Skip to main content
SpringerLink
Log in

A Molecular Comparison of Plumage and Soil Bacteria Across Biogeographic, Ecological, and Taxonomic Scales

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

We used molecular methods to determine the microbial community of soil and avian plumage across biogeographic, ecological, and taxonomic scales. A total of 17 soil and 116 feather samples were collected from five avian species across multiple habitat types within one Neotropical and one temperate locality. Hypotheses regarding patterns of microbial composition relative to acquisition and dispersal of plumage bacteria in the ecosystem were tested by comparing microbial communities within and between soil and plumage. Samples from the plumage of American Redstarts (Setophaga ruticilla) were collected across both habitat types and geographic scales for intraspecific comparisons. The microbial diversity in avian plumage was moderately diverse and was dominated by Pseudomonas species. Despite a highly significant individual bird effect on microbial composition of the plumage, we detected significant biogeographic and type of habitat effects. Pseudomonas species were more abundant on the temperate site when all avian species were included in the analysis, and Bacillus subtilis and Xanthomonas groups were more abundant on the Neotropical site for redstarts alone. However, 16S rDNA sequence libraries were not significantly different between Jamaican and Maryland redstarts. Biogeographic and habitat effects were significant and more pronounced for soil samples indicating lower dispersal of soil microbiota. We detected a significant difference between soil and plumage microbial communities suggesting that soil plays a small role in plumage bacterial acquisition. Our results suggest bacterial communities on the plumage of birds are dynamic and may change at different stages in a bird’s annual cycle.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Atkins, MS, Teske, AP, Anderson, OR (2000) J Eukaryot Microbiol 47: 400

    Article  PubMed  CAS  Google Scholar 

  2. Baas-Becking, LGM (1934) Geologie of Inleiding Tot de Milieu-kunde. WP Van Stokum, The Hague, The Netherlands

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

    Article  Google Scholar 

  4. Broughton, LC, Gross, KL (2000) Patterns of diversity in plant and soil microbial communities along a productivity gradient in a Michigan old-field. Oecologia 125: 420–427

    Article  Google Scholar 

  5. Buckely, D, Schmidt, T (2001) The structure of microbial communities in soil and the lasting impact of cultivation. Microb Ecol 42: 11–21

    Google Scholar 

  6. Burtt, EH Jr (1999) Think small. Auk 116: 878–881

    Google Scholar 

  7. Burtt, EH Jr, Ichida, JM (2004) Gloger’s Rule, feather-degrading bacteria, and color variation among Song Sparrows. Condor 106: 681–686

    Article  Google Scholar 

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

    Google Scholar 

  9. Burtt, EH Jr, Chow, W, Babbitt, GA (1991) Occurrence and demography of mites of tree swallow, house wren, and eastern bluebird nests. In: Loye, JE, Zuk, M (Eds.) Bird–Parasite Interactions: Ecology, Evolution, and Behaviour, Oxford University Press, Oxford, pp 104–122

    Google Scholar 

  10. Cho, JC, Tiedje, JM (2000) Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl Environ Microbiol 66: 5448–5456

    Article  PubMed  CAS  Google Scholar 

  11. Clarke, KR, Gorley, RN (2001) Primer v.5: User Manual/Tutorial. PRIMER-E, Plymouth Marine Laboratory, UK

    Google Scholar 

  12. Clayton, DH (1991) Coevolution of avian grooming and ectoparasite avoidance. In: Loye, JE, Zuk, M (Eds.) Bird–Parasite Interactions: Ecology, Evolution, and Behaviour, Oxford University Press, Oxford

    Google Scholar 

  13. Clayton, DH, Price, RD (1999) Taxonomy of New World Columbicola (Phthiraptera: Philopteridae) from the Columbiformes (Aves), with descriptions of five new species. Ann Entomol Soc Am 92: 675–685

