Flexibility and resilience of great tit (Parus major) gut microbiomes to changing diets
Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
CF17-0248
Carlsbergfondet
18-23794Y
Grantová Agentura České Republiky
GAJU n.048/2019/P
Jihočeská Univerzita v Českých Budějovicích
PubMed
33602335
PubMed Central
PMC7893775
DOI
10.1186/s42523-021-00076-6
PII: 10.1186/s42523-021-00076-6
Knihovny.cz E-zdroje
- Klíčová slova
- 16S rRNA gene, Bacterial communities, Community flexibility, Community resilience, Gut symbionts, Illumina MiSeq,
- Publikační typ
- časopisecké články MeSH
BACKGROUND: Gut microbial communities play important roles in nutrient management and can change in response to host diets. The extent of this flexibility and the concomitant resilience is largely unknown in wild animals. To untangle the dynamics of avian-gut microbiome symbiosis associated with diet changes, we exposed Parus major (Great tits) fed with a standard diet (seeds and mealworms) to either a mixed (seeds, mealworms and fruits), a seed, or a mealworm diet for 4 weeks, and examined the flexibility of gut microbiomes to these compositionally different diets. To assess microbiome resilience (recovery potential), all individuals were subsequently reversed to a standard diet for another 4 weeks. Cloacal microbiomes were collected weekly and characterised through sequencing the v4 region of the 16S rRNA gene using Illumina MiSeq. RESULTS: Initial microbiomes changed significantly with the diet manipulation, but the communities did not differ significantly between the three diet groups (mixed, seed and mealworm), despite multiple diet-specific changes in certain bacterial genera. Reverting birds to the standard diet led only to a partial recovery in gut community compositions. The majority of the bacterial taxa that increased significantly during diet manipulation decreased in relative abundance after reversion to the standard diet; however, bacterial taxa that decreased during the manipulation rarely increased after diet reversal CONCLUSIONS: The gut microbial response and partial resilience to dietary changes support that gut bacterial communities of P. major play a role in accommodating dietary changes experienced by wild avian hosts. This may be a contributing factor to the relaxed association between microbiome composition and the bird phylogeny. Our findings further imply that interpretations of wild bird gut microbiome analyses from single-time point sampling, especially for omnivorous species or species with seasonally changing diets, should be done with caution. The partial community recovery implies that ecologically relevant diet changes (e.g., seasonality and migration) open up gut niches that may be filled by previously abundant microbes or replaced by different symbiont lineages, which has important implications for the integrity and specificity of long-term avian-symbiont associations.
Biology Centre of Czech Academy of Sciences Institute of Entomology Ceske Budejovice Czech Republic
Faculty of Science University of South Bohemia Ceske Budejovice Czech Republic
Natural History Museum of Denmark University of Copenhagen Copenhagen Denmark
Section for Ecology and Evolution Department of Biology University of Copenhagen Copenhagen Denmark
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Flint HJ, Scott KP, Louis P, Duncan SH. The role of the gut microbiota in nutrition and health. Nat Rev Gastro Hepat. 2012;9(10):577–589. doi: 10.1038/nrgastro.2012.156. PubMed DOI
Waite DW, Taylor MW. Exploring the avian gut microbiota: current trends and future directions. Front Microbiol. 2015;6:673. doi: 10.3389/fmicb.2015.00673. PubMed DOI PMC
Hanning I, Diaz-Sanchez S. The functionality of the gastrointestinal microbiome in non-human animals. Microbiome. 2015;3:51. doi: 10.1186/s40168-015-0113-6. PubMed DOI PMC
