Hoopoes color their eggs with antimicrobial uropygial secretions

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.

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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 65:665–673

    Article  Google 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 273:2821–2829

    Article  Google 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 171:327–338

    PubMed  Article  Google 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 23:293–301

    PubMed  Article  Google 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 65:1721–1730

    Article  Google Scholar 

  6. Burley N (1988) The differential-allocation hypothesis: an experimental test. Am Nat 132:611–628

    Article  Google 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 8:532–537

    PubMed  Article  Google Scholar 

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

    PubMed  Article  Google Scholar 

  9. English PA, Montgomerie R (2011) Robin’s egg blue: does egg color influence male parental care? Behav Ecol Sociobiol 65:1029–1036

    Article  Google 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 6:453–457

    PubMed Central  PubMed  Article  Google 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 584:770–774

    CAS  PubMed  Article  Google 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 359–362

    Google Scholar 

  13. Kilner RM (2006) The evolution of egg colour and patterning in birds. Biol Rev 81:383–406

    CAS  PubMed  Article  Google Scholar 

  14. Krištín A (2001) In: del Hoyo J, Elliot A, Sargatal J (eds) Handbook of the Birds of the World pp 396–441

  15. Küppers H (2002) Atlas de los colores. Blume, Barcelona

    Google Scholar 

  16. Lopez-Rull I, Pagan I, Macias Garcia C (2010) Cosmetic enhancement of signal coloration: experimental evidence in the house finch. Behav Ecol 21:781–787

    Article  Google 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 72:4245–4249

    PubMed Central  PubMed  Article  Google 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 46:205–216

    Article  Google 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 40:191–205

    Article  Google 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 277:123–130

    Article  Google 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:

    PubMed  Google Scholar 

  22. Møller AP, Czirjak GA, Heeb P (2009) Feather micro-organisms and uropygial antimicrobial defences in a colonial passerine bird. Funct Ecol 23:1097–1102

    Article  Google Scholar 

  23. Møller AP, Erritzøe J, Rózsa L (2010) Ectoparasites, uropygial glands and hatching success in birds. Oecologia 163:303–311

    PubMed  Article  Google 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 35:300–304

    Article  Google 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 114:1078–1083

    Article  Google 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 65:1425–1435

    Article  Google 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 19:703–709

    Article  Google Scholar 

  28. Reynolds SJ, Martin GR, Cassey P (2009) Is sexual selection blurring the functional significance of eggshell coloration hypotheses? Anim Behav 78:209–215

    Article  Google 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 212:3621–3626

    PubMed  Article  Google 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:e41843

    PubMed Central  PubMed  Article  Google 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 85:495–502

    CAS  PubMed  Article  Google Scholar 

  32. Shawkey MD, Pillai SR, Hill GE (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J Avian Biol 34:345–349

    Article  Google Scholar 

  33. Soler JJ, Møller AP, Soler M (1998) Nest building, sexual selection and parental investment. Evol Ecol 12:427–441

    Article  Google 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 22:864–871

    Article  Google Scholar 

  35. Soler JJ, Navarro C, Pérez-Contreras T, Avilés JM, Cuervo JJ (2008b) Sexually selected egg coloration in spotless starlings. Am Nat 171:183–194

    PubMed  Article  Google 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 3:93–100

    Article  Google 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 25:1779–1791

    CAS  PubMed  Article  Google 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 280–289

    Google Scholar 

  39. Wesolowski T, Maziarz M (2012) Dark tree cavities—a challenge for hole nesting birds? J Avian Biol 43:454–460

    Article  Google Scholar 

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Acknowledgments

Jorge Doña Reguera, Ana Belén García Martín, Jonathan Romero Masegosa, and Manuel Soto Cárdenas helped in caring for the captive breeding population. Estefanía López Hernández helped with the laboratory tasks. Comments and suggestions by Magdalena Ruiz Rodríguez and two anonymous reviewers on a previous version greatly improved the understanding of the paper. Support by funding was provided by Spanish Ministerio de Ciencia e Innovación, European funds (FEDER) (CGL2005-06975/BOS, CGL2009-14006, CGL2010-19233-C03-01 and CGL2010-19233-C03-03) and Junta de Andalucía (P09-RNM-4557).

Ethical standards

The experiment was conducted according to relevant Spanish national guidelines (Real Decreto 1201/2005, de 10 de Octubre) and under the permission of Junta de Andalucía, Dirección General de Gestión del Medio Natural which authorized the establishment and maintenance of the captive breeding population (Resolución de 14 de Abril de 2008) and conceded the permits required to perform the present research according to Spanish regulations (Resoluciones de 14 de Abril de 2008 and 23 de Marzo de 2010).

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Correspondence to Juan J. Soler.

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Juan J. Soler and M. Martín-Vivaldi contributed equally to this work.

Communicated by: Alexandre Roulin

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Soler, J.J., Martín-Vivaldi, M., Peralta-Sánchez, J.M. et al. Hoopoes color their eggs with antimicrobial uropygial secretions. Naturwissenschaften 101, 697–705 (2014). https://doi.org/10.1007/s00114-014-1201-3

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Keywords

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