Journal of Comparative Physiology B

, Volume 182, Issue 5, pp 591–602 | Cite as

Diversity and function of the avian gut microbiota

  • Kevin D. KohlEmail author


The intestinal microbiota have now been shown to largely affect host health through various functional roles in terms of nutrition, immunity, and other physiological systems. However, the majority of these studies have been carried out in mammalian hosts, which differ in their physiological traits from other taxa. For example, birds possess several unique life history traits, such as hatching from eggs, which may alter the interactions with and transmission of intestinal microbes compared to most mammals. This review covers the diversity of microbial taxa hosted by birds. It also discusses how avian microbial communities strongly influence nutrition, immune function, and processing of toxins in avian hosts, in manners similar to and different from mammalian systems. Finally, areas demanding further research are identified, along with descriptions of existing techniques that could be employed to answer these questions.


Avian hosts Intestinal microbes Symbiosis 



I would like to thank M. Denise Dearing, Hannah Carey, and the two anonymous reviewers for comments that helped to improve this manuscript. This work was supported by a National Science Foundation Graduate Research Fellowship.


  1. An D, Dong X, Dong Z (2005) Prokaryote diversity in the rumen of yak (Bos grunniens) and Jinnan cattle (Bos taurus) estimated by 16S rDNA homology analyses. Anaerobe 11:207–215PubMedCrossRefGoogle Scholar
  2. Baker BJ, Tyson GW, Webb RI, Flanagan J, Hugenholtz P, Allen EE, Banfield JF (2006) Lineages of acidophilic archaea revealed by community genomic analysis. Science 22:1933–1935CrossRefGoogle Scholar
  3. Banks JC, Cary SC, Hogg ID (2009) The phylogeography of Adelie penguin faecal flora. Environ Microbiol 11:577–588PubMedCrossRefGoogle Scholar
  4. Barnes EM (1972) The avian intestinal flora with particular reference to the possible ecological significance of the cecal anaerobic bacteria. Am J Clin Nutr 25:1475–1479PubMedGoogle Scholar
  5. Boissé L, Mouihate A, Ellis S, Pittman QJ (2004) Long-term alterations in neuroimmune responses after neonatal exposure to lipopolysaccharide. J Neurosci 24:4928–4934PubMedCrossRefGoogle Scholar
  6. Bolton W (1965) Digestion in the crop of the fowl. Br Poult Sci 6:97–102PubMedCrossRefGoogle Scholar
  7. Boot R, Koopman JP, Kruijt BC, Lammers RM, Kennis HM, Lankhorst A, Mullink JWMA, Stadhouders AM, de Boer D, Welling GW, Hectors MPC (1985) The ‘normalization’ of germ-free rabbits with host-specific caecal flora. Lab Anim 19:344–352PubMedCrossRefGoogle Scholar
  8. Brisbin JT, Gong J, Sharif S (2008) Interactions between commensal bacteria and the gut-associated immune system of the chicken. Anim Health Res Rev 9:101–110PubMedCrossRefGoogle Scholar
  9. Byrne CM, Clyne M, Bourke B (2007) Campylobacter jejuni adhere to and invade chicken intestinal epithelial cells in vitro. Microbiol 153:561–569CrossRefGoogle Scholar
  10. Caviedes-Vidal E, McWhorter TJ, Lavin SR, Chediack JG, Tracy CR, Karasov WH (2007) The digestive adaptation of flying vertebrates: high intestinal paracellular absorption compensates for smaller guts. Proc Natl Acad Sci 104:19132–19137PubMedCrossRefGoogle Scholar
  11. Clarke A, Rothery P (2008) Scaling of body temperature in mammals and birds. Funct Ecol 22:58–67Google Scholar
