Naturwissenschaften

, Volume 101, Issue 9, pp 697–705

Hoopoes color their eggs with antimicrobial uropygial secretions

  • Juan J. Soler
  • M. Martín-Vivaldi
  • J. M. Peralta-Sánchez
  • L. Arco
  • N. Juárez-García-Pelayo
Original Paper

Abstract

Uropygial gland secretions are used as cosmetics by some species of birds to color and enhance properties of feathers and teguments, which may signal individual quality. Uropygial secretions also reach eggshells during incubation and, therefore, may influence the coloration of birds’ eggs, a trait that has attracted the attention of evolutionary biologists for more than one century. The color of hoopoe eggs typically changes along incubation, from bluish-gray to greenish-brown. Here, we test experimentally the hypothesis that dark uropygial secretion of females is responsible for such drastic color change. Moreover, since uropygial secretion of hoopoes has antimicrobial properties, we also explore the association between color and antimicrobial activity of the uropygial secretion of females. We found that eggs stayed bluish-gray in nests where female access to the uropygial secretion was experimentally blocked. Furthermore, experimental eggs that were maintained in incubators and manually smeared with uropygial secretion experienced similar color changes that naturally incubated eggs did, while control eggs that were not in contact with the secretions did not experience such color changes. All these results strongly support the hypothesis that female hoopoes use their uropygial gland secretion to color the eggs. Moreover, saturation of the uropygial secretion was associated with antimicrobial activity against Bacillus licheniformis. Given the known antimicrobial potential of uropygial secretions of birds, this finding opens the possibility that in scenarios of sexual selection, hoopoes in particular and birds in general signal antimicrobial properties of their uropygial secretion by mean of changes in egg coloration along incubation.

Keywords

Antimicrobials Bacteria Egg color change Cosmetics Eggshells Sexual signal Uropygial gland secretion 