Sabree ZL, Moran NA. Host-specific assemblages typify gut microbial communities of related insect species. Springerplus. 2014;3:138. doi: 10.1186/2193-1801-3-138. PubMed DOI PMC
Colman DR, Toolson EC, Takacs-Vesbach CD. Do diet and taxonomy influence insect gut bacterial communities? Mol Ecol. 2012;21(20):5124–5137. doi: 10.1111/j.1365-294X.2012.05752.x. PubMed DOI
Dietrich C, Kohler T, Brune A. The cockroach origin of the termite gut microbiota: patterns in bacterial community structure reflect major evolutionary events. Appl Environ Microbiol. 2014;80(7):2261–2269. doi: 10.1128/AEM.04206-13. PubMed DOI PMC
Anderson KE, Russell JA, Moreau CS, Kautz S, Sullam KE, Hu Y, Basinger U, Mott BM, Buck N, Wheeler DE. Highly similar microbial communities are shared among related and trophically similar ant species. Mol Ecol. 2012;21(9):2282–2296. doi: 10.1111/j.1365-294X.2011.05464.x. PubMed DOI
Kennedy SR, Tsau S, Gillespie R, Krehenwinkel H. Are you what you eat? A highly transient and prey-influenced gut microbiome in the grey house spider Badumna longinqua. Mol Ecol. 2020;29(5):1001–1015. doi: 10.1111/mec.15370. PubMed DOI
Liu H, Guo X, Gooneratne R, Lai R, Zeng C, Zhan F, Wang W. The gut microbiome and degradation enzyme activity of wild freshwater fishes influenced by their trophic levels. Sci Rep. 2016;6:24340. doi: 10.1038/srep24340. PubMed DOI PMC
Sullam KE, Rubin BE, Dalton CM, Kilham SS, Flecker AS, Russell JA. Divergence across diet, time and populations rules out parallel evolution in the gut microbiomes of Trinidadian guppies. ISME J. 2015;9(7):1508–1522. doi: 10.1038/ismej.2014.231. PubMed DOI PMC
Chang CW, Huang BH, Lin SM, Huang CL, Liao PC. Changes of diet and dominant intestinal microbes in farmland frogs. BMC Microbiol. 2016;16:33. doi: 10.1186/s12866-016-0660-4. PubMed DOI PMC
Muegge BD, Kuczynski J, Knights D, Clemente JC, Gonzalez A, Fontana L, Henrissat B, Knight R, Gordon JI. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science. 2011;332(6032):970–974. doi: 10.1126/science.1198719. PubMed DOI PMC
Delsuc F, Metcalf JL, Wegener Parfrey L, Song SJ, Gonzalez A, Knight R. Convergence of gut microbiomes in myrmecophagous mammals. Mol Ecol. 2014;23(6):1301–1317. doi: 10.1111/mec.12501. PubMed DOI
Bodawatta KH, Sam K, Jonsson KA, Poulsen M. Comparative analyses of the digestive tract microbiota of new Guinean passerine birds. Front Microbiol. 2018;9:1830. doi: 10.3389/fmicb.2018.01830. PubMed DOI PMC
Hird SM, Sanchez C, Carstens BC, Brumfield RT. Comparative gut microbiota of 59 neotropical bird species. Front Microbiol. 2015;6:1403. doi: 10.3389/fmicb.2015.01403. PubMed DOI PMC
Capunitan DC, Johnson O, Terrill RS, Hird SM. Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea. Mol Ecol. 2020;29(4):829–847. doi: 10.1111/mec.15354. PubMed DOI
Grond K, Sandercock BK, Jumpponen A, Zeglin LH. The avian gut microbiota: community, physiology and function in wild birds. J Avian Biol. 2018;49(11):e01788.
Waite DW, Taylor MW. Characterizing the avian gut microbiota: membership, driving influences, and potential function. Front Microbiol. 2014;5:223. doi: 10.3389/fmicb.2014.00223. PubMed DOI PMC
Youngblut ND, Reischer GH, Walters W, Schuster N, Walzer C, Stalder G, Ley RE, Farnleitner AH. Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat Commun. 2019;10(1):2200. doi: 10.1038/s41467-019-10191-3. PubMed DOI PMC
Song SJ, Sanders JG, Delsuc F, Metcalf J, Amato K, Taylor MW, Mazel F, Lutz HL, Winker K, Graves GR, et al. Comparative analyses of vertebrate gut microbiomes reveal convergence between birds and bats. mBio. 2020;11(1):e02901–19. PubMed PMC
Amato KR, Leigh SR, Kent A, Mackie RI, Yeoman CJ, Stumpf RM, Wilson BA, Nelson KE, White BA, Garber PA. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra) Microb Ecol. 2015;69(2):434–443. doi: 10.1007/s00248-014-0554-7. PubMed DOI
Maurice CF, Knowles SCL, Ladau J, Pollard KS, Fenton A, Pedersen AB, Turnbaugh PJ. Marked seasonal variation in the wild mouse gut microbiota. ISME J. 2015;9(11):2423–2434. doi: 10.1038/ismej.2015.53. PubMed DOI PMC
