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Review

Dominant factors shaping the gut microbiota of wild birds

, ORCID Icon & ORCID Icon
Pages 255-268 | Received 08 Jul 2021, Accepted 12 Aug 2022, Published online: 29 Aug 2022

References

  • Ambrosini, R., Corti, M., Franzetti, A., Caprioli, M., Rubolini, D., Motta, V. M., and Costanzo, A. (2019). Cloacal microbiomes and ecology of individual barn swallows. FEMS Microbiology and Ecology 95, fiz061. doi:10.1093/femsec/fiz061.
  • Anderson, J. F., Johnson, R. C., Magnarelli, L. A., and Hyde, F. W. (1986). Involvement of birds in the epidemiology of the Lyme disease agent Borrelia burgdorferi. Infection and Immunity 51, 394–396. doi:10.1128/iai.51.2.394-396.1986.
  • Aukema, J. E., and Martinez Del Rio, C. (2002). Mistletoes as parasites and seed-dispersing birds as disease vectors: Current understanding, challenges, and opportunities. In ‘Seed Dispersal and Frugivory: Ecology, Evolution, and Conservation Levey, D. J., Silva, W. R., Galetti, M.’ pp. 99–110. (CABI International: Wallingford, UK.)
  • Banks, J. C., Cary, S. C., and Hogg, I. D. (2009). The phylogeography of Adelie penguin faecal flora. Environmental Microbiology 11, 577–588. doi:10.1111/j.1462-2920.2008.01816.x.
  • Barbosa, A., Balagué, V., Valera, F., Martínez, A., Benzal, J., Motas, M., and Diaz, J. I. (2016). Age-related differences in the gastrointestinal microbiota of chinstrap penguins (Pygoscelis Antarctica). PloS one 11, e0153215. doi:10.1371/journal.pone.0153215
  • Becker, A. A., Harrison, S. W., Whitehouse-Tedd, G., Budd, J. A., and Whitehouse-Tedd, K. M. (2020). Integrating gut bacterial diversity and captive husbandry to optimize vulture conservation. Frontiers in Microbiology 11, 1025. doi:10.3389/fmicb.2020.01025.
  • Bedford, A., and Gong, J. (2018). Implications of butyrate and its derivatives for gut health and animal production. Animal Nutrition 4(2), 151–159. doi:10.1016/j.aninu.2017.08.010.
  • Ben-Yosef, M., Zaada, D. S. Y., Dudaniec, R. Y., Pasternak, Z., Jurkevitch, E., Smith, R. J., and Causton, C. E. (2017). Host-specific associations affect the microbiome of Philornis downsi, an introduced parasite to the Galápagos Islands. Molecular Ecology 26(18), 4644–4656. doi:10.1111/mec.14219.
  • Berasategui, A., Salem, H., Paetz, C., Santoro, M., Gershenzon, J., Kaltenpoth, M., and Schmidt, A. (2017). Gut microbiota of the pine weevil degrades conifer diterpenes and increases insect fitness. Molecular Ecology 26, 4099–4110. doi:10.1111/mec.14186.
  • Berlow, M., Phillips, J. N., and Derryberry, E. P. (2020). Effects of urbanization and landscape on gut microbiomes in white-crowned sparrows. Microbial Ecology 81, 253–266. doi:10.1007/s00248-020-01569-8.
  • Bo, T. B., Zhang, X. Y., Kohl, K. D., Wen, J., Tian, S. J., and Wang, D. H. (2020). Coprophagy prevention alters microbiome, metabolism, neurochemistry, and cognitive behavior in a small mammal. The ISME Journal 14, 2625–2645. doi:10.1038/s41396-020-0711-6.
  • Bodawatta, K. H., Freiberga, I., Puzejova, K., Sam, K., Poulsen, M., and Jønsson, K. A. (2021). Flexibility and resilience of great tit (Parus major) gut microbiomes to changing diets. Animal Microbiome 3, 1–14. doi:10.1186/s42523-021-00076-6.
  • Bodawatta, K. H., Hird, S. M., Grond, K., Poulsen, M., and Jønsson, K. A. (2021a). Avian gut microbiomes taking flight. Trends in Microbiology 30, 268–280.
  • Bodawatta, K. H., Koane, B., Maiah, G., Sam, K., Poulsen, M., and Jønsson, K. A. (2021b). Species-specific but not phylosymbiotic gut microbiomes of New Guinean passerine birds are shaped by diet and flight-associated gut modifications. Proceedings of the Royal Society B 288, 20210446. doi:10.1098/rspb.2021.0446.
  • Bodawatta, K. H., Sam, K., Jønsson, K. A., and Poulsen, M. (2018). Comparative analyses of the digestive tract microbiota of New Guinean passerine birds. Frontiers in Microbiology 9, 1830. doi:10.3389/fmicb.2018.01830.
  • Brandl, H. B., Van Dongen, W. F., Darolová, A., Krištofík, J., Majtan, J., Hoi, H., and Shawkey, M. (2014). Composition of bacterial assemblages in different components of reed warbler nests and a possible role of egg incubation in pathogen regulation. PloS one 9, e114861. doi:10.1371/journal.pone.0114861.
  • Brooks, A. W., Kohl, K. D., Brucker, R. M., van Opstal, E. J., Bordenstein, S. R., and Relman, D. (2016). Phylosymbiosis: Relationships and functional effects of microbial communities across host evolutionary history. PLoS Biology 14, e2000225. doi:10.1371/journal.pbio.2000225.
  • Bukhari, S. M., Alghamdi, H. A., Rehman, K. U., Andleeb, S. S. A., Khalid, N., and Khalid, N. (2021). Metagenomics analysis of the fecal microbiota in ring-necked pheasants (Phasianus colchicus) and green pheasants (Phasianus versicolor) using next generation sequencing. Saudi Journal of Biological Sciences 29, 1781–1788. doi:10.1016/j.sjbs.2021.10.050.