  12. Claus SP, Ellero SL, Berger B, Krause L, Bruttin A, Molina J, Paris A, Want EJ, de Waziers I, Cloarec O, Richards SE, Wang Y, Dumas M-E, Ross A, Rezzi S, Kochhar S, Van Bladeren P, Lindon JC, Holmes E, Nicholson JK (2011) Colonization-induced host-gut microbial metabolic interaction. MBio 2:e00271–e00310PubMedCrossRefGoogle Scholar
  13. Comstedt P, Jakobsson T, Bergström S (2011) Global ecology and epidemiology of Borrelia garinii spirochetes. Infect Ecol Epidemiol 1:9545Google Scholar
  14. Cook MI, Beissinger SR, Toranzos GA, Arendt WJ (2005) Incubation reduces microbial growth on eggshells and the opportunity for trans-shell infection. Ecol Lett 8:532–537PubMedCrossRefGoogle Scholar
  15. Cooper RG (2004) Ostrich (Struthio camelus) chick and grower nutrition. Anim Sci J 75:487–490CrossRefGoogle Scholar
  16. Costello EK, Gordon JI, Secor SM, Knight R (2010) Postprandial remodeling of the gut microbiota in Burmese pythons. ISME J 11:1375–1385CrossRefGoogle Scholar
  17. Craven SE, Stern NJ, Line E, Bailey JS, Cox NA, Fedorka-Cray P (2000) Determination of the incidence of Salmonella spp., Campylobacter jejuni, and Clostridium perfringens in wild birds near broiler chicken houses by sampling intestinal droppings. Avian Dis 44:715–720PubMedCrossRefGoogle Scholar
  18. Dadd RH, Krieger DL (1968) Dietary requirements of the aphid Myzus persicae. J Insect Phsiol 14:741–764CrossRefGoogle Scholar
  19. Dearing MD, Foley WJ, McLean S (2005) The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Ann Rev Ecol Evol Syst 36:169–185CrossRefGoogle Scholar
  20. DeGolier TF, Mahoney SA, Duke GE (1999) Relationships of avian cecal lengths to food habits, taxonomic position, and intestinal lengths. Condor 101:622–634CrossRefGoogle Scholar
  21. Dehority BA (1997) Foregut fermentation. In: Mackie RI, White BA (eds) Gastrointestinal microbiology. Chapman and Hall, New YorkGoogle Scholar
  22. Deplancke B, Gaskins HR (2001) Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am J Clin Nutr 73:1131S–1141SPubMedGoogle Scholar
  23. Dominguez-Bello MG, Costello EK, Contreras M, Magris M, Hidalgo G, Fierer N, Knight R (2010) Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc Natl Acad Sci 107:11971–11975PubMedCrossRefGoogle Scholar
  24. Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 8:125PubMedCrossRefGoogle Scholar
  25. Ekino S, Suginohara K, Urano T, Fujii H, Matsuno K, Kotani M (1985) The bursa of Fabricius: a trapping site for environmental antigens. Immunology 55:405–410PubMedGoogle Scholar
  26. Ellström P, Jourdain E, Gunnarsson O, Waldenström J, Olsen B (2009) The “human influenza receptor” Neu5Acα2,6Gal is expressed among different taxa of wild birds. Arch Virol 154:1533–1537PubMedCrossRefGoogle Scholar
  27. Fisher MM, Triplett EW (1999) Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its application to freshwater bacterial communities. Appl Environ Microbiol 65:4630–4636PubMedGoogle Scholar
  28. Ford DJ, Coates ME (1971) Absorption of glucose and vitamins of the B complex by germ-free and conventional chicks. Proc Nutr Soc 30:10A–11APubMedGoogle Scholar
  29. Friedman A (2008) Oral tolerance in birds and mammals: digestive tract development determines the strategy. J Appl Poult Res 17:168–173CrossRefGoogle Scholar