Carmody RN, Gerber GK, Luevano JM, Gatti DM, Somes L, Svenson KL, Turnbaugh PJ. Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe. 2015;17(1):72–84. doi: 10.1016/j.chom.2014.11.010. PubMed DOI PMC
Ren TT, Boutin S, Humphries MM, Dantzer B, Gorrell JC, Coltman DW, McAdam AG, Wu M. Seasonal, spatial, and maternal effects on gut microbiome in wild red squirrels. Microbiome. 2017;5:163. doi: 10.1186/s40168-017-0382-3. PubMed DOI PMC
Hang I, Rinttila T, Zentek J, Kettunen A, Alaja S, Apajalahti J, Harmoinen J, de Vos WM, Spillmann T. Effect of high contents of dietary animal-derived protein or carbohydrates on canine faecal microbiota. BMC Vet Res. 2012;8:90. doi: 10.1186/1746-6148-8-90. PubMed DOI PMC
David LA, Maurice CF, Carmody RN, Gootenberg DB, Button JE, Wolfe BE, Ling AV, Devlin AS, Varma Y, Fischbach MA, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505(7484):559–563. doi: 10.1038/nature12820. PubMed DOI PMC
Cao J, Hu Y, Liu F, Wang Y, Bi Y, Lv N, Li J, Zhu B, Gao GF. Metagenomic analysis reveals the microbiome and resistome in migratory birds. Microbiome. 2020;8(1):26. doi: 10.1186/s40168-019-0781-8. PubMed DOI PMC
Loo WT, Garcia-Loor J, Dudaniec RY, Kleindorfer S, Cavanaugh CM. Host phylogeny, diet, and habitat differentiate the gut microbiomes of Darwin’s finches on Santa Cruz Island. Sci Rep. 2019;9(1):18781. doi: 10.1038/s41598-019-54869-6. PubMed DOI PMC
Grond K, Santo Domingo JW, Lanctot RB, Jumpponen A, Bentzen RL, Boldenow ML, Brown SC, Casler B, Cunningham JA, Doll AC, et al. Composition and drivers of gut microbial communities in arctic-breeding shorebirds. Front Microbiol. 2019;10:2258. doi: 10.3389/fmicb.2019.02258. PubMed DOI PMC
Wang W, Wang F, Li L, Wang A, Sharshov K, Druzyaka A, Lancuo Z, Wang S, Shi Y. Characterization of the gut microbiome of black-necked cranes (Grus nigricollis) in six wintering areas in China. Arch Microbiol. 2020;202:983–93. PubMed
Hird SM, Carstens BC, Cardiff SW, Dittmann DL, Brumfield RT. Sampling locality is more detectable than taxonomy or ecology in the gut microbiota of the brood-parasitic Brown-headed cowbird (Molothrus ater) Peerj. 2014;2:e231. doi: 10.7717/peerj.321. PubMed DOI PMC
Araújo PM, Viegas I, Rocha AD, Villegas A, Jones JG, Mendonça L, Ramos JA, Masero JA, Alves JA. Understanding how birds rebuild fat stores during migration: insights from an experimental study. Sci Rep-Uk. 2019;9:10065. doi: 10.1038/s41598-019-46487-z. PubMed DOI PMC
Pierce BJ, McWilliams SR. Seasonal changes in composition of lipid stores in migratory birds: causes and consequences. Condor. 2005;107(2):269–279. doi: 10.1093/condor/107.2.269. DOI
Boyle WA, Conway CJ, Bronstein JL. Why do some, but not all, tropical birds migrate? A comparative study of diet breadth and fruit preference. Evol Ecol. 2010;25:219–236. doi: 10.1007/s10682-010-9403-4. DOI
Witmer MC. Annual diet of Cedar Waxwings based on U.S. Biological Survey Records (1885-1950) compared to diet of American robins: contrasts in dietary patterns and natural history. Auk. 1996;113(2):414–430. doi: 10.2307/4088908. DOI
Vel’ky M, Kanuch P, Kristin A. Food composition of wintering great tits (Parus major): habitat and seasonal aspects. J Vertebrate Biol. 2011;60(3):228–236.
Bakour S, Moulaï R. Dietary analysis across breeding seasons of Eleonora's Falcon Falco eleonorae on the western coast of Algeria. Ostrich. 2019;90(1):63–72. doi: 10.2989/00306525.2018.1546774. DOI
Westerberg K, Brown R, Eagle G, Votier SC. Intra-population variation in the diet of an avian top predator: generalist and specialist foraging in great black-backed gulls Larus marinus. Bird Stud. 2019;66(3):390–397. doi: 10.1080/00063657.2019.1693961. DOI
Ankney CD, Scott DM. Changes in nutrient reserves and diet of breeding Brown-headed cowbirds. Auk. 1980;97(4):684–696.