  • Butchart, S. H., Lowe, S., Martin, R. W., Symes, A., Westrip, J. R., and Wheatley, H. (2018). Which bird species have gone extinct? A novel quantitative classification approach. Biological Conservation 227, 9–18. doi:10.1016/j.biocon.2018.08.014.
  • Cao, J., Hu, Y., Liu, F., Wang, Y., Bi, Y., Lv, N., and Li, J. (2020). Metagenomic analysis reveals the microbiome and resistome in migratory birds. Microbiome 8, 1–18. doi:10.1186/s40168-019-0781-8
  • Capunitan, D. C., Johnson, O., Terrill, R. S., and Hird, S. M. (2020). Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea. Molecular Ecology 29, 829–847. doi:10.1111/mec.15354.
  • Carthey, A. J., Blumstein, D. T., Gallagher, R. V., Tetu, S. G., Gillings, M. R., and Bennett, A. (2020). Conserving the holobiont. Functional Ecology 34, 764–776. doi:10.1111/1365-2435.13504.
  • Caviedes-Vidal, E., McWhorter, T. J., Lavin, S. R., Chediack, J. G., Tracy, C. R., and Karasov, W. H. (2007). The digestive adaptation of flying vertebrates: High intestinal paracellular absorption compensates for smaller guts. Proceedings of the National Academy of Sciences 104, 19132–19137. doi:10.1073/pnas.0703159104.
  • Chassard, C., Delmas, E., Robert, C., and Bernalier-Donadille, A. (2010). The cellulose-degrading microbial community of the human gut varies according to the presence or absence of methanogens. FEMS Microbiology Ecology 74, 205–213. doi:10.1111/j.1574-6941.2010.00941.x.
  • Chen, C. Y., Chen, C. K., Chen, Y. Y., Fang, A., Shaw, G. T. W., Hung, C. M., and Wang, D. (2020). Maternal gut microbes shape the early-life assembly of gut microbiota in passerine chicks via nests. Microbiome 8, 1–13. doi:10.1186/s40168-020-00896-9.
  • Cho, H., and Lee, W. Y. (2020). Interspecific comparison of the fecal microbiota structure in three Arctic migratory bird species. Ecology and Evolution 10, 5582–5594. doi:10.1002/ece3.6299.
  • Cockerham, S., Lee, B., Orben, R. A., Suryan, R. M., Torres, L. G., Warzybok, P., and Bradley, R. (2019). Microbial ecology of the western gull (Larus occidentalis). Microbial Ecology 78, 665–676. doi:10.1007/s00248-019-01352-4
  • Daft, J. G., Ptacek, T., Kumar, R., Morrow, C., and Lorenz, R. G. (2015). Cross-fostering immediately after birth induces a permanent microbiota shift that is shaped by the nursing mother. Microbiome 3, 1–10. doi:10.1186/s40168-015-0080-y.
  • Davidson, G. L., Wiley, N., Cooke, A. C., Johnson, C. N., Fouhy, F., Reichert, M. S., and de la Hera, I. (2020). Diet induces parallel changes to the gut microbiota and problem-solving performance in a wild bird. Scientific Reports 10, 1–13. doi:10.1038/s41598-020-77256-y
  • Dewar, M. L., Arnould, J. P., Dann, P., Trathan, P., Groscolas, R., and Smith, S. (2013). Interspecific variations in the gastrointestinal microbiota in penguins. Microbiology Open 2, 195–204. doi:10.1002/mbo3.66.
  • Dewar, M. L., Arnould, J. P., Krause, L., Dann, P., and Smith, S. C. (2014). Interspecific variations in the faecal microbiota of procellariiform seabirds. FEMS Microbiology Ecology 89, 47–55. doi:10.1111/1574-6941.12332.
  • Ding, J., Liao, N., Zheng, Y., Yang, L., Zhou, H., Xu, K., and Han, C. (2020). The composition and function of pigeon milk microbiota transmitted from parent pigeons to squabs. Frontiers in Microbiology 11, 1789. doi:10.3389/fmicb.2020.01789
  • Dutch, R., Tell, L. A., Bandivadekar, R., and Vannette, R. L. (2021). Microbiome composition of Anna’s hummingbirds differs among regions of the gastrointestinal tract. Journal of Avian Biology 3, e02856.
  • Escallón, C., Belden, L. K., and Moore, I. T. (2019). The cloacal microbiome changes with the breeding season in a wild bird. Integrative Organismal Biology 1, oby009. doi:10.1093/iob/oby009.
  • Fleischer, R., Risely, A., Hoeck, P. E., Keller, L. F., and Sommer, S. (2020). Mechanisms governing avian phylosymbiosis: Genetic dissimilarity based on neutral and MHC regions exhibits little relationship with gut microbiome distributions of Galápagos mockingbirds. Ecology and Evolution 10, 13345–13354. doi:10.1002/ece3.6934.
  • Frese, S. A., Parker, K., Calvert, C. C., and Mills, D. A. (2015). Diet shapes the gut microbiome of pigs during nursing and weaning. Microbiome 3, 1–10. doi:10.1186/s40168-015-0091-8.
  • Fu, R., Xiang, X., Dong, Y., Cheng, L., and Zhou, L. (2020). Comparing the intestinal bacterial communies of sympatric wintering Hooded Crane (Grus monacha) and domestic goose (Anser anser domesticus). Avian Research 11, 1–9. doi:10.1186/s40657-020-00195-9.
