Variation in Plumage Microbiota Depends on Season and Migration

Abstract

Migratory birds can be efficient dispersers of pathogens, yet we know little about the effect of migration and season on the microbial community in avian plumage. This is the first study to describe and compare the microbial plumage community of adult and juvenile migratory birds during the annual cycle and compare the plumage community of migrants to that of resident birds at both neotropical and nearctic locations. We used length heterogeneity PCR (16S rRNA) to describe the microbial assemblage sampled from the plumage of 66 birds in two age classes and from 16 soil samples. Resident birds differed significantly in plumage microbial community composition from migrants (R ≥ 0.238, P < 0.01). Nearctic resident birds had higher plumage microbial diversity than nearctic migrants (R = 0.402, P < 0.01). Plumage microbial composition differed significantly between fall premigratory and either breeding (R ≥ 0.161, P < 0.05) or nonbreeding stages (R = 0.267, P < 0.01). Six bacterial operational taxonomic units contributed most to the dissimilarities found in this assay. Soil microbial community composition was significantly different from all samples of plumage microbial communities (R ≥ 0.700, P < 0.01). The plumage microbial community varies in relation to migration strategy and stage of the annual cycle. We suggest that plumage microbial acquisition begins in the first year at natal breeding locations and reaches equilibrium at the neotropical wintering sites. These data lead us to conclude that migration and season play an important role in the dynamics of the microbial community in avian plumage and may reflect patterns of pathogen dispersal by birds.

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References

  1. 1.

    Baas Becking LGM (1934) Geobiologie of inleiding tot de milieukunde. WP Van Stockum and Zoon, The Hague

    Google Scholar 

  2. 2.

    Bandyopadhyay A, Bhattacharyya SP (1999) Influence of fowl uropygial gland and its secretory lipid components on the growth of skin surface fungi of fowl. Indian J Exp Biol 37:1218–1222

    PubMed  CAS  Google Scholar 

  3. 3.

    Bisson I-A, Marra PP, Burtt EH, Sikaroodi M, Gillevet PM (2007) A molecular comparison of plumage and soil bacteria across biogeographic, ecological, and taxonomic scales. Microb Ecol 54:65–81

    PubMed  Article  Google Scholar 

  4. 4.

    Bray JR, Curtis JT (1957) An ordination of the upland forest communities of Southern Wisconsin. Ecol Monogr 27:325–349

    Article  Google Scholar 

  5. 5.

    Burtt EH, Ichida JM (2004) Gloger’s rule, feather-degrading bacteria, and color variation among song sparrows. Condor 106:681–686

    Article  Google Scholar 

  6. 6.

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

    Google Scholar 

  7. 7.

    Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  8. 8.

    Clarke KR, Gorley RN (2001) Primer v.5: user manual/tutorial. PRIMER-E. Plymouth Marine Laboratory, Plymouth

    Google Scholar 

  9. 9.

    Cristol DA, Armstrong JL, Whitaker JM, Forsyth MH (2005) Feather-degrading bacteria do not affect feathers on captive birds. Auk 122:222–230

    Article  Google Scholar 

  10. 10.

    Gunderson AR, Forsythe MH, Swaddle JP (2009) Evidence that plumage bacteria influence feather coloration and body condition in a passerine. J Avian Biol 40 (in press)

  11. 11.

    Guzy MJ, Ritchison G (1999) Common Yellowthroat (Geothlypis trichas). In: Poole, A, Gill, F (eds) The birds of North America, No. 448. The Birds of North America, Philadelphia

    Google Scholar 

  12. 12.

    Gylfe A, Bergström S, Lundström J, Olsen B (2000) Reactivation of Borrelia infection in birds. Nature 403:724–725

    PubMed  Article  CAS  Google Scholar 

  13. 13.

    Hubalék Z (2004) An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildlife Dis 40:639–659

    Google Scholar 

  14. 14.

    Lane DJ (1991) 16S/23S rRNA sequencing. Nucleic acid techniques in bacterial systematics. E.S. a. M. Goodlfellow. Wiley, West Sussex

    Google Scholar 

  15. 15.

    Litchfield CD, Gillevet PM (2002) Microbial diversity and complexity in hypersaline environments: a preliminary assessment. J Ind Microbiol Biot 28:48–55

    Article  CAS  Google Scholar 

  16. 16.

    Liu J, Xiao H, Lei F, Zhu Q, Qin K, Zhang X-W, Zhang X-I, Zhao D, Wang G, Feng Y, Ma J, Liu W, Wang J, Gao GF (2005) Highly pathogenic H5N 1 influenza virus infection in migratory birds. Science 309:1206

    PubMed  Article  CAS  Google Scholar 

  17. 17.

    Lucas FS, Moureau B, Jourdie V, Heeb P (2005) Brood size modifications affect plumage bacterial assemblages of European starlings. Mol Ecol 14:639–646

    PubMed  Article  Google Scholar 

  18. 18.