  30. Garcia-Amado MA, Michelangeli F, Gueneau P, Perez ME, Dominguez-Bello MG (2007) Bacterial detoxification of saponins in the crop of the avian foregut fermenter Opisthocomus hoazin. J Anim Feed Sci 16:82–85Google Scholar
  31. Gaukler SM, Linz GM, Sherwood JS, Dyer NW, Bleier WJ, Wannemuehler YM, Nolan LK, Logue CM (2009) Escherichia coli, Salmonella, and Mycobacterium avium subsp. paratuberculosis in wild European Starlings at a Kansas cattle feedlot. Avian Dis 53:544–551PubMedCrossRefGoogle Scholar
  32. Godoy-Vitorino F, Ley RE, Gao Z, Pei Z, Ortiz-Zuazaga H, Pericchi LR, Garcia-Amado MA, Michelangeli F, Blaser MJ, Gordon JI, Dominguez-Bello MG (2008) Bacterial community in the crop of the hoatzin, a neotropical folivorous flying bird. Appl Environ Microbiol 74:5905–5912PubMedCrossRefGoogle Scholar
  33. Godoy-Vitorino F, Goldfarb KC, Brodie EL, Garcia-Amado MA, Michelangeli F, Dominguez-Bello MG (2010) Developmental microbial ecology of the crop of the folivorous hoatzin. ISME J 4:611–620PubMedCrossRefGoogle Scholar
  34. Grajal A, Strahl SD, Parra R, Dominguez MG, Neher A (1989) Foregut fermentation in the hoatzin, a neotropical leaf-eating bird. Science 245:1236–1238PubMedCrossRefGoogle Scholar
  35. Head IM, Saunders JR, Pickup RW (1998) Microbial evolution, diversity, and ecology: a decade of ribosomal RNA analysis of uncultivated microorganisms. Microb Ecol 35:1–21PubMedCrossRefGoogle Scholar
  36. Helgeland L, Dissen E, Dai KZ, Midtvedt T, Brandtzaeg P, Vaage JT (2004) Microbial colonization induces oligoclonal expansions of intraepithelial CD8 T cells in the gut. Eur J Immunol 34:3389–3400PubMedCrossRefGoogle Scholar
  37. Hellgren O, Sheldon BC, Buckling A (2010) In vitro tests of natural allelic variation of innate immune genes (avian β-defensins) reveal functional differences in microbial inhibition. J Evol Biol 23:2726–2730PubMedCrossRefGoogle Scholar
  38. Hooper LV, Gordon JI (2001) Glycans as legislators of host–microbial interactions: spanning the spectrum from symbiosis to pathogenicity. Glycobiology 11:1R–10RPubMedCrossRefGoogle Scholar
  39. Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI (2001) Molecular analysis of commensal host–microbial relationships in the intestine. Science 291:881–884PubMedCrossRefGoogle Scholar
  40. Hosokawa T, Koga R, Kikuchi Y, Meng X-Y, Fukatsu T (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci 107:769–774PubMedCrossRefGoogle Scholar
  41. Hubálek Z, Halouzka J, Heroldová M (1998) Growth temperature ranges of Borrelia burgdorferi sensu lato strains. J Med Microbiol 47:929–932PubMedCrossRefGoogle Scholar
  42. Hur HG, Lay JO Jr, Beger RD, Freeman JP, Rafii F (2000) Isolation of human intestinal bacteria metabolizing the natural isoflavone glycosides daidzin and genistin. Arch Microbiol 174:422–428PubMedCrossRefGoogle Scholar
  43. Johansson MEV, Ambort D, Pelaseyed T, Schütte A, Gustafsson JK, Ermund A, Subramani DB, Holmén-Larsson JM, Thomsson KA, Bergström JH, van der Post S, Rodriguez-Piñeiro AM, Sjövall H, Bäckström M, Hansson GC (2011) Composition and functional role of the mucus layers in the intestine. Cell Mol Life Sci 68:3635–3641PubMedCrossRefGoogle Scholar
  44. Jozefiak D, Rutkowski A, Martin SA (2004) Carbohydrate fermentation in the avian ceca: a review. Anim Feed Sci Technol 113:1–15CrossRefGoogle Scholar
  45. Karasov WH, Martinez del Rio C (2007) Physiological ecology: how animals process energy, nutrients, and toxins. Princeton University Press, PrincetonGoogle Scholar
