Skip to main content

Do feather-degrading bacteria actually degrade feather colour? No significant effects of plumage microbiome modifications on feather colouration in wild great tits

Abstract

Parasites are known to exert selective pressures on host life history traits since the energy and nutrients needed to mount an immune response are no longer available to invest in other functions. Bird feathers harbour numerous microorganisms, some of which are able to degrade feather keratin (keratinolytic microorganisms) and affect feather integrity and colouration in vitro. Although named “feather-degrading” microorganisms, experimental evidence for their effects on feathers of free-living birds is still lacking. Here, we tested whether (i) keratinolytic microorganisms can degrade feathers in vivo and thus modify the colour of feathers during the nesting period and (ii) whether feather microorganisms have a long-term effect on the investment in colouration of newly moulted feathers. We designed treatments to either favour or inhibit bacterial growth, thus experimentally modifying plumage bacterial communities, in a wild breeding population of great tits (Parus major). Our analyses revealed no significant effects of the treatments on feather colours. Moreover, we found that differences in bacterial exposure during nesting did not significantly affect the colouration of newly moulted feathers. Our results suggest that significant feather degradation obtained during in vitro studies could have led to an overestimation of the potential of keratinolytic microorganisms to shape feather colouration in free-living birds.

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

Fig. 1

References

  • Aguilera E, Amat JA (2007) Carotenoids, immune response and the expression of sexual ornaments in male greenfinches (Carduelis chloris). Naturwissenschaften 94:895–902. doi:10.1007/s00114-007-0268-5

    PubMed  Article  CAS  Google Scholar 

  • Burtt JE, Ichida J (1999) Occurrence of feather-degrading bacilli in the plumage of birds. Auk 116:364–372

    Article  Google Scholar 

  • Burtt EH, Schroeder MR, Smith LA et al (2011) Colourful parrot feathers resist bacterial degradation. Biol Lett 7:214–216. doi:10.1098/rsbl.2010.0716

    PubMed  Article  PubMed Central  Google Scholar 

  • Clayton D (1999) Feather-busting bacteria. Auk 116:302–304

    Article  Google Scholar 

  • Clayton DH, Moore J (1997) Host-parasite evolution: general principles and avian models. Press, Oxford University

    Google Scholar 

  • 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 

  • Cristol D, Armstrong J, Whitaker J (2005) Feather-degrading bacteria do not affect feathers on captive birds. Auk 122:222–230

    Article  Google Scholar 

  • Cuthill IC, Partridge JC, Bennett ATD et al (2000) Ultraviolet vision in birds. Adv Study Behav 29:159–215

    Article  Google Scholar 

  • Czirják GA, Møller AP, Mousseau TA, Heeb P (2010) Microorganisms associated with feathers of barn swallows in radioactively contaminated areas around chernobyl. Microb Ecol 60:373–380

    PubMed  Article  Google Scholar 

  • Delhey K, Burger C, Fiedler W, Peters A (2010) Seasonal changes in colour: a comparison of structural, melanin- and carotenoid-based plumage colours. PLoS One 5:e11582. doi:10.1371/journal.pone.0011582

    PubMed  Article  PubMed Central  Google Scholar 

  • Economou T, Pournis N, Ntzimani A, Savvaidis IN (2009) Nisin–EDTA treatments and modified atmosphere packaging to increase fresh chicken meat shelf-life. Food Chem 114:1470–1476

    Article  CAS  Google Scholar 

  • Faust K, Sathirapongsasuti JF, Izard J et al (2012) Microbial co-occurrence relationships in the human microbiome. PLoS Comput Biol 8:e1002606

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Galván I (2010) Plumage coloration can be perceived as a multiple condition-dependent signal by Great Tits Parus major. Ibis 152:359–367

    Article  Google Scholar 

  • Gilbert S, Sapp J, Tauber A (2012) A symbiotic view of life: we have never been individuals. Q Rev Biol 87:325–341

    PubMed  Article  Google Scholar 

  • Giraudeau M, Czirják GÁ, Duval C et al (2010) No detected effect of moult on feather bacterial loads in mallards Anas platyrhynchos. J Avian Biol 41:678–680. doi:10.1111/j.1600-048X.2010.05144.x

    Article  Google Scholar 

  • Giraudeau M, Czirják GÁ, Duval C et al (2012) Effect of preen oil on plumage bacteria: an experimental test with the mallard. Behav Process 92:1–5