  • Gadau, A., Meli’Sa, S. C., Mayek, R., Giraudeau, M., McGraw, K. J., Whisner, C. M., and Kondrat-Smith, C. (2019). A comparison of the nutritional physiology and gut microbiome of urban and rural house sparrows (Passer domesticus). Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 237, 110332. doi:10.1016/j.cbpb.2019.110332
  • García-Amado, M. A., Shin, H., Sanz, V., Lentino, M., Martínez, L. M., Contreras, M., and Michelangeli, F. (2018). Comparison of gizzard and intestinal microbiota of wild neotropical birds. PLoS One 13, e0194857. doi:10.1371/journal.pone.0194857
  • Gilbert, J. A., Blaser, M. J., Caporaso, J. G., Jansson, J. K., Lynch, S. V., and Knight, R. (2018). Current understanding of the human microbiome. Nature Medicine 24, 392–400. doi:10.1038/nm.4517.
  • Gilbert, J. A., Jansson, J. K., and Knight, R. (2014). The Earth Microbiome project: Successes and aspirations. BMC Biology 12, 1–4. doi:10.1186/s12915-014-0069-1.
  • Gillingham, M. A. F., Béchet, A., Cézilly, F., Wilhelm, K., Rendón-Martos, M., Borghesi, F., and Nissardi, S. (2019). Offspring microbiomes differ across breeding sites in a panmictic species. Frontiers in Microbiology 10, 35. doi:10.3389/fmicb.2019.00035.
  • Godoy-Vitorino, F., Goldfarb, K. C., Karaoz, U., Leal, S., Garcia-Amado, M. A., Hugenholtz, P., and Tringe, S. G. (2012). Comparative analyses of foregut and hindgut bacterial communities in hoatzins and cows. The ISME Journal 6, 531–541. doi:10.1038/ismej.2011.131
  • Godoy-Vitorino, F., Ley, R. E., Gao, Z., Pei, Z., Ortiz-Zuazaga, H., Pericchi, L. R., and Garcia-Amado, M. A. (2008). Bacterial community in the crop of the hoatzin, a neotropical folivorous flying bird. Applied and Environmental Microbiology 74, 5905–5912. doi:10.1128/AEM.00574-08
  • Góngora, E., Elliott, K. H., and Whyte, L. (2021). Gut microbiome is affected by inter-sexual and inter-seasonal variation in diet for thick-billed murres (Uria lomvia). Scientific Reports 11, 1–12. doi:10.1038/s41598-020-80557-x.
  • Goossens, E., Boonyarittichaikij, R., Dekeukeleire, D., Van Praet, S., Bonte, D., Verheyen, K., and Verbrugghe, E. (2021). Exploring the faecal microbiome of the Eurasian nuthatch (Sitta europaea). Archives of Microbiology 203, 2119–2127.
  • Grant, P. R. (1999). ‘Ecology and Evolution of Darwin’s Finches.’ (Princeton University Press: New Jersey.)
  • Grond, K., Ryu, H., Baker, A. J., Santo Domingo, J. W., and Buehler, D. M. (2014). Gastro-intestinal microbiota of two migratory shorebird species during spring migration staging in Delaware Bay, USA. Journal of Ornithology 155, 969–977. doi:10.1007/s10336-014-1083-3.
  • Grond, K., Sandercock, B. K., Jumpponen, A., and Zeglin, L. H. (2018). The avian gut microbiota: Community, physiology and function in wild birds. Journal of Avian Biology 49, e01788. doi:10.1111/jav.01788.
  • Grond, K., Santo Domingo, J. W., Lanctot, R. B., Jumpponen, A., Bentzen, R. L., Boldenow, M. L., and Brown, S. C. (2019). Composition and drivers of gut microbial communities in Arctic-breeding shorebirds. Frontiers in Microbiology 10, 2258. doi:10.3389/fmicb.2019.02258
  • Groussin, M., Mazel, F., Sanders, J. G., Smillie, C. S., Lavergne, S., Thuiller, W., and Alm, E. J. (2017). Unraveling the processes shaping mammalian gut microbiomes over evolutionary time. Nature Communications 8, 1–12. doi:10.1038/ncomms14319.
  • Gunasekaran, M., Lalzar, M., Sharaby, Y., Izhaki, I., and Halpern, M. (2020). The effect of toxic pyridine alkaloid secondary metabolites on the sunbird gut microbiome. Biofilms and Microbiomes 6, 53. doi:10.1038/s41522-020-00161-9.
  • Hellström, S., Kiviniemi, K., Autio, T., and Korkeala, H. (2008). Listeria monocytogenes is common in wild birds in Helsinki region and genotypes are frequently similar with those found along the food chain. Journal of Applied Microbiology 104, 883–888. doi:10.1111/j.1365-2672.2007.03604.x.
  • Hemarajata, P., and Versalovic, J. (2013). Effects of probiotics on gut microbiota: Mechanisms of intestinal immunomodulation and neuromodulation. Therapeutic Advances in Gastroenterology 6, 39–51. doi:10.1177/1756283X12459294.
  • Herder, E. A., Spence, A. R., Tingley, M. W., and Hird, S. M. (2021). Elevation correlates with significant changes in relative abundance in hummingbird fecal microbiota, but composition changes little. Frontiers in Ecology and Evolution 8. doi:10.3389/fevo.2020.597756.
  • Hird, S. M. (2017). Evolutionary biology needs wild microbiomes. Frontiers in Microbiology 8, 725. doi:10.3389/fmicb.2017.00725.
  • Hird, S. M., Carstens, B. C., Cardiff, S. W., Dittmann, D. L., and Brumfield, R. T. (2014). Sampling locality is more detectable than taxonomy or ecology in the gut microbiota of the brood-parasitic Brown-headed Cowbird (Molothrus ater). PeerJ 2, e321. doi:10.7717/peerj.321.
