Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Community richness of amphibian skin bacteria correlates with bioclimate at the global scale

Nature Ecology & Evolution volume 3, pages 381–389 (2019)Cite this article

Subjects

Abstract

Animal-associated microbiomes are integral to host health, yet key biotic and abiotic factors that shape host-associated microbial communities at the global scale remain poorly understood. We investigated global patterns in amphibian skin bacterial communities, incorporating samples from 2,349 individuals representing 205 amphibian species across a broad biogeographic range. We analysed how biotic and abiotic factors correlate with skin microbial communities using multiple statistical approaches. Global amphibian skin bacterial richness was consistently correlated with temperature-associated factors. We found more diverse skin microbiomes in environments with colder winters and less stable thermal conditions compared with environments with warm winters and less annual temperature variation. We used bioinformatically predicted bacterial growth rates, dormancy genes and antibiotic synthesis genes, as well as inferred bacterial thermal growth optima to propose mechanistic hypotheses that may explain the observed patterns. We conclude that temporal and spatial characteristics of the host’s macro-environment mediate microbial diversity.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

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

Similar content being viewed by others

Data availability

A full description of data analyses is provided in the Supplementary Information. Data for all newly sequenced samples is available on the Short Read Archive (Bioproject PRJNA474496). All figures include associated raw data and there are no restrictions on data availability. Correspondence and requests for materials should be addressed to M.V. or D.C.W.

References

  1. Thompson, L. et al. A communal catalogue reveals Earth’s multiscale microbial diversity. Nature 551, 457–463 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hird, S. M. Evolutionary biology needs wild microbiomes. Front. Microbiol. 8, 1–10 (2017).

    Article  Google Scholar 

  3. Jiménez, R. R. & Sommer, S. The amphibian microbiome: natural range of variation, pathogenic dysbiosis, and role in conservation. Biodivers. Conserv. 26, 763–786 (2016).

    Article  Google Scholar 

  4. Lear, G. et al. Following Rapoport’s Rule: the geographic range and genome size of bacterial taxa decline at warmer latitudes. Environ. Microbiol. 8, 3152–3162 (2017).

    Article  Google Scholar 

  5. Amend, A. S. et al. Macroecological patterns of marine bacteria on a global scale. J. Biogeogr. 40, 800–811 (2013).

    Article  Google Scholar 

  6. Baldwin, A. J. et al. Microbial diversity in a pacific ocean transect from the arctic to antarctic circles. Aquat. Microb. Ecol. 41, 91–102 (2005).

    Article  Google Scholar 

  7. Fuhrman, J. A. et al. A latitudinal diversity gradient in planktonic marine bacteria. Proc. Natl Acad. Sci. USA 105, 7774–7778 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Tedersoo, L. & Nara, K. General latitudinal gradient of biodiversity is reversed in ectomycorrhizal fungi. New Phytol. 185, 351–354 (2010).

    Article  PubMed  Google Scholar 

  9. Ladau, J. et al. Global marine bacterial diversity peaks at high latitudes in winter. ISME. J. 7, 1669–1677 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Milici, M. et al. Low diversity of planktonic bacteria in the tropical ocean. Sci. Rep. 6, 19054 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Fierer, N. & Jackson, R. B. The diversity and biogeography of soil bacterial communities. Proc. Natl Acad. Sci. USA 103, 626–631 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Lozupone, C. A. & Knight, R. Global patterns in bacterial diversity. Proc. Natl Acad. Sci. USA 104, 11436–11440 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Jones, S. E. & Lennon, J. T. Dormancy contributes to the maintenance of microbial diversity. Proc. Natl Acad. Sci. USA 107, 5881–5886 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Crevecoeur, S., Vincent, W. F., Comte, J. & Lovejoy, C. Bacterial community structure across environmental gradients in permafrost thaw ponds: methanotroph-rich ecosystems. Front. Microbiol. 6, 1–15 (2015).

    Article  Google Scholar 

  15. Fierer, N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat. Rev. Microbiol. 15, 579–590 (2017).

    Article  CAS  PubMed  Google Scholar 

  16. Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222–227 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647–1651 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Muegge, B. D. et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970–974 (2012).

    Article  CAS  Google Scholar 

  19. Bletz, M. C. et al. Mitigating amphibian chytridiomycosis with bioaugmentation: characteristics of effective probiotics and strategies for their selection and use. Ecol. Lett. 16, 807–820 (2013).

    Article  PubMed  Google Scholar 

  20. Walke, J. B. & Belden, L. K. Harnessing the microbiome to prevent fungal infections: lessons from amphibians. PLoS Pathog. 12, e1005796 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Fisher, M. C., Garner, T. W. & Walker, S. F. Global emergence of Batrachochytrium dendrobatidis and amphibian chytridiomycosis in space, time, and host. Annu. Rev. Microbiol. 63, 291–310 (2009).

    Article  CAS  PubMed  Google Scholar 

  22. Lips, K. R. et al. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc. Natl Acad. Sci. USA 103, 3165–3170 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Martel, A. et al. Batrachochytrium salamandrivorans sp. nov. causes lethal chytridiomycosis in amphibians. Proc. Natl Acad. Sci. USA 110, 15325–15329 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Martel, A. et al. Recent introduction of a chytrid fungus endangers western palearctic salamanders. Science 6209, 630–631 (2014).

    Article  CAS  Google Scholar 

  25. Stegen, G. et al. Drivers of salamander extirpation mediated by Batrachochytrium salamandrivorans. Nature 544, 353–356 (2017).