    Article  Google Scholar 

  • Gosler A (1993) The great tit. Hamlyn Species Guides, Paul Hamlyn, London

    Google Scholar 

  • Gunderson AR (2008) Feather-degrading bacteria: a new frontier in avian and host-parasite research? Auk 125:972–979

    Article  Google Scholar 

  • Gunderson AR, Forsyth MH, Swaddle JP (2009) Evidence that plumage bacteria influence feather coloration and body condition of eastern bluebirds Sialia sialis. J Avian Biol 40:440–447. doi:10.1111/j.1600-048X.2008.04650.x

    Article  Google Scholar 

  • Harris L, Fleming H, Klaenhammer T (1992) Developments in nisin research. Food Res Int 25:57–66

    Article  CAS  Google Scholar 

  • Hill G, McGraw K (2006) Bird coloration, volume 2: function and evolution. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Hõrak P, Vellau H, Ots I, Møller AP (2000) Growth conditions affect carotenoid-based plumage coloration of great tit nestlings. Naturwissenschaften 87:460–464

    PubMed  Article  Google Scholar 

  • Jacob S, Immer A, Leclaire S et al (2014) Uropygial gland size and composition varies according to experimentally modified microbiome in Great tits. BMC Evol Biol 14:134. doi:10.1186/1471-2148-14-134

    PubMed  Article  PubMed Central  Google Scholar 

  • Jacobs G (1981) Comparative color vision. Academic, New York

    Google Scholar 

  • Kilgas P, Saag P, Mägi M et al (2012a) Variation in assemblages of feather bacteria in relation to plumage color in female great tits. Condor 114:606–611. doi:10.1525/cond.2012.110103

    Article  Google Scholar 

  • Kilgas P, Saag P, Mägi M et al (2012b) Plumage bacterial load increases during nest-building in a passerine bird. J Ornithol 153:833–838. doi:10.1007/s10336-011-0801-3

    Article  Google Scholar 

  • Lucas FS, Broennimann O, Febbraro I, Heeb P (2003) High diversity among feather-degrading bacteria from a dry meadow soil. Microb Ecol 45:282–290. doi:10.1007/s00248-002-2032-x

    PubMed  Article  CAS  Google Scholar 

  • Lucas F, Moureau B, Jourdie V, Heeb P (2005) Brood size modifications affect plumage bacterial assemblages of European starlings. Mol Ecol 14:639–646. doi:10.1111/j.1365-294x.2005.02436.x

    PubMed  Article  Google Scholar 

  • McFall-Ngai M, Hadfield MG, Bosch TCG et al (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci U S A 110:3229–3236

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Metcalfe NB, Monaghan P (2013) Does reproduction cause oxidative stress? An open question. Trends Ecol Evol 28:347–350

    PubMed  Article  Google Scholar 

  • Møller AP, Czirjak GÃ, Heeb P (2009) Feather micro-organisms and uropygial antimicrobial defences in a colonial passerine bird. Funct Ecol 23:1097–1102. doi:10.1111/j.1365-2435.2009.01594.x

    Article  Google Scholar 

  • Moreno-Rueda G (2010) Experimental test of a trade-off between moult and immune response in house sparrows Passer domesticus. J Evol Biol 23:2229–2237. doi:10.1111/j.1420-9101.2010.02090.x

    PubMed  Article  CAS  Google Scholar 

  • Morgan XC, Segata N, Huttenhower C (2013) Biodiversity and functional genomics in the human microbiome. Trends Genet 29:51–58. doi:10.1016/j.tig.2012.09.005

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Navara KJ, Hill GE (2003) Dietary carotenoid pigments and immune function in a songbird with extensive carotenoid-based plumage coloration. Behav Ecol 14:909–916. doi:10.1093/beheco/arg085

    Article  Google Scholar 

  • Olson VA, Owens IP (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514

    PubMed  Article  CAS  Google Scholar 

  • Onifade AA, Al-Sane NA, Al-Musallam AA, Al-Zarban S (1998) A review: Potentials for biotechnological applications of keratin-degrading microorganisms and their enzymes for nutritional improvement of feathers and other keratins as livestock feed resources. Bioresour Technol 66:1–11. doi:10.1016/S0960-8524(98)00033-9

    Article  CAS  Google Scholar 

  • Ranjard L, Brothier E, Nazaret S (2000) Sequencing bands of ribosomal intergenic spacer analysis fingerprints for characterization and microscale distribution of soil bacterium populations responding to mercury spiking. Appl Environ Microbiol 66:5334–5339

