Greater flamingos Phoenicopterus roseus use uropygial secretions as make-up

Abstract

It was long thought that the colour of bird feathers does not change after plumage moult. However, there is increasing evidence that the colour of feathers may change due to abrasion, photochemical change and staining, either accidental or deliberate. The coloration of plumage due to deliberate staining, i.e. with cosmetic purposes, may help individuals to communicate their quality to conspecifics. The presence of carotenoids in preen oils has been previously only suggested, and here we confirm for the first time its presence in such oils. Moreover, the carotenoids in the uropygial secretions were the same specific pigments found in feathers. We show not only that the colour of feathers of greater flamingos Phoenicopterus roseus became more colourful due to the application of carotenoids from uropygial secretions over the plumage but also that the feathers became more colourful with the quantity of pigments applied over them, thus providing evidence of cosmetic coloration. Flamingos used uropygial secretions as cosmetic much more frequently during periods when they were displaying in groups than during the rest of the year, suggesting that the primary function of cosmetic coloration is mate choice. Individuals with more colourful plumage initiated nesting earlier. There was a correlation between plumage coloration before and after removal of uropygial secretions from feathers’ surfaces, suggesting that the use of these pigmented secretions may function as a signal amplifier by increasing the perceptibility of plumage colour, and hence of individual quality. As the cosmetic coloration strengthens signal intensity by reinforcing base-plumage colour, its use may help to the understanding of selection for signal efficacy by making interindividual differences more apparent.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–267

    PubMed  Article  CAS  Google Scholar 

  2. Amat JA, Rendón MA, Rendón-Martos M, Garrido A, Ramírez JM (2005) Ranging behaviour of greater flamingos during the breeding and post-breeding periods: linking connectivity to biological processes. Biol Conserv 125:183–192

    Article  Google Scholar 

  3. Bennett ATD, Cuthill IC (1994) Ultraviolet vision in birds: what is its function? Vis Res 34:1471–1478

    PubMed  Article  CAS  Google Scholar 

  4. Blanco G, Frías O, Garrido-Fernández J, Hornero-Méndez D (2005) Environmental-induced acquisition of nuptial plumage expression: a role of denaturation of feathers caroproteins? Proc R Soc B 272:1893–1900

    PubMed  Article  CAS  Google Scholar 

  5. Britton G (1995) UV/visible spectroscopy. In: Britton G, Liaan-Jensen S, Pfander H (eds) Carotenoids: spectroscopy, vol 1B. Birkäuser, Basel, pp 13–63

    Google Scholar 

  6. Cézilly F, Johnson AR (1995) Re-mating between and within breeding seasons in the greater flamingo Phoenicopterus ruber roseus. Ibis 137:543–546

    Article  Google Scholar 

  7. Cramp S, Simmons KEL (1977) The birds of the Western Palearctic, vol 1. Oxford University Press, Oxford

    Google Scholar 

  8. Davies BH, Köst HP (1988) Carotenoids. In: Köst HP (ed) Handbook of chromatography, vol 1. CRC, Boca Raton, pp 3–188

    Google Scholar 

  9. Delhey K, Peters A, Kempenaers B (2007) Cosmetic coloration in birds: occurrence, function, and evolution. Am Nat 169:S145–S158

    PubMed  Article  Google Scholar 

  10. Delhey K, Peters A, Biedermann P, Kempenaers K (2008) Optical properties of the uropygial gland secretion: no evidence for UV cosmetics in birds. Naturwissenchaften 95:939–946

    Article  CAS  Google Scholar 

  11. Eugster CH (1995) Chemical derivatization: microscale tests for the presence of common functional groups in carotenoids. In: Britton G, Liaan-Jensen S, Pfander H (eds) Carotenoids: isolation and analysis, vol. 1A. Birkäuser, Basel, pp 71–80

    Google Scholar 

  12. Figuerola J, Senar JC (2005) Seasonal changes in carotenoid- and melanin-based plumage coloration in the great tit Parus major. Ibis 147:797–802