    Google Scholar 

  14. De Deyn, GB, Van der Putten, WH (2005) Linking aboveground and belowground diversity. TREE 20: 625–633

    PubMed  Google Scholar 

  15. DeLong, EF, Karl, DM (2005) Genomic perspectives in microbial diversity. Nature 437: 336–342

    Article  PubMed  CAS  Google Scholar 

  16. Fall, S, Nazaret, S, Chotte, JL, Brauman, A (2004) Bacterial density and community structure associated with aggregate size fractions of soil-feeding termite mounds. Microb Ecol 48: 191–199

    Article  PubMed  CAS  Google Scholar 

  17. Finlay, BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296: 1061–1063

    Article  PubMed  CAS  Google Scholar 

  18. Finlay, BJ, Clarke, KJ (1999) Ubiquitous dispersal of microbial species. Nature 400: 828

    Article  CAS  Google Scholar 

  19. Gagnevin, L, Leach, JE, Pruvost, O (1997) Genomic variability of the Xanthonomas pathovar mangiferaeindicae, agent of mango bacterial black spot. Appl Environ Microbiol 63: 246–253

    PubMed  CAS  Google Scholar 

  20. Graham, JM, Kent, AD, Lauster, GH, Yannarell, AC, Graham, LE, Triplett, EW (2004) Seasonal dynamics of phytoplankton and planktonic protozoan communities in a northern temperate humic lake: diversity in a dinoflagellate dominated system. Microb Ecol 48: 528–540

    Article  PubMed  CAS  Google Scholar 

  21. Grant, A, Ogilvie, LA (2004) Name that microbe: rapid identification of taxa responsible for individual fragments in fingerprints of microbial community structure. Mol Ecol Notes 4: 133–136

    Article  CAS  Google Scholar 

  22. Green, JL, Holmes, AJ, Westoby, M, Oliver, I, Briscoe, D, Dangerfield, M, Gillings, M, Beattie, AJ (2004) Spatial scaling of microbial eukaryote diversity. Nature 432: 747–750

    Article  PubMed  CAS  Google Scholar 

  23. Hawkins, BA, Porter, EE, Diniz-Filho, F, Alexandre, J (2003) Productivity and history as predictors of the latitudinal diversity gradient of terrestrial birds. Ecology 84: 1608–1623

    Article  Google Scholar 

  24. Hawkins, BA (2001) Ecology’s oldest pattern? TREE 16: 470

    Google Scholar 

  25. Hewson, I, Fuhrman, JA (2004) Richness and diversity of bacterioplankton species along an estuarine gradient in Moreton Bay, Australia. Appl Environ Microbiol 70: 3425–3433

    Article  PubMed  CAS  Google Scholar 

  26. Holmes, RT (1994) Black-throated Blue Warbler (Dendroica caerulescens). In: Poole, A, Gill, F (Eds.) The Birds of North America, No. 87. The Academy of Natural Sciences, Philadelphia, The American Ornithologists Union, Washington, DC

  27. Horner-Devine, MC, Carney, K, Bohannan, BJM (2004) An ecological perspective on bacterial biodiversity. Proc R Soc Lond B 271: 113–122

    Article  Google Scholar 

  28. Johnson, ML, Speare, R (2005) Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Dis Aquat Org 65: 181–186

    PubMed  Google Scholar 

  29. Kent, AD, Jones, SE, Yannarell, AC, Graham, JM, Lauster, GH, Kratz, TK, Triplett, EW (2004) Annual patterns in bacterioplankton community variability in a humic lake. Microb Ecol 48: 550–560

    Article  PubMed  CAS  Google Scholar 

  30. Lane, DJ (1991) 16S/23S rRNA Sequencing. Nucleic Acid Techniques in Bacterial Systematics. E. S. a. M. Goodfellow. Wiley, West Sussex, England

    Google Scholar 

  31. Lazzi, C, Rossetti, L, Zago, M, Neviani, E, Giraffa, G (2004) Evaluation of bacterial communities belonging to natural whey starters for Grana Padano cheese by length heterogeneity-PCR. J Appl Microbiol 96: 481–490