  • Hird, S. M., Sánchez, C., Carstens, B. C., and Brumfield, R. T. (2015). Comparative gut microbiota of 59 neotropical bird species. Frontiers in Microbiology 6, 1403. doi:10.3389/fmicb.2015.01403.
  • Hooper, L. V., Littman, D. R., and Macpherson, A. J. (2012). Interactions between the microbiota and the immune system. Science 336, 1268–1273. doi:10.1126/science.1223490.
  • Immerseel, F. V., Buck, J. D., Pasmans, F., Huyghebaert, G., Haesebrouck, F., and Ducatelle, R. (2004). Clostridium perfringens in poultry: An emerging threat for animal and public health. Avian Pathology 33, 537–549. doi:10.1080/03079450400013162.
  • Ippolito, M. M., Denny, J. E., Langelier, C., Sears, C. L., and Schmidt, N. W. (2018). Malaria and the microbiome: A systematic review. Clinical Infectious Diseases 67, 1831–1839. doi:10.1093/cid/ciy374.
  • Jiang, H. Y., Ma, J. E., Li, J., Zhang, X. J., Li, L. M., He, N., and Liu, H.-Y. (2017). Diets alter the gut microbiome of crocodile lizards. Frontiers in Microbiology 8, 2073. doi:10.3389/fmicb.2017.02073
  • Knutie, S. A. (2018). Relationships among introduced parasites, host defenses, and gut microbiota of Galapagos birds. Ecosphere 9, e02286. doi:10.1002/ecs2.2286.
  • Knutie, S. A., Chaves, J. A., and Gotanda, K. M. (2019). Human activity can influence the gut microbiota of Darwin’s finches in the Galapagos Islands. Molecular Ecology 28, 2441–2450. doi:10.1111/mec.15088.
  • Knutie, S. A., and Elderd, B. (2020). Food supplementation affects gut microbiota and immunological resistance to parasites in a wild bird species. Journal of Applied Ecology 57, 536–547. doi:10.1111/1365-2664.13567.
  • Kogut, M. H. (2013). The gut microbiota and host innate immunity: Regulators of host metabolism and metabolic diseases in poultry? Journal of Applied Poultry Research 22, 637–646. doi:10.3382/japr.2013-00741.
  • Kohl, K. D. (2012). Diversity and function of the avian gut microbiota. Journal of Comparative Physiology B 182, 591–602. doi:10.1007/s00360-012-0645-z.
  • Kohl, K. D., Brun, A., Bordenstein, S. R., Caviedes‐Vidal, E., and Karasov, W. H. (2018). Gut microbes limit growth in house sparrow nestlings (Passer domesticus) but not through limitations in digestive capacity. Integrative Zoology 13, 139–151. doi:10.1111/1749-4877.12289.
  • Kosiewicz, M. M., Zirnheld, A. L., and Alard, P. (2011). Gut microbiota, immunity, and disease: A complex relationship. Frontiers in Microbiology 2, 180. doi:10.3389/fmicb.2011.00180.
  • Kropáčková, L., Těšický, M., Albrecht, T., Kubovčiak, J., Čížková, D., Tomášek, O., and Martin, J.-F. (2017). Codiversification of gastrointestinal microbiota and phylogeny in passerines is not explained by ecological divergence. Molecular Ecology 26, 5292–5304. doi:10.1111/mec.14144
  • Kuhl, H., Frankl-Vilches, C., Bakker, A., Mayr, G., Nikolaus, G., Boerno, S. T., and Klages, S. (2020). An unbiased molecular approach using 3ʹUTRs resolves the avian family-level tree of life. Molecular Biology and Evolution 38, 108–127. doi:10.1093/molbev/msaa191.
  • Lee, C. Y., Peralta-Sánchez, J. M., Martínez-Bueno, M., Møller, A. P., Rabelo-Ruiz, M., Zamora-Muñoz, C., and Soler, J. J. (2020). The gut microbiota of brood parasite and host nestlings reared within the same environment: Disentangling genetic and environmental effects. The ISME Journal 14, 2691–2702. doi:10.1038/s41396-020-0719-y.
  • Lewis, W. B., Moore, F. R., and Wang, S. (2016). Characterization of the gut microbiota of migratory passerines during stopover along the northern coast of the Gulf of Mexico. Journal of Avian Biology 47, 659–668. doi:10.1111/jav.00954.
  • Li, C., Liu, Y., Gong, M., Zheng, C., Zhang, C., Li, H., and Wen, W. (2021). Diet-induced microbiome shifts of sympatric overwintering birds. Applied Microbiology and Biotechnology 105, 5993–6005. doi:10.1007/s00253-021-11448-y
  • Liao, F., Gu, W., Li, D., Liang, J., Fu, X., Xu, W., and Duan, R. (2019). Characteristics of microbial communities and intestinal pathogenic bacteria for migrated Larus ridibundus in southwest China. Microbiology Open 8, e00693. doi:10.1002/mbo3.693
  • Liu, H., Chen, Z., Gao, G., Sun, C., Li, Y., and Zhu, Y. (2019). Characterization and comparison of gut microbiomes in nine species of parrots in captivity. Symbiosis 78, 241–250. doi:10.1007/s13199-019-00613-7.
  • Liu, G., Gong, Z., and Li, Q. (2020a). Variations in gut bacterial communities between lesser white‐fronted geese wintering at Caizi and Shengjin lakes in China. Microbiology Open 9, e1037. doi:10.1002/mbo3.1037.
  • Liu, G., Meng, D., Gong, M., Li, H., Wen, W., Wang, Y., and Zhou, J. (2020b). Effects of sex and diet on gut microbiota of farmland-dependent wintering birds. Frontiers in Microbiology 11, 2813. doi:10.3389/fmicb.2020.587873.