Lewis WB, Moore FR, Wang SA. Characterization of the gut microbiota of migratory passerines during stopover along the northern coast of the Gulf of Mexico. J Avian Biol. 2016;47(5):659–668. doi: 10.1111/jav.00954. DOI
Wu Y, Yang Y, Cao L, Yin H, Xu M, Wang Z, Liu Y, Wang X, Deng Y. Habitat environments impacted the gut microbiome of long-distance migratory swan geese but central species conserved. Sci Rep. 2018;8(1):13314. doi: 10.1038/s41598-018-31731-9. PubMed DOI PMC
Risely A, Waite DW, Ujvari B, Hoye BJ, Klaassen M. Active migration is associated with specific and consistent changes to gut microbiota in Calidris shorebirds. J Anim Ecol. 2018;87(2):428–437. doi: 10.1111/1365-2656.12784. PubMed DOI
Dong Y, Xiang X, Zhao G, Song Y, Zhou L. Variations in gut bacterial communities of hooded crane (Grus monacha) over spatial-temporal scales. Peerj. 2019;7:e7045. doi: 10.7717/peerj.7045. PubMed DOI PMC
Zhang F, Xiang X, Dong Y, Yan S, Song Y, Zhou L. Significant differences in the gut bacterial communities of hooded crane (Grus monacha) in different seasons at a stopover site on the flyway. Animals. 2020;10(4):701. doi: 10.3390/ani10040701. PubMed DOI PMC
Liu G, Gong Z, Li Q. Variations in gut bacterial communities between lesser white-fronted geese wintering at Caizi and Shengjin lakes in China. Microbiologyopen. 2020;00:e1037. PubMed PMC
Juan PAS, Hendershot JN, Daily GC, Fukami T. Land-use change has host-specific influences on avian gut microbiomes. ISME J. 2020;14:318–321. doi: 10.1038/s41396-019-0535-4. PubMed DOI PMC
Phillips JN, Berlow M, Derryberry EP. The effects of landscape urbanization on the gut microbiome: an exploration into the gut of urban and rural white-crowned sparrows. Front Ecol Evol. 2018;6:148. 10.3389/fevo.2018.00148.
Teyssier A, Rouffaer LO, Saleh Hudin N, Strubbe D, Matthysen E, Lens L, White J. Inside the guts of the city: urban-induced alterations of the gut microbiota in a wild passerine. Sci Total Environ. 2018;612:1276–1286. doi: 10.1016/j.scitotenv.2017.09.035. PubMed DOI
Gillingham MAF, Bechet A, Cezilly F, Wilhelm K, Rendon-Martos M, Borghesi F, Nissardi S, Baccetti N, Azafzaf H, Menke S, et al. Offspring microbiomes differ across breeding sites in a panmictic species. Front Microbiol. 2019;10:35. doi: 10.3389/fmicb.2019.00035. PubMed DOI PMC
Murray MH, Lankau EW, Kidd AD, Welch CN, Ellison T, Adams HC, Lipp EK, Hernandez SM. Gut microbiome shifts with urbanization and potentially facilitates a zoonotic pathogen in a wading bird. PLoS One. 2020;15(3):e0220926. doi: 10.1371/journal.pone.0220926. PubMed DOI PMC
Teyssier A, Matthysen E, Hudin NS, de Neve L, White J, Lens L. Diet contributes to urban-induced alterations in gut microbiota: experimental evidence from a wild passerine. Proc Biol Sci. 2020;287(1920):20192182. PubMed PMC
Davidson G, Wiley N, Cooke AC, Johnson CN, Fouhy F, Reichert MS, Hera I, Crane JMS, Kulahci IG, Ross RP, et al. Diet induces parallel changes to the gut microbiota and problem solving performance in a wild bird. Sci Rep. 2020;10:20783. doi: 10.1038/s41598-020-77256-y. PubMed DOI PMC
Hicks AL, Lee KJ, Couto-Rodriguez M, Patel J, Sinha R, Guo C, Olson SH, Seimon A, Seimon TA, Ondzie AU, et al. Gut microbiomes of wild great apes fluctuate seasonally in response to diet. Nat Commun. 2018;9(1):1786. doi: 10.1038/s41467-018-04204-w. PubMed DOI PMC
Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP. DADA2: high-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13(7):581–583. doi: 10.1038/nmeth.3869. PubMed DOI PMC
Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37(8):852–857. doi: 10.1038/s41587-019-0209-9. PubMed DOI PMC
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013;41(D1):D590–D596. doi: 10.1093/nar/gks1219. PubMed DOI PMC
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550. doi: 10.1186/s13059-014-0550-8. PubMed DOI PMC
Finke MD. Complete nutrient composition of commercially raised invertebrates used as food for insectivores. Zoo Biol. 2002;21:269–285. doi: 10.1002/zoo.10031. DOI
Muhammad Anjum F, Nadeem M, Issa Khan M, Hussain S. Nutritional and therapeutic potential of sunflower seeds. Br Food J. 2012;114(4):544–552. doi: 10.1108/00070701211219559. DOI
Barbeau WE, Hilu KW. Protein, calcium, iron, and amino acid content of selected wild and domesticated cultivars of finger millet. Plant Foods Hum Nutr. 1993;43(2):97–104. doi: 10.1007/BF01087914. PubMed DOI
Escarnot E, Jacquemin J, Agneessens R, Paquot M. Comparative study of the content and profiles of macronutrients in spelt and wheat, a review. Biotechnol, Agronomy, Soc Environ. 2012;16(2):243–256.
Trevelline BK, Sosa J, Hartup BK, Kohl KD. A bird's-eye view of phylosymbiosis: weak signatures of phylosymbiosis among all 15 species of cranes. Proc Biol Sci. 2020;287(1923):20192988. PubMed PMC
Hofstad T. The genus Fusobacterium. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E, editors. The Prokaryotes - A handbook on the biology of bacteria. New York: Springer-Verlag; 2006. pp. 1016–1027.
Bennett DC, Tun HM, Kim JE, Leung FC, Cheng KM. Characterization of cecal microbiota of the emu (Dromaius novaehollandiae) Vet Microbiol. 2013;166(1–2):304–310. doi: 10.1016/j.vetmic.2013.05.018. PubMed DOI
Wang W, Zheng SS, Li LX, Yang YS, Liu YB, Wang AZ, Sharshov K, Li Y. Comparative metagenomics of the gut microbiota in wild Greylag geese (Anser anser) and ruddy shelducks (Tadorna ferruginea) Microbiologyopen. 2019;8(5):e00725. doi: 10.1002/mbo3.725. PubMed DOI PMC
Drovetski SV, O'Mahoney M, Ransome EJ, Matterson KO, Lim HC, Chesser RT, Graves GR. Spatial organization of the gastrointestinal microbiota in urban Canada geese. Sci Rep-Uk. 2018;8:3713. doi: 10.1038/s41598-018-21892-y. PubMed DOI PMC
Burapan S, Kim M, Han J. Demethylation of polymethoxyflavones by human gut bacterium, Blautia sp MRG-PMF1. J Agr Food Chem. 2017;65(8):1620–1629. doi: 10.1021/acs.jafc.7b00408. PubMed DOI
Rowland I, Gibson G, Heinken A, Scott K, Swann J, Thiele I, Tuohy K. Gut microbiota functions: metabolism of nutrients and other food components. Eur J Nutr. 2018;57(1):1–24. doi: 10.1007/s00394-017-1445-8. PubMed DOI PMC
La Reau AJ, Suen G. The Ruminococci: key symbionts of the gut ecosystem. J Microbiol. 2018;56(3):199–208. doi: 10.1007/s12275-018-8024-4. PubMed DOI
Montagne L, Piel C, Lalles JP. Effect of diet on mucin kinetics and composition: nutrition and health implications. Nutr Rev. 2004;62(3):105–114. doi: 10.1111/j.1753-4887.2004.tb00031.x. PubMed DOI
Amaretti A, Gozzoli C, Simone M, Raimondi S, Righini L, Perez-Brocal V, Garcia-Lopez R, Moya A, Rossi M. Profiling of protein degraders in cultures of human gut microbiota. Front Microbiol. 2019;10:2614. doi: 10.3389/fmicb.2019.02614. PubMed DOI PMC
Leblanc DJ. Enterococcus. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E, editors. The Prokaryotes - A handbook on the biology of bacteria. 3. New York: Springer-Verlag; 2006. pp. 175–204.