  46. Kibe R, Sakamoto M, Hayashi H, Yokota H, Benno Y (2004) Maturation of the murine cecal microbiota as revealed by terminal restriction fragment length polymorphism and 16S rRNA gene clone libraries. FEMS Microbiol Lett 235:139–146PubMedCrossRefGoogle Scholar
  47. Kimura N, Yoshikane M, Kobayashi A (1986) Microflora of the bursa of Fabricius of chickens. Poult Sci 65:1801–1807PubMedCrossRefGoogle Scholar
  48. Klomp JE, Murphy MT, Bartos Smith S, McKay JE, Ferrera I, Reysenbach A-L (2008) Cloacal microbial communities of female spotted towhees Pipilo maculatus: microgeographic variation and individual sources of variability. J Avian Biol 39:530–538CrossRefGoogle Scholar
  49. Kyle PD, Kyle GZ (1993) An evaluation of the role of microbial flora in the salivary transfer technique for hand-rearing Chimney Swifts. Wildlife Rehabil 8:65–71Google Scholar
  50. Lahti JM, Chen CL, Tjoelker LW, Pickel JM, Schat KA, Calnek BW, Thompson CB, Cooper MD (1991) Two distinct alpha beta T-cell lineages can be distinguished by the differential usage of T-cell receptor V beta gene segments. Proc Natl Acad Sci 88:10956–10960PubMedCrossRefGoogle Scholar
  51. Lee KP, Carlson LM, Woodcock JB, Ramachandra N, Schultz TL, Davis TA, Lowe JB, Thompson CB, Larsen RD (1996) Molecular cloning and characterization of CFT1, a developmentally regulated avian α(1,3)-fucosyltransferase gene. J Biol Chem 271:32960–32967PubMedCrossRefGoogle Scholar
  52. Leser TD, Mølbak L (2009) Better living through microbial action: the benefits of the mammalian gastrointestinal microbiota on the host. Environ Microbiol 11:2194–2206PubMedCrossRefGoogle Scholar
  53. Ley RE, Hamady M, Lozupone C, Turnbaugh PJ, Ramey RR, Bircher JS, Schlegel ML, Tucker TA, Schrenzel MD, Knight R, Gordon JI (2008a) Evolution of mammals and their gut microbes. Science 320:1647–1651PubMedCrossRefGoogle Scholar
  54. Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008b) Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Rev Microbiol 6:776–788CrossRefGoogle Scholar
  55. Love OP, Williams TD (2008) Plasticity in the adrenalcortical response of a free-living vertebrate: the role of pre- and post-natal developmental stress. Horm Behav 54:496–505PubMedCrossRefGoogle Scholar
  56. Lu J, Idris U, Harmon B, Hofacre C, Maurer JJ, Lee MD (2003) Diversity and succession of the intestinal bacterial community of the maturing broiler chicken. Appl Environ Microbiol 69:6816–6824PubMedCrossRefGoogle Scholar
  57. Lu J, Santo Domingo JW, Lamendella R, Edge TA, Hill S (2008) Phylogenetic diversity and molecular detection of bacteria in gull feces. Appl Environ Microbiol 74:3969–3976PubMedCrossRefGoogle Scholar
  58. Lu J, Santo Domingo JW, Hill S, Edge TA (2009) Microbial diversity and host-specific sequences of Canada goose feces. Appl Environ Microbiol 75:5919–5926PubMedCrossRefGoogle Scholar
  59. Lucas FS, Heeb P (2005) Environmental factors shape cloacal bacterial assemblages in great tit Parus major and blue tit P. caerulus nestlings. J Avian Biol 36:510–516CrossRefGoogle Scholar
  60. Lynn DJ, Higgs R, Gaines S, Tierney J, James T, Lloyd AT, Fares MA, Mulcahy G, O’Farrelly C (2004) Bioinformatic discovery and initial characterisation of nine novel antimicrobial peptide genes in the chicken. Immunogenetics 56:170–177PubMedCrossRefGoogle Scholar
  61. Macpherson AJ, Harris NL (2004) Interactions between commensal intestinal bacteria and the immune system. Nature Rev Immunol 4:478–485CrossRefGoogle Scholar