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  33. Liu, J, Xiao, H, Lei, F, Zhu, Q, Qin, K, Zhang, X-W, Zhang, X-L, Zhao, D, Wang, G, Feng, Y, Ma, J, Liu, W, Wang, J, Gao, GF (2005) Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309: 1206

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  35. 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

    Article  PubMed  CAS  Google Scholar 

  36. Madigan, MT, Martinko, JM, Parker, J (1996) Brock Biology of Microorganisms. Prentice-Hall, Upper Saddle River, NJ

    Google Scholar 

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

    Article  Google Scholar 

  38. 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 Methods 54: 57–74

    Article  PubMed  CAS  Google Scholar 

  39. Mlot, C (2004) Microbial diversity unbound. BioScience 54: 1064–1068

    Article  Google Scholar 

  40. Moreira, D, Lopéz-García, P (2005) The molecular ecology of microbial eukaryotes unveils a hidden world. TREE 10: 31–38

    Google Scholar 

  41. Muza, M, Burtt, EH Jr, Ichida, JM (2000) Distribution of bacteria on feathers of some eastern North American birds. Wilson Bull 112: 432–435

    Article  Google Scholar 

  42. Nee, S (2004) More than meets the eye. Nature 429: 804–805

    Article  PubMed  CAS  Google Scholar 

  43. Norris, DR, Marra, PP, Montgomerie, R, Kyser, TK, Ratcliffe, LM (2004) Reproductive effort, molting latitude, and feather color in a migratory songbird. Science 306: 2249–2250

    Article  PubMed  CAS  Google Scholar 

  44. Nusslein, K, Tiedje, JM (1999) Soil bacterial community shift correlated with change from forest to pasture vegetation in a tropical soil. Appl Environ Microbiol 65: 3622–3626

    PubMed  CAS  Google Scholar 

  45. Ou, CY, Moore, JL, Schochetman, G (1991) Use of UV irradiation to reduce false positivity in polymerase chain reaction. BioTechniques 10: 442–446

    PubMed  CAS  Google Scholar 

  46. Pérez-Tris, J, Bensch, S (2005) Dispersal increases local transmission of avian malarial parasites. Ecol Lett 8: 838–845

    Article  Google Scholar 

  47. Price, RD, Hellenthal, RA, Palma, RL, Johnson, KP, Clayton, DH (2003) The chewing lice: world checklist and biological overview. Ill Nat Hist Surv Spec Publ 24

  48. Pyle, P (1997) Identification Guide to North American Birds, Part I: Columbidae to Ploceidae. Slate Creek Press, Bolinas, CA

    Google Scholar 

  49. Schloss, PD, Hay, AG, Wilson, DB, Walker, LP (2003) Tracking temporal changes of bacterial community fingerprints during the initial stages of composting. FEMS Microbiol Ecol 46: 1–9

    Article  CAS  Google Scholar 

  50. Shannon, CE, Weaver, W (1949) The Mathematical Theory of Communication. University of Illinois Press, Urbana, IL

    Google Scholar 

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

    Article  Google Scholar 

  52. 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

    Article  PubMed  Google Scholar 

  53. Singleton, DR, Furlong, MA, Rathbun, SL, Whitman, WB (2001) Quantitative comparisons of 16S rDNA sequence libraries from environmental samples. Appl Environ Microbiol 67: 4373–4376

    Article  Google Scholar 

  54. SPSS statistical software package version 11.0. 2001. SPSS, Lead Technologies, Inc

  55. Suh, HJ, Lee, HK (2001) Characterization of keratinolytic serine protease from Bacillus subtilis KS-1. J Protein Chem 20: 165–169

    Article  PubMed  CAS  Google Scholar 

  56. Suzuki, M, Rappe, MS, Giovannoni, SJ (1998) Kinetic bias in estimates of coastal picoplankton community structure obtained by measurements of small-subunit rRNA gene PCR amplicon length heterogeneity. Appl Environ Microbiol 64: 4522–4529

