  35. Wilkie SE, Robinson PR, Cronin TW, Poopalasundaram S, Bowmaker JK, Hunt DM (2000) Spectral tuning of avian violet- and ultraviolet-sensitive visual pigments. Biochemistry 39:7895–7901CrossRefPubMedGoogle Scholar
  36. Yokoyama S (2002) Molecular evolution of color vision in vertebrates. Gene 300:69–78CrossRefPubMedGoogle Scholar
  37. Yokoyama S, Radlwimmer FB, Blow NS (2000) Ultraviolet pigments in birds evolved from violet pigments by a single amino acid change. Proc Natl Acad Sci USA 97:7366–7371CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Department of Animal EcologyUppsala UniversityUppsalaSweden
  2. 2.Department of Evolutionary Organismal BiologyUppsala UniversityUppsalaSweden

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