References

  1. Amat JA, Rendon MA, Garrido-Fernandez J, Garrido A, Rendon-Martos M, Perez-Galvez A (2011) Greater flamingos Phoenicopterus roseus use uropygial secretions as make-up. Behav Ecol Sociobiol 65:665–673CrossRefGoogle Scholar
  2. Avilés JM, Soler JJ, Pérez-Contreras T (2006) Dark nests and egg colour in birds: a possible functional role of ultraviolet reflectance in egg detectability. Proc R Soc Lond B 273:2821–2829CrossRefGoogle Scholar
  3. Avilés JM, Perez-Contreras T, Navarro C, Soler JJ (2008) Dark nests and conspicuousness in color patterns of nestlings of altricial birds. Am Nat 171:327–338PubMedCrossRefGoogle Scholar
  4. Avilés JM, Vikan JR, Fossoy F, Antonov A, Moksnes A, Roskaft E, Stokke BG (2010) Avian colour perception predicts behavioural responses to experimental brood parasitism in chaffinches. J Evol Biol 23:293–301PubMedCrossRefGoogle Scholar
  5. Avilés JM, Soler JJ, Hart NS (2011) Sexual selection based on egg colour: physiological models and egg discrimination experiments in a cavity-nesting bird. Behav Ecol Sociobiol 65:1721–1730CrossRefGoogle Scholar
  6. Burley N (1988) The differential-allocation hypothesis: an experimental test. Am Nat 132:611–628CrossRefGoogle Scholar
  7. Cook MI, Beissinger SR, Toranzos GA, Arendt WJ (2005) Incubation reduces microbial growth on eggshells and the opportunity for trans-shell infection. Ecol Lett 8:532–537PubMedCrossRefGoogle Scholar
  8. Delhey K, Peters A, Kempenaers B (2007) Cosmetic coloration in birds: occurrence, function, and evolution. Am Nat 169:S145–S158PubMedCrossRefGoogle Scholar
  9. English PA, Montgomerie R (2011) Robin’s egg blue: does egg color influence male parental care? Behav Ecol Sociobiol 65:1029–1036CrossRefGoogle Scholar
  10. Holveck MJ, Doutrelant C, Guerreiro R, Perret P, Gomez D, Grégoire A (2010) Can eggs in a cavity be a female secondary sexual signal? Male nest visits and modelling of egg visual discrimination in blue tits. Biol Lett 6:453–457PubMedCentralPubMedCrossRefGoogle Scholar
  11. Ishikawa S, Suzuki K, Fukuda E, Arihara K, Yamamoto Y, Mukai T, Itoh M (2010) Photodynamic antimicrobial activity of avian eggshell pigments. FEBS Lett 584:770–774PubMedCrossRefGoogle Scholar
  12. Jacob J, Ziswiler V (1982) The uropygial gland. In: Farner DS, King JR, Parkes KC (eds) Avian biology, vol VII. Academic, London, pp 359–362Google Scholar
  13. Kilner RM (2006) The evolution of egg colour and patterning in birds. Biol Rev 81:383–406PubMedCrossRefGoogle Scholar
  14. Krištín A (2001) In: del Hoyo J, Elliot A, Sargatal J (eds) Handbook of the Birds of the World pp 396–441Google Scholar
  15. Küppers H (2002) Atlas de los colores. Blume, BarcelonaGoogle Scholar
  16. Lopez-Rull I, Pagan I, Macias Garcia C (2010) Cosmetic enhancement of signal coloration: experimental evidence in the house finch. Behav Ecol 21:781–787CrossRefGoogle Scholar
  17. Martín-Platero AM, Valdivia E, Ruiz-Rodríguez M, Soler JJ, Martín-Vivaldi M, Maqueda M, Martínez-Bueno M (2006) Characterization of antimicrobial substances produced by Enterococcus faecalis MRR 10–3, isolated from the uropygial gland of the hoopoe Upupa epops. Appl Environ Microbiol 72:4245–4249PubMedCentralPubMedCrossRefGoogle Scholar
  18. Martín-Vivaldi M, Palomino JJ, Soler M, Soler JJ (1999) Determinants of reproductive success in the hoopoe Upupa epops, a hole-nesting non-passerine bird with asynchronous hatching. Bird Study 46:205–216CrossRefGoogle Scholar
  19. Martín-Vivaldi M, Ruiz-Rodriguez M, Soler JJ, Peralta-Sanchez JM, Mendez M, Valdivia E, Martin-Platero AM, Martínez-Bueno M (2009) Seasonal, sexual and developmental differences in hoopoe Upupa epops preen gland morphology and secretions: evidence for a role of bacteria. J Avian Biol 40:191–205CrossRefGoogle Scholar
  20. Martín-Vivaldi M, Peña A, Peralta-Sánchez JM, Sánchez L, Ananou S, Ruiz-Rodríguez M, Soler JJ (2010) Antimicrobial chemicals in hoopoe preen secretions are produced by symbiotic bacteria. Proc R Soc Lond B 277:123–130CrossRefGoogle Scholar
  21. Martín-Vivaldi M, Soler JJ, Peralta-Sánchez JM, Arco L, Martín-Platero AM, Martínez-Bueno M, Ruiz-Rodríguez M, Valdivia E (2014) Special structures of hoopoe eggshells enhance the adhesion of symbiont-carrying uropygial secretion that increase hatching success. J Anim Ecol. doi:10.1111/1365-2656.12243: PubMedGoogle Scholar