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Ruiz-De-Castañeda R, Gonzalez-Braojos S, Moreno J (2012) Bacterial degradability of an intrafeather unmelanized ornament: a role for feather-degrading bacteria in sexual selection? Biol J Linn Soc 105:409–419. doi:10.1111/j.1095-8312.2011.01806.x

  • Ruiz-Rodríguez M, Valdivia E, Soler JJ et al (2009) Symbiotic bacteria living in the hoopoe’s uropygial gland prevent feather degradation. J Exp Biol 212:3621–3626. doi:10.1242/jeb.031336

    PubMed  Article  Google Scholar 

  • Saag P, Tilgar V, Mänd R et al (2011) Plumage bacterial assemblages in a breeding wild passerine: relationships with ecological factors and body condition. Microb Ecol 61:740–749. doi:10.1007/s00248-010-9789-0

    PubMed  Article  Google Scholar 

  • Schmid-Hempel P (2011) Evolutionary parasitology: the integrated study of infections, immunology, ecology, and genetics. Press, Oxford University

    Google Scholar 

  • Schulte-Hostedde A, Zinner B, Millar J, Hickling G (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 84:155–163

    Article  Google Scholar 

  • Senar JC, Negro J, Quesada J et al (2008) Two pieces of information in a single trait? The yellow breast of the great tit (Parus major) reflects both and body condition pigment acquisition. Behaviour 145:1195–1210

    Article  Google Scholar 

  • Shawkey MD, Pillai SR, Hill GE (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J Avian Biol 34:345–349. doi:10.1111/j.0908-8857.2003.03193.x

    Article  Google Scholar 

  • Shawkey MD, Pillai SR, Hill GE et al (2007) Bacteria as an agent for change in structural plumage color: correlational and experimental evidence. Am Nat 169(Suppl):S112–S121. doi:10.1086/510100

    PubMed  Article  Google Scholar 

  • Shawkey MD, Pillai SR, Hill GE (2009) Do feather-degrading bacteria affect sexually selected plumage color? Naturwissenschaften 96:123–128. doi:10.1007/s00114-008-0462-0

    PubMed  Article  CAS  Google Scholar 

  • Slagsvold T, Lifjeld J (1985) Variation in plumage colour of the great tit Parus major in relation to habitat, season and food. J Zool 206:321–328

    Article  Google Scholar 

  • Vézina F, Gustowska A, Jalvingh K (2009) Hormonal correlates and thermoregulatory consequences of molting on metabolic rate in a northerly wintering shorebird. Physiol Biochem Zool 82:129–142

    PubMed  Article  Google Scholar 

  • Wang JM, Firestone MK, Beissinger SR (2011) Microbial and environmental effects on avian egg viability: do tropical mechanisms act in a temperate environment? Ecology 92:1137–1145

    PubMed  Article  Google Scholar 

  • Yamamura S, Morita Y, Hasan Q et al (2002) Keratin degradation: a cooperative action of two enzymes from Stenotrophomonas sp. Biochem Biophys Res Commun 294:1138–1143. doi:10.1016/S0006-291X(02)00580-6

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgements

We wish to dedicate this paper to our invaluable collaborator Léa Colmas who was recently sadly taken by an avalanche. Léa performed an excellent work during this study as part of her master’s. She was greatly appreciated and liked for her warmth, kindness and intellectual abilities and is profoundly missed. We thank the families Bordes, Gers and Labories who allowed us to install nest boxes on their site. Carole Sembeille, Marion Roullin, Marc Etchecopart Echechar and Charlotte Perrot helped during the fieldwork. We thank Mélanie Roy, Jean-Baptiste Ferdy and Pascal Le Bourgeois for discussions and Bob Montgomerie for useful comments on an earlier version of the manuscript. This work is part of the Laboratoires d’Excellence (LABEX) entitled TULIP (ANR-10-LABX-41).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Staffan Jacob.

Additional information

Communicated by: Alexandre Roulin

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Jacob, S., Colmas, L., Parthuisot, N. et al. Do feather-degrading bacteria actually degrade feather colour? No significant effects of plumage microbiome modifications on feather colouration in wild great tits. Naturwissenschaften 101, 929–938 (2014). https://doi.org/10.1007/s00114-014-1234-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-014-1234-7

Keywords

  • Feather colouration
  • Feather-degrading microorganisms
  • Keratinolytic microorganisms
  • Microbiome
  • Sexual selection
  • Visual communication