A Molecular Comparison of Plumage and Soil Bacteria Across Biogeographic, Ecological, and Taxonomic Scales
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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.
Keywords
Bacterial Community West Nile Virus Migratory Bird Terminal Restriction Fragment Length Polymorphism Bacterial CompositionNotes
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.
References
- 1.Atkins, MS, Teske, AP, Anderson, OR (2000) J Eukaryot Microbiol 47: 400PubMedCrossRefGoogle Scholar
- 2.Baas-Becking, LGM (1934) Geologie of Inleiding Tot de Milieu-kunde. WP Van Stokum, The Hague, The NetherlandsGoogle Scholar
- 3.Bray, JR, Curtis, JT (1957) An ordination of the upland forest communities of Southern Wisconsin. Ecol Monogr 27: 325–349CrossRefGoogle 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: 420–427CrossRefGoogle Scholar
- 5.Buckely, D, Schmidt, T (2001) The structure of microbial communities in soil and the lasting impact of cultivation. Microb Ecol 42: 11–21Google Scholar
- 6.Burtt, EH Jr (1999) Think small. Auk 116: 878–881Google Scholar
- 7.Burtt, EH Jr, Ichida, JM (2004) Gloger’s Rule, feather-degrading bacteria, and color variation among Song Sparrows. Condor 106: 681–686CrossRefGoogle Scholar
- 8.Burtt, EH Jr, Ichida, JM (1999) Occurrence of feather-degrading bacilli in the plumage of birds. Auk 116: 364–372Google 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 104–122Google Scholar
- 10.Cho, JC, Tiedje, JM (2000) Biogeography and degree of endemicity of fluorescent Pseudomonas strains in soil. Appl Environ Microbiol 66: 5448–5456PubMedCrossRefGoogle Scholar
- 11.Clarke, KR, Gorley, RN (2001) Primer v.5: User Manual/Tutorial. PRIMER-E, Plymouth Marine Laboratory, UKGoogle 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, OxfordGoogle 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: 675–685Google Scholar
- 14.De Deyn, GB, Van der Putten, WH (2005) Linking aboveground and belowground diversity. TREE 20: 625–633PubMedGoogle Scholar
- 15.DeLong, EF, Karl, DM (2005) Genomic perspectives in microbial diversity. Nature 437: 336–342PubMedCrossRefGoogle 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: 191–199PubMedCrossRefGoogle Scholar
- 17.Finlay, BJ (2002) Global dispersal of free-living microbial eukaryote species. Science 296: 1061–1063PubMedCrossRefGoogle Scholar
- 18.Finlay, BJ, Clarke, KJ (1999) Ubiquitous dispersal of microbial species. Nature 400: 828CrossRefGoogle 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: 246–253PubMedGoogle 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: 528–540PubMedCrossRefGoogle 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: 133–136CrossRefGoogle 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: 747–750PubMedCrossRefGoogle 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: 1608–1623CrossRefGoogle Scholar
- 24.Hawkins, BA (2001) Ecology’s oldest pattern? TREE 16: 470Google 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: 3425–3433PubMedCrossRefGoogle 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, DCGoogle Scholar
- 27.Horner-Devine, MC, Carney, K, Bohannan, BJM (2004) An ecological perspective on bacterial biodiversity. Proc R Soc Lond B 271: 113–122CrossRefGoogle Scholar
- 28.Johnson, ML, Speare, R (2005) Possible modes of dissemination of the amphibian chytrid Batrachochytrium dendrobatidis in the environment. Dis Aquat Org 65: 181–186PubMedGoogle 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: 550–560PubMedCrossRefGoogle Scholar
- 30.Lane, DJ (1991) 16S/23S rRNA Sequencing. Nucleic Acid Techniques in Bacterial Systematics. E. S. a. M. Goodfellow. Wiley, West Sussex, EnglandGoogle 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: 481–490PubMedCrossRefGoogle Scholar