    Article  Google Scholar 

  13. Foppen FH (1971) Tables for identification of carotenoid pigments. Chromatogr Rev 14:133–298

    PubMed  Article  CAS  Google Scholar 

  14. Fox DL (1975) Carotenoids in pigmentation. In: Kear J, Duplaix-Hall N (eds) Flamingos. Poyser, Berkhamsted, pp 162–182

    Google Scholar 

  15. Grafen A (1990) Sexual selection unhandicapped by the Fisher process. J Theor Biol 144:473–516

    PubMed  Article  CAS  Google Scholar 

  16. Griggio M, Hoi H, Pilastro A (2010) Plumage maintenance affects ultraviolet colour and female preference in the budgerigar. Behav Proc 84:739–744

    Article  Google Scholar 

  17. Guilford T, Dawkins MS (1991) Receiver psychology and the evolution of animal signals. Anim Behav 42:1–14

    Article  Google Scholar 

  18. Hasson O (1991) Sexual displays as amplifiers: practical examples with an emphasis on feather decorations. Behav Ecol 2:189–197

    Article  Google Scholar 

  19. Hays H, Hudon J, Cormons G, Diconstanzo J, Lima P (2006) The pink feather blush of the roseate tern. Waterbirds 29:296–301

    Article  Google Scholar 

  20. Hill GE (2002) A red bird in a brown bag: the function and evolution of ornamental plumage coloration in the house finch. Oxford University Press, Oxford

    Google Scholar 

  21. Hill GE, Nolan PM, Stoehr AM (1999) Pairing success relative to male plumage redness and pigment symmetry in the house finch: temporal and geographic constancy. Behav Ecol 10:48–53

    Article  Google Scholar 

  22. Johnson A, Cézilly F (2007) The greater flamingo. Poyser, London

    Google Scholar 

  23. Kahl MP (1972) Comparative ethology of the Ciconiidae. The wood-storks (genera Mycteria and Ibis). Ibis 114:15–29

    Article  Google Scholar 

  24. López-Rull I, Pagán I, Macías García C (2010) Cosmetic enhancement of signal coloration: experimental evidence in the house finch. Behav Ecol 21:781–787

    Article  Google Scholar 

  25. Maynard Smith J, Harper D (2003) Animal signals. Oxford University Press, Oxford

    Google Scholar 

  26. McGraw KJ, Hill GE (2004) Plumage color as a dynamic trait: carotenoid pigmentation of male house finches (Carpocadacus mexicanus) fades during the breeding season. Can J Zool 82:734–738

    Article  Google Scholar 

  27. Mínguez-Mosquera MI, Hornero-Méndez D (1993) Separation and quantification of the carotenoid pigments in red peppers (Capsicum annuum L), paprika and oleoresin by reversed-phase HPLC. J Agric Food Chem 41:1616–1620

    Article  Google Scholar 

  28. Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian Poult Biol Rev 11:137–159

    Google Scholar 

  29. Montgomerie R (2006) Cosmetic and adventitious colors. In: Hill GE, McGraw KJ (eds) Bird coloration, vol. I. Harvard University Press, Cambridge, pp 399–427

    Google Scholar 

  30. Negro JJ, Margalida A, Hiraldo F, Heredia R (1999) The function of the cosmetic coloration of bearded vultures: when art imitates life. Anim Behav 58:F14–F17

    PubMed  Article  Google Scholar 

  31. Perdeck AC, Cavé AJ (1992) Laying date in the coot: effects of age and mate choice. J Anim Ecol 61:13–19

    Article  Google Scholar 

  32. Piault R, Gasparini J, Bize P, Paulet M, McGraw KJ, Roulin A (2008) Experimental support for the make-up hypothesis in nestling tawny owls (Strix aluco). Behav Ecol 19:703–709