  22. Møller AP, Czirjak GA, Heeb P (2009) Feather micro-organisms and uropygial antimicrobial defences in a colonial passerine bird. Funct Ecol 23:1097–1102CrossRefGoogle Scholar
  23. Møller AP, Erritzøe J, Rózsa L (2010) Ectoparasites, uropygial glands and hatching success in birds. Oecologia 163:303–311PubMedCrossRefGoogle Scholar
  24. Moreno J, Osorno JL, Morales J, Merino S, Tomás G (2004) Egg colouration and male parental effort in the pied flycatcher Ficedula hypoleuca. J Avian Biol 35:300–304CrossRefGoogle Scholar
  25. Moreno J, Lobato E, Merino S, Martinez-de La Puente J (2008) Blue-green eggs in pied flycatchers: an experimental demonstration that a supernormal stimulus elicits improved nestling condition. Ethology 114:1078–1083CrossRefGoogle Scholar
  26. Perez-Rodriguez L, Mougeot F, Bortolotti GR (2011) The effects of preen oils and soiling on the UV-visible reflectance of carotenoid-pigmented feathers. Behav Ecol Sociobiol 65:1425–1435CrossRefGoogle Scholar
  27. Piault R, Gasparini J, Bize P, Paulet M, McGraw KJ, Roulin A (2008) Experimental support for the makeup hypothesis in nestling tawny owls (Strix aluco). Behav Ecol 19:703–709CrossRefGoogle Scholar
  28. Reynolds SJ, Martin GR, Cassey P (2009) Is sexual selection blurring the functional significance of eggshell coloration hypotheses? Anim Behav 78:209–215CrossRefGoogle Scholar
  29. Ruiz-Rodríguez M, Valdivia E, Soler JJ, Martin-Vivaldi M, Martin-Platero AM, Martinez-Bueno M (2009) Symbiotic bacteria living in the hoopoe’s uropygial gland prevent feather degradation. J Exp Biol 212:3621–3626PubMedCrossRefGoogle Scholar
  30. Ruiz-Rodríguez M, Valdivia E, Martín-Vivaldi M, Martín-Platero AM, Martínez-Bueno M, Méndez M, Peralta-Sánchez JM, Soler JJ (2012) Antimicrobial activity and genetic profile of enteroccoci isolated from hoopoes uropygial gland. PLoS ONE 7:e41843PubMedCentralPubMedCrossRefGoogle Scholar
  31. Ruiz-Rodriguez M, Martinez-Bueno M, Martin-Vivaldi M, Valdivia E, Soler JJ (2013) Bacteriocins with a broader antimicrobial spectrum prevail in enterococcal symbionts isolated from the hoopoe’s uropygial gland. FEMS Microbiol Ecol 85:495–502PubMedCrossRefGoogle Scholar
  32. Shawkey MD, Pillai SR, Hill GE (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J Avian Biol 34:345–349CrossRefGoogle Scholar
  33. Soler JJ, Møller AP, Soler M (1998) Nest building, sexual selection and parental investment. Evol Ecol 12:427–441CrossRefGoogle Scholar
  34. Soler JJ, Martín-Vivaldi M, Ruiz-Rodríguez M, Valdivia E, Martín-Platero AM, Martínez-Bueno M, Peralta-Sánchez JM, Méndez M (2008a) Symbiotic association between hoopoes and antibiotic-producing bacteria that live in their uropygial gland. Funct Ecol 22:864–871CrossRefGoogle Scholar
  35. Soler JJ, Navarro C, Pérez-Contreras T, Avilés JM, Cuervo JJ (2008b) Sexually selected egg coloration in spotless starlings. Am Nat 171:183–194PubMedCrossRefGoogle Scholar
  36. Soler JJ, Martín-Vivaldi M, Peralta-Sánchez JM, Ruiz-Rodríguez M (2010) Antibiotic-producing bacteria as a possible defence of birds against pathogenic microorganisms. Open Ornithol J 3:93–100CrossRefGoogle Scholar
  37. Soler JJ, Peralta-Sánchez JM, Martín-Platero AM, Martín-Vivaldi M, Martínez-Bueno M, Møller AP (2012) The evolution of size of the uropygial gland: mutualistic feather mites and uropygial secretion reduce bacterial loads of eggshells and hatching failures of European birds. J Evol Biol 25:1779–1791PubMedCrossRefGoogle Scholar
  38. Underwood TJ, Sealy SG (2002) Adaptive significance of egg coloration. In: Deeming DC (ed) Avian incubation, behaviour, environment and evolution. Oxford University Press, Oxford, pp 280–289Google Scholar
  39. Wesolowski T, Maziarz M (2012) Dark tree cavities—a challenge for hole nesting birds? J Avian Biol 43:454–460CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Juan J. Soler
    • 1
    • 2
  • M. Martín-Vivaldi
    • 2
    • 3
  • J. M. Peralta-Sánchez
    • 2
    • 4
  • L. Arco
    • 2
    • 3
  • N. Juárez-García-Pelayo
    • 5
  1. 1.Estación Experimental de Zonas Áridas (CSIC)AlmeríaSpain
  2. 2.Grupo Coevolución, Unidad Asociada al CSICUniversidad de GranadaGranadaSpain
  3. 3.Departamento de ZoologíaUniversidad de GranadaGranadaSpain
  4. 4.Departamento de MicrobiogíaUniversidad de GranadaGranadaSpain
  5. 5.EstepaSpain

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