  • Loo, W. T., Dudaniec, R. Y., Kleindorfer, S., Cavanaugh, C. M., and Duperron, S. (2019b). An inter-island comparison of Darwin’s finches reveals the impact of habitat, host phylogeny, and island on the gut microbiome. PLoS One 14, e0226432. doi:10.1371/journal.pone.0226432.
  • Loo, W. T., García-Loor, J., Dudaniec, R. Y., Kleindorfer, S., and Cavanaugh, C. M. (2019a). Host phylogeny, diet, and habitat differentiate the gut microbiomes of Darwin’s finches on Santa Cruz Island. Scientific Reports 9, 1–12. doi:10.1038/s41598-019-54869-6.
  • Lucas, F. S., and Heeb, P. (2005). Environmental factors shape cloacal bacterial assemblages in great tit Parus major and blue tit P. caeruleus nestlings. Journal of Avian Biology 36, 510–516. doi:10.1111/j.0908-8857.2005.03479.x.
  • Lyte, J. M., Keane, J., Eckenberger, J., Anthony, N., Shrestha, S., Marasini, D., and Daniels, K. M. (2021). Japanese quail (Coturnix japonica) as a novel model to study the relationship between the avian microbiome and microbial endocrinology-based host-microbe interactions. Microbiome 9, 1–24. doi:10.1186/s40168-020-00962-2.
  • Mateos-Hernández, L., Risco-Castillo, V., Torres-Maravilla, E., Bermúdez-Humarán, L. G., Alberdi, P., Hodžić, A., and Hernández-Jarguin, A. (2020). Gut microbiota abrogates anti-α-Gal IgA response in lungs and protects against experimental Aspergillus infection in poultry. Vaccines 8, 285. doi:10.3390/vaccines8020285
  • Mendoza, M. L. Z., Roggenbuck, M., Vargas, K. M., Hansen, L. H., Brunak, S., Gilbert, M. T. P., and Sicheritz-Pontén, T. (2018). Protective role of the vulture facial skin and gut microbiomes aid adaptation to scavenging. Acta Veterinaria Scandinavica 60, 1–19. doi:10.1186/s13028-017-0355-3.
  • Michel, A. J., Ward, L. M., Goffredi, S. K., Dawson, K. S., Baldassarre, D. T., Brenner, A., and Gotanda, K. M. (2018). The gut of the finch: Uniqueness of the gut microbiome of the Galápagos vampire finch. Microbiome 6, 167. doi:10.1186/s40168-018-0555-8
  • Mirón, L., Mira, A., Rocha-Ramírez, V., Belda-Ferre, P., Cabrera-Rubio, R., Folch-Mallol, J., and Cardénas-Vázquez, R. (2014). Gut bacterial diversity of the house sparrow (Passer domesticus) inferred by 16S rRNA sequence analysis. Metagenomics 3, 1–11. doi:10.4303/mg/235853.
  • Moeller, A. H., Suzuki, T. A., Lin, D., Lacey, E. A., Wasser, S. K., and Nachman, M. W. (2017). Dispersal limitation promotes the diversification of the mammalian gut microbiota. Proceedings of the National Academy of Sciences 114, 13768–13773. doi:10.1073/pnas.1700122114.
  • Muegge, B. D., Kuczynski, J., Knights, D., Clemente, J. C., González, A., Fontana, L., and Henrissat, B. (2011). Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970–974. doi:10.1126/science.1198719
  • Murray, M. H., Lankau, E. W., Kidd, A. D., Welch, C. N., Ellison, T., Adams, H. C., and Lipp, E. K. (2020). Gut microbiome shifts with urbanization and potentially facilitates a zoonotic pathogen in a wading bird. PLoS One 15, e0220926. doi:10.1371/journal.pone.0220926.
  • Noguera, J. C., Aira, M., Pérez-Losada, M., Domínguez, J., and Velando, A. (2018). Glucocorticoids modulate gastrointestinal microbiome in a wild bird. Royal Society Open Science 5, 171743. doi:10.1098/rsos.171743.
  • Oliveira, B. C., Murray, M., Tseng, F., and Widmer, G. (2020). The fecal microbiota of wild and captive raptors. Animal Microbiome 2, 1–9. doi:10.1186/s42523-020-00035-7.
  • Pan, D., and Yu, Z. (2014). Intestinal microbiome of poultry and its interaction with host and diet. Gut Microbes 5, 108–119. doi:10.4161/gmic.26945.
  • Parois, S., Calandreau, L., Kraimi, N., Gabriel, I., and Leterrier, C. (2017). The influence of a probiotic supplementation on memory in quail suggests a role of gut microbiota on cognitive abilities in birds. Behavioural Brain Research 331, 47–53. doi:10.1016/j.bbr.2017.05.022.
  • Pekarsky, S., Corl, A., Turjeman, S., Kamath, P. L., Getz, W. M., Bowie, R. C., and Markin, Y. (2021). Drivers of change and stability in the gut microbiota of an omnivorous avian migrant exposed to artificial food supplementation. Molecular Ecology 30, 4723–4739. doi:10.1111/mec.16079
  • Pérez-Cobas, A. E., Maiques, E., Angelova, A., Carrasco, P., Moya, A., and Latorre, A. (2015). Diet shapes the gut microbiota of the omnivorous cockroach Blattella germanica. FEMS Microbiology Ecology 91, fiv022. doi:10.1093/femsec/fiv022.
  • Petrosino, J. F., Highlander, S., Luna, R. A., Gibbs, R. A., and Versalovic, J. (2009). Metagenomic pyrosequencing and microbial identification. Clinical Chemistry 55, 856–866. doi:10.1373/clinchem.2008.107565.