    Article  Google Scholar 

  33. Piersma T, Dekker M, Damsté JSS (1999) An avian equivalent of make-up? Ecol Lett 2:201–203

    Article  Google Scholar 

  34. Rendón MA, Garrido A, Ramírez JM, Rendón-Martos M, Amat JA (2001) Despotic establishment of breeding colonies of greater flamingos, Phoenicopterus ruber, in southern Spain. Behav Ecol Sociobiol 50:55–60

    Article  Google Scholar 

  35. Reneerkens J, Korsten P (2004) Plumage reflectance is not affected by preen wax composition in red knots Calidris canutus. J Avian Biol 35:405–409

    Article  Google Scholar 

  36. Reneerkens J, Piersma T, Damsté JSS (2002) Sandpipers (Scolopacidae) switch from monoester to diester preen waxes during courtship and incubation, but why? Proc R Soc Lond B 269:2135–2139

    Article  Google Scholar 

  37. Searcy WA, Nowicki S (2005) The evolution of animal communication: reliability and deception in signaling systems. Princeton University Press, Princeton

    Google Scholar 

  38. Seddon N, Tobias JA, Eaton M, Ödeen A (2010) Human vision can provide a valid proxy for avian perception of sexual dichromatism. Auk 127:283–292

    Article  Google Scholar 

  39. Shannon PW (2000) Plumages and molt patterns in captive Caribbean flamingos. Waterbirds 23(Spec Publ 1):160–172

    Google Scholar 

  40. StatSoft Inc (2001) STATISTICA (data analysis software system), version 6. StatSoft, Tulsa

    Google Scholar 

  41. Stegmann B (1956) Über die Herkunft des flüchtigen rosenroten Federpigments. J Ornithol 97:204–205

    Article  CAS  Google Scholar 

  42. Surmacki A (2008) Preen waxes do not protect carotenoid plumage from bleaching by sunlight. Ibis 150:335–341

    Article  Google Scholar 

  43. Surmacki A, Nowakowski JK (2007) Soil and preen waxes influence the expression of carotenoid-based plumage coloration. Naturwissenschaften 94:829–835

    PubMed  Article  CAS  Google Scholar 

  44. Uchida Y (1970) On the color change in Japanese crested ibis. A new type of cosmetic coloration in birds. Misc Rep Yamashina Inst Ornithol 6:54–72, In Japanese, with English summary

    Google Scholar 

  45. Vevers HG (1985) Colour. In: Campbell BC, Lack E (eds) A dictionary of birds. Poyser, Berkhamsted, pp 99–100

    Google Scholar 

  46. Walter BA, Clayton DH (2005) Elaborate ornaments are costly to maintain: evidence for high maintenance handicaps. Behav Ecol 16:89–95

    Article  Google Scholar 

  47. Wiki W (1991) Biological functions and activities of animal carotenoids. Pure Appl Chem 63:141–146

    Article  Google Scholar 

  48. Zahavi A (1975) Mate selection—a selection for a handicap. J Theor Biol 53:205–214

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank M. Adrián, O. González, P. Rodríguez, N. Varo and M. Vázquez for helping to capture flamingos and taking samples, and F. Cézilly, K. Delhey, K.J. McGraw, J.J. Negro, J.C. Senar and two referees for commenting on the manuscript. The Consejería de Medio Ambiente of the Junta de Andalucía and ‘Cañada de los Pájaros’ provided facilities. Funding was provided by Ministerio de Educación y Ciencia of Spain with EU–ERDF support (research grants BOS2002-04695 and CGL2005-01136/BOS).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Juan A. Amat.

Additional information

Communicated by J. Lindström

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 2252 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Amat, J.A., Rendón, M.A., Garrido-Fernández, J. et al. Greater flamingos Phoenicopterus roseus use uropygial secretions as make-up. Behav Ecol Sociobiol 65, 665–673 (2011). https://doi.org/10.1007/s00265-010-1068-z

Download citation

Keywords

  • Carotenoids
  • Cosmetic coloration
  • Plumage colour
  • Plumage maintenance
  • Signals
  • Uropygial secretions