    PubMed  CAS  Google Scholar 

  57. Tiirola, MA, Suvilampi, JE, Kulomaa, MS, Rintala, JA (2003) Microbial diversity in a thermophilic aerobic biofilm process: analysis by length heterogeneity PCR (LH-PCR). Water Res 37: 2259–2268

    Article  PubMed  CAS  Google Scholar 

  58. Ward, DM, Ferris, MJ, Nold, SC, Bateson, MM (1998) A natural view of microbial biodiversity within hot spring cyanobacterial mat communities. Microbiol Mol Biol Rev 62: 1353–1370

    PubMed  CAS  Google Scholar 

  59. Whitaker, JM, Cristol, DA, Forsyth, MH (2005) Prevalence and genetic diversity of Bacillus licheniformis in avian plumage. J Field Ornithol 76: 264–270

    Google Scholar 

  60. Whitaker, RJ, Grogan, DW, Taylor, JT (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 310: 976–978

    Article  Google Scholar 

  61. Williams, CM, Richter, CS, Mackenzie, JM Jr, Shih, JCH (1990) Isolation, identification, and characterization of feather-degrading bacterium. Appl Environ Microbiol 56: 1509–1515

    PubMed  CAS  Google Scholar 

  62. Willig, MR, Kaufman, DM, Stevens, RD (2003) Latitudinal gradients of biodiversity pattern, process, scale and synthesis. Annu Rev Ecol Evol Syst 34: 273–309

    Article  Google Scholar 

  63. Yannarell, AC, Triplett, EW (2004) Within- and between-lake variability in the composition of bacterioplankton communities: investigations using multiple spatial scales. Appl Environ Microbiol 70: 214–223

    Article  PubMed  CAS  Google Scholar 

  64. Yannarell, AC, Kent, AD, Lauster, GH, Kratz, TK, Triplett, EW (2003) Temporal patterns in bacterial communities in three temperate lakes of different trophic status. Microb Ecol 46: 391–405

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This research was supported, in part, by funding from the Loeb fund and a Postdoctoral 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. All protocols were approved by the Institutional Animal Care and Use Committee of the Smithsonian Environmental Research Center. We would additionally like to thank 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 and useful suggestions in the laboratory analyses.

Author information

Author notes

  1. Isabelle-Anne Bisson

    Present address: Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, 08544, USA

  2. Peter P. Marra

    Present address: Smithsonian Migratory Bird Center, National Zoological Park, 3001 Connecticut Ave, Washington, DC, 20008, USA

Authors and Affiliations

  1. Smithsonian Environmental Research Center, 647 Contees Wharf Road, Edgewater, MD, 21037, USA

    Isabelle-Anne Bisson & Peter P. Marra

  2. Department of Zoology, Ohio Wesleyan University, Delaware, OH, 43015, USA

    Edward H. Burtt Jr.

  3. Department of Environmental Sciences and Policy, George Mason University, Manassas, VA, 22030, USA

    Masoumeh Sikaroodi & Patrick M. Gillevet

Authors
  1. Isabelle-Anne Bisson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Peter P. Marra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edward H. Burtt Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Masoumeh Sikaroodi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Patrick M. Gillevet
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isabelle-Anne Bisson.

Appendix 1

Appendix 1

Table 4 Identification of cloned bacterial sequences and LH-PCR fingerprinting (LH operational taxonomic unit (OTU) length in base pairs) results from representative sequences sampled from the feathers of one American Redstart captured in Jamaica (JA39) and one captured in Maryland (MD34)
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bisson, IA., Marra, P.P., Burtt, E.H. et al. A Molecular Comparison of Plumage and Soil Bacteria Across Biogeographic, Ecological, and Taxonomic Scales. Microb Ecol 54, 65–81 (2007). https://doi.org/10.1007/s00248-006-9173-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9173-2

Keywords

Search

Navigation