Effects of Urbanization and Landscape on Gut Microbiomes in White-Crowned Sparrows


Habitats are changing rapidly around the globe and urbanization is one of the primary drivers. Urbanization changes food availability, environmental stressors, and the prevalence of disease for many species. These changes can lead to divergence in phenotypic traits, including behavioral, physiological, and morphological features between urban and rural populations. Recent research highlights that urbanization is also changing the gut microbial communities found in a diverse group of host species. These changes have not been uniform, leaving uncertainty as to how urban habitats are shaping gut microbial communities. To better understand these effects, we investigated the gut bacterial communities of White-Crowned Sparrow (Zonotrichia leucophrys) populations along an urbanization gradient in the San Francisco Bay area. We examined how gut bacterial communities vary with the local environment and host morphological characteristics. We found direct effects of environmental factors, including urban noise levels and territory land cover, as well as indirect effects through body size and condition, on alpha and beta diversity of gut microbial communities. We also found that urban and rural birds’ microbiomes differed in which variables predicted their diversity, with urban communities driven by host morphology, and rural communities driven by environmental factors. Elucidating these effects provides a better understanding of how urbanization affects wild avian physiology.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5


  1. 1.

    Liu Z, He C, Wu J (2016) General spatiotemporal patterns of urbanization: an examination of 16 world cities. Sustain 8:1–15. https://doi.org/10.3390/su8010041

    Article  Google Scholar 

  2. 2.

    Blouin D, Pellerin S, Poulin M (2019) Increase in non-native species richness leads to biotic homogenization in vacant lots of a highly urbanized landscape. Urban Ecosyst. 22:879–892. https://doi.org/10.1007/s11252-019-00863-9

    Article  Google Scholar 

  3. 3.

    Swaddle JP, Francis CD, Barber JR, Cooper CB, Kyba CCM, Dominoni DM, Shannon G, Aschehoug E, Goodwin SE, Kawahara AY, Luther D, Spoelstra K, Voss M, Longcore T (2015) A framework to assess evolutionary responses to anthropogenic light and sound. Trends Ecol Evol 30:550–560. https://doi.org/10.1016/j.tree.2015.06.009

    Article  PubMed  Google Scholar 

  4. 4.

    Seress G, Hammer T, Bókony V, Vincze E, Preiszner B, Pipoly I, Sinkovics C, Evans KL, Liker A (2018) Impact of urbanization on abundance and phenology of caterpillars and consequences for breeding in an insectivorous bird. Ecol Appl 28:1143–1156. https://doi.org/10.1002/eap.1730

    Article  PubMed  Google Scholar 

  5. 5.

    Brans KI, Stoks R, De Meester L (2018) Urbanization drives genetic differentiation in physiology and structures the evolution of pace-of-life syndromes in the water flea Daphnia magna. Proc R Soc B Biol Sci 285:20180169. https://doi.org/10.1098/rspb.2018.0169

    CAS  Article  Google Scholar 

  6. 6.

    Costantini D, Greives TJ, Hau M, Partecke J (2014) Does urban life change blood oxidative status in birds? J Exp Biol 217:2994–2997. https://doi.org/10.1242/jeb.106450

    Article  PubMed  Google Scholar 

  7. 7.

    Putman BJ, Gasca M, Blumstein DT, Pauly GB (2019) Downsizing for downtown: limb lengths, toe lengths, and scale counts decrease with urbanization in western fence lizards (Sceloporus occidentalis). Urban Ecosyst. 22:1071–1081. https://doi.org/10.1007/s11252-019-00889-z

    Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Gadau A, Crawford MS, Mayek R et al (2019) A comparison of the nutritional physiology and gut microbiome of urban and rural house sparrows (Passer domesticus). Comp Biochem Physiol Part - B Biochem Mol Biol 237:110332. https://doi.org/10.1016/j.cbpb.2019.110332

    CAS  Article  Google Scholar 

  9. 9.

    Ayeni FA, Biagi E, Rampelli S, Fiori J, Soverini M, Audu HJ, Cristino S, Caporali L, Schnorr SL, Carelli V, Brigidi P, Candela M, Turroni S (2018) Infant and adult gut microbiome and metabolome in rural Bassa and urban settlers from Nigeria. Cell Rep 23:3056–3067. https://doi.org/10.1016/j.celrep.2018.05.018

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Littleford-Colquhoun BL, Weyrich LS, Kent N, Frere CH (2019) City life alters the gut microbiome and stable isotope profiling of the eastern water dragon (Intellagama lesueurii). Mol Ecol 28:4592–4607. https://doi.org/10.1111/mec.15240

    Article  PubMed  Google Scholar 

  11. 11.