  • Phillips, J. N., Berlow, M., and Derryberry, E. P. (2018). The effects of landscape urbanization on the gut microbiome: An exploration into the gut of urban and rural white-crowned sparrows. Frontiers in Ecology and Evolution 6, 1–10. doi:10.3389/fevo.2018.00148.
  • Ran, J., Wan, Q. H., Fang, S. G., and Ishaq, S. L. (2021). Gut microbiota of endangered crested ibis: Establishment, diversity, and association with reproductive output. PloS One 16, e0250075. doi:10.1371/journal.pone.0250075.
  • Reed, K. D., Meece, J. K., Henkel, J. S., and Shukla, S. K. (2003). Birds, migration and emerging zoonoses: West Nile virus, Lyme disease, influenza A and enteropathogens. Clinical Medicine and Research 1, 5–12. doi:10.3121/cmr.1.1.5.
  • Risely, A., Waite, D. W., Ujvari, B., Hoye, B. J., Klaassen, M., and Wilson, K. (2018). Active migration is associated with specific and consistent changes to gut microbiota in Calidris shorebirds. Journal of Animal Ecology 87, 428–437. doi:10.1111/1365-2656.12784.
  • Rivero, A., and Gandon, S. (2018). Evolutionary ecology of avian malaria: From past to present. Trends in Parasitology 34, 712–726. doi:10.1016/j.pt.2018.06.002.
  • Roggenbuck, M., Schnell, I. B., Blom, N., Bælum, J., Bertelsen, M. F., Sicheritz-Pontén, T., and Sørensen, S. J. (2014). The microbiome of New World vultures. Nature Communications 5, 1–8. doi:10.1038/ncomms6498
  • Roughgarden, J., Gilbert, S. F., Rosenberg, E., Zilber-Rosenberg, I., and Lloyd, E. A. (2018). Holobionts as units of selection and a model of their population dynamics and evolution. Biological Theory 13, 44–65. doi:10.1007/s13752-017-0287-1.
  • Ruiz-Rodriguez, M., Lucas, F. S., Heeb, P., and Soler, J. J. (2009). Differences in intestinal microbiota between avian brood parasites and their hosts. Biological Journal of the Linnean Society 96, 406–414. doi:10.1111/j.1095-8312.2008.01127.x.
  • Ruiz-Rodríguez, M., Martín-Vivaldi, M., Martínez-Bueno, M., and Soler, J. J. (2018). Gut microbiota of great spotted cuckoo nestlings is a mixture of those of their foster magpie siblings and of cuckoo adults. Genes 9, 381. doi:10.3390/genes9080381.
  • Ryu, H., Grond, K., Verheijen, B., Elk, M., Buehler, D. M., and Santo Domingo, J. W. (2014). Intestinal microbiota and species diversity of campylobacter and helicobacter spp. in migrating shorebirds in Delaware Bay. Applied and Environmental Microbiology 80, 1838–1847. doi:10.1128/AEM.03793-13.
  • San Juan, P. A., Hendershot, J. N., Daily, G. C., and Fukami, T. (2020). Land-use change has host- specific influences on avian gut microbiomes. The ISME Journal 14, 318–321. doi:10.1038/s41396-019-0535-4.
  • Santos, S. S., Pardal, S., Proença, D. N., Lopes, R. J., Ramos, J. A., Mendes, L., and Morais, P. V. (2012). Diversity of cloacal microbial community in migratory shorebirds that use the Tagus estuary as stopover habitat and their potential to harbor and disperse pathogenic microorganisms. FEMS Microbiology Ecology 82, 63–74. doi:10.1111/j.1574-6941.2012.01407.x.
  • Scheelings, T. F., Moore, R. J., Van, T. T. H., Klaassen, M., and Reina, R. D. (2020). Microbial symbiosis and coevolution of an entire clade of ancient vertebrates: The gut microbiota of sea turtles and its relationship to their phylogenetic history. Animal Microbiome 2, 1–12. doi:10.1186/s42523-020-00034-8.
  • Schmiedová, L., Kreisinger, J., Požgayová, M., Honza, M., Martin, J. F., and Procházka, P. (2020). Gut microbiota in a host–brood parasite system: Insights from common cuckoos raised by two warbler species. FEMS Microbiology Ecology 96, fiaa143. doi:10.1093/femsec/fiaa143.
  • Sekercioglu, C. H. (2006). Increasing awareness of avian ecological function. Trends in Ecology and Evolution 21, 464–471. doi:10.1016/j.tree.2006.05.007.
  • Shang, W., Li, S., Zhang, L., Wu, H., and Jiang, Y. (2020). The composition of gut microbiota community structure of Jankowski’s bunting (Emberiza jankowskii). Current Microbiology 77, 3731–3737. doi:10.1007/s00284-020-02048-6.
  • Sjölund, M., Bonnedahl, J., Hernandez, J., Bengtsson, S., Cederbrant, G., Pinhassi, J., and Kahlmeter, G. (2008). Dissemination of multidrug-resistant bacteria into the Arctic. Emerging Infectious Diseases 14, 70. doi:10.3201/eid1401.070704
  • Slevin, M. C., Houtz, J. L., Bradshaw, D. J., and Anderson, R. C. (2020). Evidence supporting the microbiota–gut–brain axis in a songbird. Biology Letters 16, 20200430. doi:10.1098/rsbl.2020.0430.
  • Soler, J. J., Martín-Vivaldi, M., Peralta-Sánchez, J. M., and Ruiz-Rodríguez, M. (2010). Antibiotic-producing bacteria as a possible defence of birds against pathogenic microorganisms. The Open Ornithology Journal 3, 93–100. doi:10.2174/1874453201003010093.