- 32.Litchfield, CD, Gillevet, PM (2002) Microbial diversity and complexity in hypersaline environments: a preliminary assessment. J Ind Microbiol Biotech 28: 48–55Google 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: 1206PubMedCrossRefGoogle Scholar
- 34.Lucas, FS, Moureau, B, Jourdie, V, Heeb, P (2005) Brood size modifications affect plumage bacterial assemblages of European starlings. Mol Ecol 14: 639–646PubMedCrossRefGoogle 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: 282–290PubMedCrossRefGoogle Scholar
- 36.Madigan, MT, Martinko, JM, Parker, J (1996) Brock Biology of Microorganisms. Prentice-Hall, Upper Saddle River, NJGoogle 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: 393–402CrossRefGoogle 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: 57–74PubMedCrossRefGoogle Scholar
- 39.Mlot, C (2004) Microbial diversity unbound. BioScience 54: 1064–1068CrossRefGoogle Scholar
- 40.Moreira, D, Lopéz-García, P (2005) The molecular ecology of microbial eukaryotes unveils a hidden world. TREE 10: 31–38Google Scholar
- 41.Muza, M, Burtt, EH Jr, Ichida, JM (2000) Distribution of bacteria on feathers of some eastern North American birds. Wilson Bull 112: 432–435CrossRefGoogle Scholar
- 42.Nee, S (2004) More than meets the eye. Nature 429: 804–805PubMedCrossRefGoogle 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: 2249–2250PubMedCrossRefGoogle 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: 3622–3626PubMedGoogle Scholar
- 45.Ou, CY, Moore, JL, Schochetman, G (1991) Use of UV irradiation to reduce false positivity in polymerase chain reaction. BioTechniques 10: 442–446PubMedGoogle Scholar
- 46.Pérez-Tris, J, Bensch, S (2005) Dispersal increases local transmission of avian malarial parasites. Ecol Lett 8: 838–845CrossRefGoogle 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 24Google Scholar
- 48.Pyle, P (1997) Identification Guide to North American Birds, Part I: Columbidae to Ploceidae. Slate Creek Press, Bolinas, CAGoogle 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: 1–9CrossRefGoogle Scholar
- 50.Shannon, CE, Weaver, W (1949) The Mathematical Theory of Communication. University of Illinois Press, Urbana, ILGoogle Scholar
- 51.Shawkey, MD, Pillai, SR, Hill, GE (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J Avian Biol 34: 345–352CrossRefGoogle 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: 40–47PubMedCrossRefGoogle 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: 4373–4376CrossRefGoogle Scholar
- 54.SPSS statistical software package version 11.0. 2001. SPSS, Lead Technologies, IncGoogle Scholar
- 55.Suh, HJ, Lee, HK (2001) Characterization of keratinolytic serine protease from Bacillus subtilis KS-1. J Protein Chem 20: 165–169PubMedCrossRefGoogle 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: 4522–4529PubMedGoogle 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: 2259–2268PubMedCrossRefGoogle 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: 1353–1370PubMedGoogle Scholar
- 59.Whitaker, JM, Cristol, DA, Forsyth, MH (2005) Prevalence and genetic diversity of Bacillus licheniformis in avian plumage. J Field Ornithol 76: 264–270Google Scholar
- 60.Whitaker, RJ, Grogan, DW, Taylor, JT (2003) Geographic barriers isolate endemic populations of hyperthermophilic archaea. Science 310: 976–978CrossRefGoogle Scholar
- 61.Williams, CM, Richter, CS, Mackenzie, JM Jr, Shih, JCH (1990) Isolation, identification, and characterization of feather-degrading bacterium. Appl Environ Microbiol 56: 1509–1515PubMedGoogle Scholar
- 62.Willig, MR, Kaufman, DM, Stevens, RD (2003) Latitudinal gradients of biodiversity pattern, process, scale and synthesis. Annu Rev Ecol Evol Syst 34: 273–309CrossRefGoogle 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: 214–223PubMedCrossRefGoogle 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: 391–405PubMedCrossRefGoogle Scholar