    Teyssier A, Rouffaer LO, Saleh Hudin N, Strubbe D, Matthysen E, Lens L, White J (2018) Inside the guts of the city: urban-induced alterations of the gut microbiota in a wild passerine. Sci Total Environ 612:1276–1286. https://doi.org/10.1016/j.scitotenv.2017.09.035

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Phillips JN, Berlow M, Derryberry EP (2018) The effects of landscape urbanization on the gut microbiome: an exploration into the gut of urban and rural white-crowned sparrows. Front Ecol Evol 6:1–10. https://doi.org/10.3389/fevo.2018.00148

    Article  Google Scholar 

  13. 13.

    Heijtz RD, Wang S, Anuar F, Qian Y, Bjorkholm B, Samuelsson A, Hibberd ML, Forssberg H, Pettersson S (2011) Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci 108:3047–3052. https://doi.org/10.1073/pnas.1010529108

    Article  Google Scholar 

  14. 14.

    Bäckhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI (2005) Host-bacterial mutualism in the human intestine. Science 307:1915–1920. https://doi.org/10.1126/science.1104816

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Lyte M (2010) The microbial organ in the gut as a driver of homeostasis and disease. Med Hypotheses 74:634–638. https://doi.org/10.1016/j.mehy.2009.10.025

    Article  PubMed  Google Scholar 

  16. 16.

    West AG, Waite DW, Deines P, Bourne DG, Digby A, McKenzie VJ, Taylor MW (2019) The microbiome in threatened species conservation. Biol Conserv 229:85–98. https://doi.org/10.1016/j.biocon.2018.11.016

    Article  Google Scholar 

  17. 17.

    Trevelline BK, Fontaine SS, Hartup BK, Kohl KD (2019) Conservation biology needs a microbial renaissance: a call for the consideration of host-associated microbiota in wildlife management practices. Proc R Soc B Biol Sci:286. https://doi.org/10.1098/rspb.2018.2448

  18. 18.

    Leung MHY, Wilkins D, Li EKT, Kong FKF, Lee PKH (2014) Indoor-air microbiome in an urban subway network: diversity and dynamics. Appl Environ Microbiol 80:6760–6770. https://doi.org/10.1128/AEM.02244-14

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    De Filippo C, Cavalieri D, Di Paola M et al (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci 107:14691–14696. https://doi.org/10.1073/pnas.1005963107

    Article  PubMed  Google Scholar 

  20. 20.

    Kight CR, Swaddle JP (2011) How and why environmental noise impacts animals: an integrative, mechanistic review. Ecol Lett 14:1052–1061. https://doi.org/10.1111/j.1461-0248.2011.01664.x

    Article  PubMed  Google Scholar 

  21. 21.

    Ellis RD, McWhorter TJ, Maron M (2012) Integrating landscape ecology and conservation physiology. Landsc Ecol 27:1–12. https://doi.org/10.1007/s10980-011-9671-6

    Article  Google Scholar 

  22. 22.

    Blickley JL, Word KR, Krakauer AH et al (2012) Experimental chronic noise is related to elevated fecal corticosteroid metabolites in Lekking male greater sage-grouse (Centrocercus urophasianus). PLoS One 7. https://doi.org/10.1371/journal.pone.0050462

  23. 23.

    Elnif J, Sangild PT (1996) The role of glucocorticoids in the growth of the digestive tract in mink (Mustela vison). Comp Biochem Physiol - A Physiol 115:37–42. https://doi.org/10.1016/0300-9629(95)02137-X

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Potvin DA, MacDougall-Shackleton SA (2015) Experimental chronic noise exposure affects adult song in zebra finches. Anim Behav 107:201–207. https://doi.org/10.1016/j.anbehav.2015.06.021

    Article  Google Scholar 

  25. 25.

    Senzaki M, Yamaura Y, Francis CD, Nakamura F (2016) Traffic noise reduces foraging efficiency in wild owls. Sci Rep 6:30602. https://doi.org/10.1038/srep30602

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Phillips JN, Ruef SK, Garvin CM, le MLT, Francis CD (2019) Background noise disrupts host–parasitoid interactions. R Soc Open Sci 6:190867. https://doi.org/10.1098/rsos.190867

    Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Archie EA, Tung J (2015) Social behavior and the microbiome. Curr Opin Behav Sci 6:28–34. https://doi.org/10.1016/j.cobeha.2015.07.008

    Article  Google Scholar 

  28. 28.