Holzapfel WH, Franz CMAP, Ludwig W, Back W, LMT D. The genera Pediococcus and Tetragenococcus. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E, editors. The Prokaryotes - A handbook on the biology of bacteria. 3. New York: Springer-Verlag; 2006. pp. 229–266.
Teuber M, Geis A. The genus Lactococcus. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E, editors. The Prokaryotes - A handbook on the biology of bacteria. 3. New York: Springer-Verlag; 2006. pp. 205–228.
Kwon GT, Yuk HG, Lee SJ, Chung YH, Jang HS, Yoo JS, Cho KH, Kong H, Shin D. Mealworm larvae (Tenebrio molitor L.) exuviae as a novel prebiotic material for BALB/c mouse gut microbiota. Food Sci Biotechnol. 2020;29(4):531–537. doi: 10.1007/s10068-019-00699-1. PubMed DOI PMC
Kropackova L, Pechmanova H, Vinkler M, Svobodova J, Velova H, Tesicky M, Martin JF, Kreisinger J. Variation between the oral and faecal microbiota in a free-living passerine bird, the great tit (Parus major) PLoS One. 2017;12(6):e0179945. doi: 10.1371/journal.pone.0179945. PubMed DOI PMC
Drovetski SV, O’Mahoney MJV, Matterson KO, Schmidt BK, Grant BR. Distinct microbiotas of anatomical gut regions display idiosyncratic seasonal variation in an avian folivore. BMC Anim Microbiome. 2019;1:2. doi: 10.1186/s42523-019-0002-6. PubMed DOI PMC
Przemieniecki SW, Kosewska A, Ciesielski S, Kosewska O. Changes in the gut microbiome and enzymatic profile of Tenebrio molitor larvae biodegrading cellulose, polyethylene and polystyrene waste. Environ Pollut. 2020;256:113265. doi: 10.1016/j.envpol.2019.113265. PubMed DOI
Bodawatta KH, Puzejova K, Sam K, Poulsen M, Jonsson KA. Cloacal swabs and alcohol bird specimens are good proxies for compositional analyses of gut microbial communities of great tits (Parus major) BMC Anim Microbiome. 2020;2:9. doi: 10.1186/s42523-020-00026-8. PubMed DOI PMC
Moya A, Ferrer M. Functional redundancy-induced stability of gut microbiota subjected to disturbance. Trends Microbiol. 2016;24(5):402–413. doi: 10.1016/j.tim.2016.02.002. PubMed DOI
Trosvik P, de Muinck EJ. Ecology of bacteria in the human gastrointestinal tract-identification of keystone and foundation taxa. Microbiome. 2015;3:44. doi: 10.1186/s40168-015-0107-4. PubMed DOI PMC
Isaksson C, Anderson S. Carotenoid diet and nestling provisioning in urban and rural great tits Parus major. J Avian Biol. 2007;38(5):564–572. doi: 10.1111/j.0908-8857.2007.04030.x. DOI
Lambertucci SA, Trejo A, Di Martino S, Sánchez-Zapata JA, Donázar JA, Hiraldo F. Spatial and temporal patterns in the diet of the Andean condor: ecological replacement of native fauna by exotic species. Anim Conserv. 2009;12(4):338–345. doi: 10.1111/j.1469-1795.2009.00258.x. DOI
Griffiths R, Double MC, Orr K, Dawson RJG. A DNA test to sex most birds. Mol Ecol. 1998;7(8):1071–1075. doi: 10.1046/j.1365-294x.1998.00389.x. PubMed DOI
Lezalova-Pialkova R. Molecular evidence for extra-pair paternity and intraspecific brood parasitism in the black-headed Gull. J Ornithol. 2011;152(2):291–295. doi: 10.1007/s10336-010-0581-1. DOI
R: A language and environment for statistical computing. [https://www.R-project.org/]. Accessed 15 Jan 2020.
RStudio: Integrated Development for R [http://www.rstudio.com/]. Accessed 15 Jan 2020.
vegan: Community Ecology Package. R package version 2.5–4 [https://CRAN.R-project.org/package=vegan]. Accessed 15 Jan 2020
pairwiseAdonis: Pairwise multilevel comparison using adonis [https://github.com/pmartinezarbizu/pairwiseAdonis]. Accessed 15 Jan 2020.
McMurdie PJ, Holmes S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One. 2013;8(4):e61217. PubMed PMC
Specific gut bacterial responses to natural diets of tropical birds