  62. Matsui H, Kato Y, Chikaraishi T, Moritani M, Ban-Tokuda T, Wakita M (2010) Microbial diversity in ostrich ceca as revealed by 16S ribosomal RNA gene clone library and detection of novel Fibrobacter species. Anaerobe 16:83–93PubMedCrossRefGoogle Scholar
  63. Maul JD, Gandhi JP, Farris JL (2005) Community-level physiological profiles of cloacal microbes in songbirds (Order: Passeriformes): variation due to host species, host diet, and habitat. Microb Ecol 50:19–28PubMedCrossRefGoogle Scholar
  64. McCue MD, Sivan O, McWilliams SR, Pinshow B (2010) Tracking the oxidative kinetics of carbohydrates, amino acids, and fatty acids in the house sparrow using exhaled 13CO2. J Exp Biol 213:782–789PubMedCrossRefGoogle Scholar
  65. Mead GC (1989) Microbes of the avian cecum: types present and substrates utilized. J Exp Biol 3(Suppl):48–54Google Scholar
  66. Mills TK, Lombardo MP, Thorpe PA (1999) Microbial colonization of the cloacae of nestling tree swallows. Auk 116:947–956Google Scholar
  67. Mittler TE (1971) Dietary amino acid requirement of the aphid Myzus persicae affected by antibiotic uptake. J Nutr 101:1023–1028PubMedGoogle Scholar
  68. Mohr PW, Krawiec S (1980) Temperature characteristics and Arrhenius plots for nominal psychrophiles, mesophiles and thermophiles. Microbiology 121:311–317CrossRefGoogle Scholar
  69. Moreno J, Briones V, Merino S, Ballesteros C, Sanz JJ, Tomás G (2003) Beneficial effects of cloacal bacteria on growth and fledging size in nestling pied flycatchers (Ficedula hypoleuca) in Spain. Auk 120:784–790CrossRefGoogle Scholar
  70. Muegge BD, Kuczynski J, Knights D, Clemente JC, González A, Fontana L, Henrissat B, Knight R, Gordon JI (2011) Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332:970–974Google Scholar
  71. Mwangi WN, Beal RK, Powers C, Wu X, Humphrey T, Watson M, Bailey M, Friedman A, Smith AL (2010) Regional and global changes in TCRαβ T cell repertoires in the gut are dependent upon the complexity of the enteric microflora. Dev Comp Immunol 34:406–417PubMedCrossRefGoogle Scholar
  72. Nelson KE, Weinstock GM, Highlander SK, Worley KC, Creasy HH, Wortman JR, Rusch DB, Mitreva MES, Chinwalla AT, Feldgarden M, Gevers D, Haas BJ, Madupu R, Ward DV, Birren BW (2010) A catalog of reference genomes from the human microbiome. Science 328:994–999PubMedCrossRefGoogle Scholar
  73. O’Hara AM, Shanahan F (2006) The gut flora as a forgotten organ. EMBO Rep 7:688–693PubMedCrossRefGoogle Scholar
  74. Owen RL, Pierce NF, Apple RT, Cray WC Jr (1986) M cell transport of Vibrio cholerae from the intestinal lumen into Peyer’s Patches: a mechanism for antigen sampling and for microbial transepithelial migration. J Infect Dis 153:1108–1118PubMedCrossRefGoogle Scholar
  75. Pacheco MA, Garcia-Amado MA, Bosque C, Dominguez-Bello MG (2004) Bacteria in the crop of the seed-eating green-rumped parrotlet. Condor 106:139–143CrossRefGoogle Scholar
  76. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO (2007) Development of the human infant intestinal microbiota. PLoS Biol 5:1556–1573CrossRefGoogle Scholar
  77. Peralta-Sánchez JM, Møller AP, Martin-Platero AM, Soler JJ (2010) Number and colour composition of nest lining feathers predict eggshell bacterial community in barn swallow nests: an experimental study. Funct Ecol 24:426–433CrossRefGoogle Scholar