    Partecke J, Schwabl I, Gwinner E (2006) Stress and the city: urbanization and its effects on the stress physiology in European blackbirds. Ecology 87:1945–1952. https://doi.org/10.1890/0012-9658(2006)87[1945:SATCUA]2.0.CO;2

    Article  PubMed  Google Scholar 

  29. 29.

    Godon JJ, Arulazhagan P, Steyer JP, Hamelin J (2016) Vertebrate bacterial gut diversity: size also matters. BMC Ecol 16:1–9. https://doi.org/10.1186/s12898-016-0071-2

    Article  Google Scholar 

  30. 30.

    Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3:213–223. https://doi.org/10.1016/j.chom.2008.02.015

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Meillère A, Brischoux F, Angelier F (2015) Impact of chronic noise exposure on antipredator behavior: an experiment in breeding house sparrows. Behav Ecol 26:569–577. https://doi.org/10.1093/beheco/aru232

    Article  Google Scholar 

  32. 32.

    Grossinger RM, Striplen CJ, Askevold RA, Brewster E, Beller EE (2007) Historical landscape ecology of an urbanized California valley: wetlands and woodlands in the Santa Clara Valley. Landsc Ecol 22:103–120. https://doi.org/10.1007/s10980-007-9122-6

    Article  Google Scholar 

  33. 33.

    Berlow M, Kohl KD, Derryberry EP (2019) Evaluation of non-lethal gut microbiome sampling methods in a passerine bird. Ibis (Lond 1859) ibi.12807. https://doi.org/10.1111/ibi.12807

  34. 34.

    Phillips JN, Gentry KE, Luther DA, Derryberry EP (2018) Surviving in the city: higher apparent survival for urban birds but worse condition on noisy territories. Ecosphere 9:1–12. https://doi.org/10.1002/ecs2.2440

    Article  Google Scholar 

  35. 35.

    Bolnick DI, Snowberg LK, Hirsch PE, Lauber CL, Org E, Parks B, Lusis AJ, Knight R, Caporaso JG, Svanbäck R (2014) Individual diet has sex-dependent effects on vertebrate gut microbiota. Nat Commun 5:4500. https://doi.org/10.1038/ncomms5500

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Pyle P (1997) Identification guide to north American birds

  37. 37.

    Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891. https://doi.org/10.1111/j.1600-0706.2009.17643.x

    Article  Google Scholar 

  38. 38.

    Brumm H (2004) The impact of environmental noise on song amplitude in a territorial bird. J Anim Ecol 73:434–440. https://doi.org/10.1002/elps.200500921

  39. 39.

    Vo ATE, Jedlicka JA (2014) Protocols for metagenomic DNA extraction and Illumina amplicon library preparation for faecal and swab samples. Mol Ecol Resour 14:1183–1197. https://doi.org/10.1111/1755-0998.12269

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N, Owens SM, Betley J, Fraser L, Bauer M, Gormley N, Gilbert JA, Smith G, Knight R (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624. https://doi.org/10.1038/ismej.2012.8

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodríguez AM, Chase J, Cope EK, da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu YX, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson II MS, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vázquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, Wan Y, Wang M, Warren J, Weber KC, Williamson CHD, Willis AD, Xu ZZ, Zaneveld JR, Zhang Y, Zhu Q, Knight R, Caporaso JG (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 37(8):852–857. https://doi.org/10.1038/s41587-019-0209-9

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Rosen MJ, Callahan BJ, Fisher DS, Holmes SP (2012) Denoising PCR-amplified metagenome data. BMC Bioinformatics:13. https://doi.org/10.1186/1471-2105-13-283

  43. 43.

    Price MN, Dehal PS, Arkin AP (2010) FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. https://doi.org/10.1371/journal.pone.0009490

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  44. 44.

    McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J 6:610–618. https://doi.org/10.1038/ismej.2011.139

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60

    Article  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Chao A, Chiu C-H, Jost L (2014) Unifying species diversity, phylogenetic diversity, functional diversity, and related similarity and differentiation measures through hill numbers. Annu Rev Ecol Evol Syst 45:297–324. https://doi.org/10.1146/annurev-ecolsys-120213-091540

    Article  Google Scholar 

  47. 47.