  • Song, S. J., Sanders, J. G., Delsuc, F., Metcalf, J., Amato, K., Taylor, M. W., and Mazel, F. (2020). Comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats. mBio 11(1), , e02901–02919. doi:10.1128/mBio.02901-19.
  • Songer, J. G. (2010). Clostridia as agents of zoonotic disease. Veterinary Microbiology 140, 399–404. doi:10.1016/j.vetmic.2009.07.003.
  • Sottas, C., Schmiedová, L., Kreisinger, J., Albrecht, T., Reif, J., Osiejuk, T. S., and Reifová, R. (2021). Gut microbiota in two recently diverged passerine species: Evaluating the effects of species identity, habitat use and geographic distance. BMC Ecology and Evolution 21, 1–14. doi:10.1186/s12862-021-01773-1.
  • Stanley, D., Hughes, R. J., and Moore, R. J. (2014). Microbiota of the chicken gastrointestinal tract: Influence on health, productivity and disease. Applied Microbiology and Biotechnology 98, 4301–4310. doi:10.1007/s00253-014-5646-2.
  • Teyssier, A., Lens, L., Matthysen, E., and White, J. (2018b). Dynamics of gut microbiota diversity during the early development of an avian host: Evidence from a cross-foster experiment. Frontiers in Microbiology 9, 1524. doi:10.3389/fmicb.2018.01524.
  • Teyssier, A., Matthysen, E., Hudin, N. S., de Neve, L., White, J., and Lens, L. (2020). Diet contributes to urban-induced alterations in gut microbiota: Experimental evidence from a wild passerine. Proceedings of the Royal Society B 287, 20192182. doi:10.1098/rspb.2019.2182.
  • Teyssier, A., Rouffaer, L. O., Saleh Hudin, N., Strubbe, D., Matthysen, E., Lens, L., and White, J. (2018a). Inside the guts of the city: Urban-induced alterations of the gut microbiota in a wild passerine. Science of the Total Environment 612, 1276–1286. doi:10.1016/j.scitotenv.2017.09.035.
  • Trevelline, B. K., MacLeod, K. J., Knutie, S. A., Langkilde, T., and Kohl, K. D. (2018). In ovo microbial communities: A potential mechanism for the initial acquisition of gut microbiota among oviparous birds and lizards. Biology Letters 14, 20180225. doi:10.1098/rsbl.2018.0225.
  • Trevelline, B. K., Sosa, J., Hartup, B. K., and Kohl, K. D. (2020). A bird’s-eye view of phylosymbiosis: Weak signatures of phylosymbiosis among all 15 species of cranes. Proceedings of the Royal Society B 287, 20192988. doi:10.1098/rspb.2019.2988.
  • Turnbaugh, P. J., Ley, R. E., Hamady, M., Fraser-Liggett, C. M., Knight, R., and Gordon, J. I. (2007). The human microbiome project. Nature 449, 804–810. doi:10.1038/nature06244.
  • Van Dongen, W. F., White, J., Brandl, H. B., Moodley, Y., Merkling, T., Leclaire, S., Blanchard, P. (2013). Age-related differences in the cloacal microbiota of a wild bird species. BMC Ecology 13, 1–12. doi:10.1186/1472-6785-13-11
  • Videvall, E., Song, S. J., Bensch, H. M., Strandh, M., Engelbrecht, A., Serfontein, N., and Hellgren, O. (2019). Major shifts in gut microbiota during development and its relationship to growth in ostriches. Molecular Ecology 28, 2653–2667. doi:10.1111/mec.15087.
  • Videvall, E., Song, S. J., Bensch, H. M., Strandh, M., Engelbrecht, A., Serfontein, N., and Hellgren, O. (2020). Early-life gut dysbiosis linked to juvenile mortality in ostriches. Microbiome 8, 1–13. doi:10.1186/s40168-020-00925-7
  • Vrancken, G., Gregory, A. C., Huys, G. R., Faust, K., and Raes, J. (2019). Synthetic ecology of the human gut microbiota. Nature Reviews Microbiology 17, 754–763. doi:10.1038/s41579-019-0264-8.
  • Waite, D. W., Eason, D. K., Taylor, M. W., and Goodrich-Blair, H. (2014). Influence of hand rearing and bird age on the fecal microbiota of the critically endangered kakapo. Applied and Environmental Microbiology 80, 4650–4658. doi:10.1128/AEM.00975-14.
  • Waite, D. W., and Taylor, M. W. (2014). Characterizing the avian gut microbiota: Membership, driving influences, and potential function. Frontiers in Microbiology 5, 223. doi:10.3389/fmicb.2014.00223.
  • Waite, D. W., and Taylor, M. (2015). Exploring the avian gut microbiota: Current trends and future directions. Frontiers in Microbiology 6, 673. doi:10.3389/fmicb.2015.00673.
  • Wang, W., Cao, J., Yang, F., Wang, X., Zheng, S., Sharshov, K., and Li, L. (2016). High‐throughput sequencing reveals the core gut microbiome of bar‐headed goose (Anser indicus) in different wintering areas in Tibet. MicrobiologyOpen 5, 287–295. doi:10.1002/mbo3.327.
  • Wang, W., Sharshov, K., Zhang, Y., and Gui, L. (2019). Age-related changes in the cloacal microbiota of bar-headed geese (Anser indicus). Kafkas Üniversitesi Veteriner Fakültesi Dergisi 25, 575–582.
  • Wang, W., Wang, F., Li, L., Wang, A., Sharshov, K., Druzyaka, A., and Lancuo, Z. (2020). Characterization of the gut microbiome of black-necked cranes (Grus nigricollis) in six wintering areas in China. Archives of Microbiology 202, 983–993. doi:10.1007/s00203-019-01802-0
  • Wang, W., Zheng, S., Li, L., Yang, Y., Liu, Y., Wang, A., and Li, Y. (2018). Comparative metagenomics of the gut microbiota in wild greylag geese (Anser anser) and ruddy shelducks (Tadorna ferruginea). MicrobiologyOpen 8, e725.