  78. Pinchasov Y, Noy Y (1994) Early postnatal amylolysis in the gastrointestinal tract of turkey poults Meleagris gallopavo. Comp Biochem Physiol A 107:221–226CrossRefGoogle Scholar
  79. Pitala N, Gustafsson L, Sendecka J, Brommer JE (2007) Nestling immune response to phytohaemagglutinin is not heritable in collared flycatchers. Biol Lett 3:418–421PubMedCrossRefGoogle Scholar
  80. Preest MR, Folk DG, Beuchat CA (2003) Decomposition of nitrogenous compounds by intestinal bacteria in hummingbirds. Auk 4:1091–1101CrossRefGoogle Scholar
  81. Probert CSJ, Williams AM, Stepankova R, Tlaskalova-Hogenova H, Phillips A, Bland PW (2007) The effect of weaning on the clonality of αβ T-cell receptor T cells in the intestine of GF and SPF mice. Dev Comp Immunol 31:606–617PubMedCrossRefGoogle Scholar
  82. Qu A, Brulc JM, Wilson MK, Law BF, Theoret JR, Joens LA, Konkel ME, Angly F, Dinsdale EA, Edwards RA, Nelson KE, White BA (2008) Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome. PLoS One 3:e2945PubMedCrossRefGoogle Scholar
  83. Radajewski S, Ineson P, Parekh NR, Murrell JC (2000) Stable-isotope probing as a tool in microbial ecology. Nature 403:646–649PubMedCrossRefGoogle Scholar
  84. Rappe MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394PubMedCrossRefGoogle Scholar
  85. Ratcliffe MJH (2006) Antibodies, immunoglobulin genes and the bursa of Fabricius in chicken B cell development. Dev Comp Immunol 30:101–118PubMedCrossRefGoogle Scholar
  86. Ruiz-De-Castañeda R, Vela AI, Lobato E, Briones V, Moreno J (2011) Bacterial loads on eggshells of the pied flycatcher: environmental and maternal factors. Condor 113:200–208CrossRefGoogle Scholar
  87. Ruiz-Rodríguez M, Lucas FS, Heeb P, Soler JJ (2009a) Differences in intestinal microbiota between avian brood parasites and their hosts. Biol J Linn Soc 96:406–414CrossRefGoogle Scholar
  88. Ruiz-Rodríguez M, Soler JJ, Lucas FS, Heeb P, Palacios MJ, Martín-Gálvez D, de Neve L, Pérez-Contreras T, Martínez JG, Soler M (2009b) Bacterial diversity at the cloaca relates to an immune response in magpie Pica pica and to body condition of great spotted cuckoo Clamator glandarius nestlings. J Avian Biol 40:42–48CrossRefGoogle Scholar
  89. Saengkerdsub S, Anderson RC, Wilkinson HH, Kim W, Nisbet DJ, Ricke SC (2007) Identification and quantification of methanogenic archaea in adult chicken ceca. Appl Environ Microbiol 73:353–356PubMedCrossRefGoogle Scholar
  90. Salminen S, Gibson GR, McCartney AL, Isolauri E (2004) Influence of mode of delivery on gut microbiota composition in 7 year old children. Gut 53:1388–1389PubMedCrossRefGoogle Scholar
  91. Scupham AJ (2007) Succession in the intestinal microbiota of preadolescent turkeys. FEMS Microbiol Ecol 60:136–147PubMedCrossRefGoogle Scholar
  92. Scupham AJ, Patton TG, Bent E, Bayles DO (2008) Comparison of the cecal microbiota of domestic and wild turkeys. Microb Ecol 56:322–331PubMedCrossRefGoogle Scholar
  93. Shanks N, Windle RJ, Perks PA, Harbuz MS, Jessop DS, Ingram CD, Lightman SL (2000) Early-life exposure to endotoxin alters hypothalamic–pituitary–adrenal function and predisposition to inflammation. Proc Natl Acad Sci 97:5645–5650PubMedCrossRefGoogle Scholar
  94. Shetty S, Sridhar KR, Shenoy KB, Hegde SN (1990) Observations on bacteria associated with pigeon crop. Folia Microbiol 35:240–244CrossRefGoogle Scholar