    Jost L (2009) Partitioning diversity into independent alpha and beta components. Ecology 90:3593

    Article  Google Scholar 

  48. 48.

    Team RDC, R Development Core Team R (2016) R: a language and environment for statistical computing. R Found Stat Comput. https://doi.org/10.1007/978-3-540-74686-7

  49. 49.

    Mazerolle M (2019) Model selection and multimodel inference based on (Q)AIC(c) version 2.2-2 date. 1–212

  50. 50.

    Wickham H (2009) ggplot2 : Elegant graphics for data analysis. Book 35:211. https://doi.org/10.1007/978-0-387-98141-3

    Article  Google Scholar 

  51. 51.

    Lozupone C, Knight R (2005) UniFrac : a new phylogenetic method for comparing microbial communities UniFrac : a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235. https://doi.org/10.1128/AEM.71.12.8228

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Oksanen J (2015) Vegan: community ecology package. R package version 2.4–3. https://CRANR-project.org/package=vegan. https://doi.org/10.1038/sj.leu.2402722

  53. 53.

    Hubálek Z (2004) An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis 40:639–659. https://doi.org/10.7589/0090-3558-40.4.639

    Article  PubMed  Google Scholar 

  54. 54.

    Knutie SA, Chaves JA, Gotanda KM (2019) Human activity can influence the gut microbiota of Darwin’s finches in the Galapagos Islands. Mol Ecol 28:2441–2450. https://doi.org/10.1111/mec.15088

    Article  PubMed  Google Scholar 

  55. 55.

    Hsu T, Joice R, Vallarino J et al (2016) Urban transit system microbial communities differ by surface type and interaction with humans and the environment. mSystems 1:e00018-16. https://doi.org/10.1128/mSystems.00018-16

    Article  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Price T (1987) Diet Variation in a Population of Darwin ’ s Finches. 68:1015–1028

  57. 57.

    Kohl KD, Brun A, Magallanes M, Brinkerhoff J, Laspiur A, Acosta JC, Caviedes-Vidal E, Bordenstein SR (2017) Gut microbial ecology of lizards: insights into diversity in the wild, effects of captivity, variation across gut regions and transmission. Mol Ecol 26:1175–1189. https://doi.org/10.1111/mec.13921

    Article  PubMed  Google Scholar 

  58. 58.

    Wilderman PR, Jang HH, Malenke JR, Salib M, Angermeier E, Lamime S, Dearing MD, Halpert JR (2014) Functional characterization of cytochromes P450 2B from the desert woodrat Neotoma lepida. Toxicol Appl Pharmacol 274:393–401. https://doi.org/10.1016/j.taap.2013.12.005

    CAS  Article  PubMed  Google Scholar 

  59. 59.

    Dehler CE, Secombes CJ, Martin SAM (2017) Environmental and physiological factors shape the gut microbiota of Atlantic salmon parr (Salmo salar L.). Aquaculture 467:149–157. https://doi.org/10.1016/j.aquaculture.2016.07.017

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Ambrosini R, Corti M, Franzetti A, Caprioli M, Rubolini D, Motta VM, Costanzo A, Saino N, Gandolfi I (2019) Cloacal microbiomes and ecology of individual barn swallows. FEMS Microbiol Ecol 95:1–13. https://doi.org/10.1093/femsec/fiz061

    CAS  Article  Google Scholar 

Download references


We would like to thank a number of undergraduates who helped collect data in the field and lab for this project, especially Siyang Hu, Leanne Norden, and Nicole Moody. We thank Dr. James Fordyce for his extensive help with analyses. We also thank the members of the UTK writing workshop group for help with our manuscript, particularly Jonathan Dickey for sharing his data analysis scripts. This study was supported in part by funding from the Ecology and Evolutionary Biology Department at Tulane University, Newcomb Scholars Grant to L. Norden, and a National Science Foundation award to EPD (NSF IOS 1827290).

Author information



Corresponding author

Correspondence to Mae Berlow.

Electronic supplementary material


(XLSX 45 kb)


(DOCX 14052 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Berlow, M., Phillips, J.N. & Derryberry, E.P. Effects of Urbanization and Landscape on Gut Microbiomes in White-Crowned Sparrows. Microb Ecol 81, 253–266 (2021). https://doi.org/10.1007/s00248-020-01569-8

Download citation


  • Gut microbiome
  • Urbanization
  • Bird
  • Physiology
  • White-crowned sparrow