  • Wenny, D. G., Devault, T. L., Johnson, M. D., Kelly, D., Sekercioglu, C. H., Tomback, D. F., and Whelan, C. J. (2011). The need to quantify ecosystem services provided by birds. The Auk 128, 1–14. doi:10.1525/auk.2011.10248.
  • West, A. G., Waite, D. W., Deines, P., Bourne, D. G., Digby, A., McKenzie, V. J., and Tayor, M. W. (2019). The microbiome in threatened species conservation. Biological Conservation 229, 85–98. doi:10.1016/j.biocon.2018.11.016.
  • Whelan, C. J., Wenny, D. G., and Marquis, R. J. (2008). Ecosystem services provided by birds. Annals of the New York Academy of Sciences 1134, 25–60. doi:10.1196/annals.1439.003.
  • Wienemann, T., Schmitt-Wagner, D., Meuser, K., Segelbacher, G., Schink, B., Brune, A., and Berthold, P. (2011). The bacterial microbiota in the ceca of Capercaillie (Tetrao urogallus) differs between wild and captive birds. Systematic and Applied Microbiology 34, 542–551. doi:10.1016/j.syapm.2011.06.003.
  • Wilkinson, N., Hughes, R. J., Bajagai, Y. S., Aspden, W. J., Van, T. T. H., Moore, R. J., and Stanley, D. (2020). Reduced environmental bacterial load during early development and gut colonisation has detrimental health consequences in Japanese quail. Heliyon 6, e03213. doi:10.1016/j.heliyon.2020.e03213.
  • Worsley, S. F., Davies, C. S., Mannarelli, M. E., Hutchings, M. I., Komdeur, J., Burke, T., and Dugdale, H. L. (2021). Gut microbiome composition, not alpha diversity, is associated with survival in a natural vertebrate population. Animal Microbiome 3, 1–18. doi:10.1186/s42523-021-00149-6
  • Wright, A. D. G., Northwood, K. S., and Obispo, N. E. (2009). Rumen-like methanogens identified from the crop of the folivorous South American bird, the hoatzin (Opisthocomus hoazin). The ISME Journal 3, 1120–1126. doi:10.1038/ismej.2009.41.
  • Wu, H., Wu, F.-T., Zhou, Q.-H., and Zhao, D.-P. (2021). Comparative analysis of gut microbiota in captive and wild oriental white dtorks: Implications for conservation biology. Frontiers in Microbiology 12, 649466.
  • Wu, Y., Yang, Y., Cao, L., Yin, H., Xu, M., Wang, Z., and Queiroz, M. G. L. (2018). Habitat environments impacted the gut microbiome of long-distance migratory swan geese but central species conserved. Scientific Reports 8, 1–11. doi:10.1038/s41598-017-17765-5
  • Xenoulis, P. G., Gray, P. L., Brightsmith, D., Palculict, B., Hoppes, S., Steiner, J. M., and Tizard, I. (2010). Molecular characterization of the cloacal microbiota of wild and captive parrots. Veterinary Microbiology 146, 320–325. doi:10.1016/j.vetmic.2010.05.024
  • Xiao, K., Fan, Y., Zhang, Z., Shen, X., Li, X., Liang, X., and Bi, R. (2021). Covariation of the fecal microbiome with diet in non-passerine birds. Msphere 6, e00308–21. doi:10.1128/mSphere.00308-21
  • Yadav, S., and Jha, R. (2019). Strategies to modulate the intestinal microbiota and their effects on nutrient utilization, performance, and health of poultry. Journal of Animal Science and Biotechnology 10, 1–11. doi:10.1186/s40104-018-0310-9.
  • Yang, Y., Deng, Y., Cao, L., Landi, S., Tonazzini, I., Cecchini, M., and Piazza, V. (2016). Characterising the interspecific variations and convergence of gut microbiota in Anseriformes herbivores at wintering areas. Scientific Reports 6, 1–11. doi:10.1038/s41598-016-0001-8.
  • Youngblut, N. D., Reischer, G. H., Walters, W., Schuster, N., Walzer, C., Stalder, G., and Ley, R. E. (2019). Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nature Communications 10, 1–15. doi:10.1038/s41467-019-10191-3
  • Zeng, Y. X., Li, H. R., Han, W., and Luo, W. (2021). Comparison of gut microbiota between Gentoo and Adélie Penguins breeding sympatrically on Antarctic Ardley Island as revealed by fecal DNA sequencing. Diversity 13, 500. doi:10.3390/d13100500.
  • Zhang, Z., Yang, Z., and Zhu, L. (2021). Gut microbiome of migratory shorebirds: Current status and future perspectives. Ecology and Evolution 11, 3737–3745. doi:10.1002/ece3.7390.
  • Zhou, L., Huo, X., Liu, B., Wu, H., and Feng, J. (2020). Comparative analysis of the gut microbial communities of the Eurasian kestrel (Falco tinnunculus) at different developmental stages. Frontiers in Microbiology 11, 3152. doi:10.3389/fmicb.2020.592539.
  • Zhu, Y., Li, Y., Yang, H., He, K., and Tang, K. (2021). Establishment of gut microbiome during early life and its relationship with growth in endangered crested ibis (Nipponia nippon). Frontiers in Microbiology 2276, 723682.
  • Zilber-Rosenberg, I., and Rosenberg, E. (2008). Role of microorganisms in the evolution of animals and plants: The hologenome theory of evolution. FEMS Microbiology Reviews 32, 723–735. doi:10.1111/j.1574-6976.2008.00123.x.

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