  95. Slominski BA, Campbell LD, Stanger NE (1988) Extent of hydrolysis in the intestinal tract and potential absorption of intact glucosinolates in laying hens. J Sci Food Agric 42:305–314CrossRefGoogle Scholar
  96. Smalia K, Oros-Sichler M, Milling A, Heuer H, Baumgarte S, Becker R, Neuber G, Kropf S, Ulrich A, Tebbe CC (2007) Bacterial diversity of soils assessed by DGGE, T-RFLP and SSCP fingerprints of PCR-amplified 16S rRNA gene fragments: do the different methods provide similar results? J Microbiol Methods 69:470–479Google Scholar
  97. 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 3:93–100Google Scholar
  98. Stevens CE, Hume ID (2004) Comparative physiology of the vertebrate digestive system. Cambridge University Press, CambridgeGoogle Scholar
  99. Tennant B, Reina-Guerra M, Harrold D (1971) Influence of microorganisms on intestinal absorption. Ann NY Acad Sci 176:262–272CrossRefGoogle Scholar
  100. Turnbaugh PJ, Gordon JI (2008) An invitation to the marriage of metagenomics and metabolomics. Cell 134:708–713PubMedCrossRefGoogle Scholar
  101. van der Wielen PWJJ, Keuzenkamp DA, Lipman JA, van Knapen F, Biesterveld S (2002) Spatial and temporal variation of the intestinal bacterial community in commercially raised broiler chickens during growth. Microb Ecol 44:286–293PubMedCrossRefGoogle Scholar
  102. Verma M, Madhu M, Marrota C, Lakshmi CV, Davidson EA (1994) Mucin coding sequences are remarkably conserved. Cancer Biochem Biophys 14:41–51PubMedGoogle Scholar
  103. Vispo C, Karasov WH (1997) The interactions of avian gut microbes and their host: an elusive symbiosis. In: Mackie RI, White BA (eds) Gastrointestinal microbiology. Chapman and Hall, New YorkGoogle Scholar
  104. White J, Mirleau P, Danchin E, Mulard H, Hatch SA, Heeb P, Wagner RH (2010) Sexually transmitted bacteria affect female cloacal assemblages in a wild bird. Ecol Lett 13:1515–1524PubMedCrossRefGoogle Scholar
  105. Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, Peters EC, Siuzdak G (2009) Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci 106:3698–3703PubMedCrossRefGoogle Scholar
  106. Wilmes P, Bond PL (2006) Metaproteomics: studying functional gene expression in microbial ecosystems. Trends Microbiol 14:92–97PubMedCrossRefGoogle Scholar
  107. Wright AG, Northwood KS, Obispo NE (2009) Rumen-like methanogens identified from the crop of the folivorous South American bird, the hoatzin (Opisthocomus hoazin). ISME J 3:1120–1126PubMedCrossRefGoogle Scholar
  108. Xenoulis PG, Gray PL, Brightsmith D, Palculict B, Hoppes S, Steiner JM, Tizard I, Suchodolski JS (2010) Molecular characterization of the cloacal microbiota of wild and captive parrots. Vet Microbiol 146:320–325PubMedCrossRefGoogle Scholar
  109. Yamano H, Koike S, Kobayashi Y, Hata H (2008) Phylogenetic analysis of hindgut microbiota in Hokkaido native horses compared to light horses. Anim Sci J 79:234–242Google Scholar
  110. Young JC, Zhou T, Yu H, Zhu H, Gong J (2007) Degradation of trichothecene mycotoxins by chicken intestinal microbes. Food Chem Toxicol 45:136–143PubMedCrossRefGoogle Scholar
  111. Zhu XY, Zhong T, Pandya Y, Joerger RD (2002) 16S rRNA-based analysis of microbiota from the cecum of broiler chickens. Appl Environ Microbiol 68:124–137PubMedCrossRefGoogle Scholar

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© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Department of BiologyUniversity of UtahSalt Lake CityUSA

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