    Lucas FS, Broenimann O, Febbraro I, Heeb P (2003) High diversity among feather-degrading bacteria from a dry meadow soil. Microb Ecol 45:282–290

    PubMed  Article  CAS  Google Scholar 

  19. 19.

    MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton

    Google Scholar 

  20. 20.

    Marra PP, Griffing S, Cafree CL, Kilpatrick AM, Mclean R, Brand C, Kramer L, Novak R (2004) West Nile virus and wildlife. Bioscience 54:393–402

    Article  Google Scholar 

  21. 21.

    Mills DK, Fitzgerald K, Litchfield CD, Gillevet PM (2003) A comparison of DNA profiling techniques for monitoring nutrient impact on microbial community composition during bioremediation of petroleum contaminated soils. J Microbiol Meth 54:57–74

    Article  CAS  Google Scholar 

  22. 22.

    Peele AM, Burtt EH Jr, Schroeder MR, Greenberg RS (2009) Dark color of Coastal Plains Swamp Sparrow may be an evolutionary response to occurrence and abundance of salt-tolerant, feather-degrading bacilli in its plumage. Auk 126 (in press)

  23. 23.

    Raffaele H, Wiley J, Garrido OH, Keith A, Raffaele JI (1998) A guide to the birds of the West Indies. Princeton University Press, Princeton

    Google Scholar 

  24. 24.

    Rappole JH, Derrickson SR, Hubalek Z (2000) Migratory birds and spread of West Nile virus in the western hemisphere. Emerg Infect Dis 6:319–328

    PubMed  CAS  Google Scholar 

  25. 25.

    Reche I, Pulido-Villena E, Morales-Baquero R, Casamayor EO (2005) Does ecosystem size determine aquatic bacterial richness? Ecology 86:1715–1722

    Article  Google Scholar 

  26. 26.

    Reed KD, Meece JK, Henkel JS, Shukla KS (2003) Birds, migration and emerging zoonoses: West Nile virus, Lyme disease, Influenza A and enteropathogens. Clin Med Res 1:5–12

    PubMed  Article  Google Scholar 

  27. 27.

    Reneerkens J, Versteegh MA, Schneider AM, Piersma T, Burtt EH (2008) Seasonally changing preen-wax composition: red knots (Calidris canutus) flexible defense against feather-degrading bacteria? Auk 125:285–290

    Article  Google Scholar 

  28. 28.

    Reneerkens J, Piersma T, Sinninghe Damste’ JS (2002) Sandpipers (Scolopacidae) switch from mono- to diester preen waxes during courtship and incubation, but why? Proc R Soc Lond B Biol Sci 269:2135–2139

    Article  Google Scholar 

  29. 29.

    Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, Urbana

    Google Scholar 

  30. 30.

    Shawkey MD, Pilai SR, Hill GE (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J Avian Biol 34:345–352

    Article  Google Scholar 

  31. 31.

    Shawkey MD, Mills KL, Dale C, Hill GE (2005) Microbial diversity of wild bird feathers revealed through culture-based and culture-independent techniques. Microb Ecol 50:40–47

    PubMed  Article  Google Scholar 

  32. 32.

    Soini, HA, Schrock SE, Bruce KE, Wiesler D, Ketterson ED, Novotny MV (2007) Seasonal variation in volatile compound profiles of preen gland secretions of the Dark-eyed Junco (Junco hyemalis). J Chem Ecol 33:183–198

    PubMed  Article  CAS  Google Scholar 

  33. 33.

    Waldenström J, Broman T, Carlsson I, Hasselquist D, Achterberg RP, Wagenaar JA, Olsen B (2002) Prevalence of Campylobacter jejuni, Campylobacter lari, and Campylobacter coli in different ecological guilds and taxa of migrant birds. Appl Environ Microbiol 68:5911–5917

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

This research was supported, in part, by funding from the Loeb fund and a Post-doctoral fellowship from the Smithsonian Institution and a National Science Foundation DEB-0089565 grant to P. P. Marra. We thank the Petroleum Corporation of Jamaica for permission to conduct this research at the Font Hill Nature Preserve and the National Environmental Protection Agency of Jamaica for their cooperation with our research in Jamaica. Thank you to the Patuxent River Park for permission to work in the park in Maryland. The Institutional Animal Care and Use Committee of the Smithsonian Environmental Research Center approved all protocols used in this study. We also thank L. Butler, T. Sherry, C. Studds. S. Sillett, D. Brown, L. Duda, A. Logie, J. O’Neil, M. McCormick, and D. Whigham for their help in the field, useful suggestions in the laboratory analyses, and helpful comments on the manuscript.

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Correspondence to Isabelle-A. Bisson.

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Bisson, IA., Marra, P.P., Burtt Jr, E.H. et al. Variation in Plumage Microbiota Depends on Season and Migration. Microb Ecol 58, 212 (2009). https://doi.org/10.1007/s00248-009-9490-3

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Keywords

  • Microbial Community
  • West Nile Virus
  • Microbial Community Composition
  • Resident Bird
  • Neotropical Migrant