    Article  CAS  PubMed  Google Scholar 

  26. McKenzie, V. J., Bowers, R. M., Fierer, N., Knight, R. & Lauber, C. L. Co-habiting amphibian species harbor unique skin bacterial communities in wild populations. ISME. J. 6, 588–596 (2012).

    Article  CAS  PubMed  Google Scholar 

  27. Jani, A. J. & Briggs, C. J. The pathogen Batrachochytrium dendrobatidis disturbs the frog skin microbiome during a natural epidemic and experimental infection. Proc. Natl Acad. Sci. USA 111, E5049–E5058 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kueneman, J. G. et al. The amphibian skin-associated microbiome across species, space and life history stages. Mol. Ecol. 23, 1238–1250 (2014).

    Article  PubMed  Google Scholar 

  29. Bletz, M. C. et al. Host ecology rather than host phylogeny drives amphibian skin microbial community structure in the biodiversity hotspot of Madagascar. Front. Microbiol. 8, Article 1530 (2017).

    Article  PubMed  Google Scholar 

  30. Wolz, M. et al. Effects of host species and environment on the skin microbiome of Plethodontid salamanders. J. Anim. Ecol. 87, 341–353 (2017).

    Article  Google Scholar 

  31. Longo, A. V., Savage, A. E., Hewson, I. & Zamudio, K. R. Seasonal and ontogenetic variation of skin microbial communities and relationships to natural disease dynamics in declining amphibians. R. Soc. Open Sci. 2, 140377 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Sabino-Pinto, J. et al. Temporal changes in cutaneous bacterial communities of terrestrial- and aquatic-phase newts (Amphibia).Environ. Microbiol. 19, 3025–3038 (2017).

    Article  CAS  PubMed  Google Scholar 

  33. Bletz, M. C. et al. Amphibian skin microbiota exhibits temporal variation in community structure but stability of predicted Bd-inhibitory function. ISME. J. 11, 1521–1534 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Becker, M. H., Richards-Zawacki, C. L., Gratwicke, B. & Belden, L. K. The effect of captivity on the cutaneous bacterial community of the critically endangered Panamanian golden frog (Atelopus zeteki). Biol. Conserv. 176, 199–206 (2014).

    Article  Google Scholar 

  35. Becker, C. G.., Longo, A. V., Haddad, C. F. B. & Zamudio, K. R. Land cover and forest connectivity alter the interactions among host, pathogen and skin microbiome.Proc. Biol. Sci. 284, pii: 20170582 (2017).

    Google Scholar 

  36. McKenzie, V. J. et al. The effects of captivity on the mammalian gut microbiome. Integr. Comp. Biol. 57, 690–704 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Agler, M. T. et al. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol. 14, 1–31 (2016).

    Article  CAS  Google Scholar 

  38. Vavre, F. & Kremer, N. Microbial impacts on insect evolutionary diversification: from patterns to mechanisms. Curr. Opin. Insect Sci. 4, 29–34 (2014).

    Article  PubMed  Google Scholar 

  39. Webster, N. S. et al. Host-associated coral reef microbes respond to the cumulative pressures of ocean warming and ocean acidification. Sci. Rep. 6, 19324 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. O’Brien, P. A., Morrow, K. M., Willis, B. & Bourne, D. Implications of ocean acidification for marine microorganisms from the free-living to the host-associated. Front. Mar. Sci 3, 47 (2016).

    Google Scholar 

  41. Longo, A. V. & Zamudio, K. R. Temperature variation, bacterial diversity and fungal infection dynamics in the amphibian skin. Mol. Ecol. 18, 4787–4797 (2017).

    Article  Google Scholar 

  42. Longo, A. V. & Zamudio, K. R. Environmental fluctuations and host skin bacteria shift survival advantage between frogs and their fungal pathogen. ISME. J. 11, 349–361 (2017).

    Article  PubMed  Google Scholar 

  43. Novakova, E. et al. Mosquito microbiome dynamics, a background for prevalence and seasonality of West Nile virus. Front. Microbiol. 8, 526 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Corkrey, R. et al. The biokinetic spectrum for temperature. PLoS ONE. 11, 1–29 (2016).

    Google Scholar 

  45. Roller, B. R., Stoddard, S. F. & Schmidt, T. M. Exploiting rRNA operon copy number to investigate bacterial reproductive strategies. Nat. Microbiol. 18, 386–392 (2015).

    Google Scholar 

  46. Nemergut, D. R. et al. Decreases in average bacterial community rRNA operon copy number during succession. ISME. J. 10, 1147–1156 (2016).

    Article  CAS  PubMed  Google Scholar 

  47. Kerns, P. & Shade, A. Trait-based patterns of microbial dynamics in dormancy potential and heterotrophic strategy: case studies of resource-based and post-press succession.ISME J. 12, 2575–2581 (2018).

    Article  CAS  Google Scholar 

  48. Czaran, T., Hoekstra, R. F. & Pagie, L. Chemical warfare between microbes. PNAS 99, 786–790 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lennon, J. T. & Jones, S. E. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol. 9, 119–130 (2011).

    Article  CAS  PubMed  Google Scholar 

  50. Langille, M. G. et al. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol. 31, 814–821 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Mittelbach, G. G. et al. Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecol. Lett. 10, 315–331 (2007).

    Article  PubMed  Google Scholar 

  52. Wiens, J. J. Global patterns of diversification and species richness in amphibians. Am. Nat. 170, S86–S106 (2007).

    Article  PubMed  Google Scholar 

  53. Prest, T. L., Kimball, A. K., Kueneman, J. G. & McKenzie, V. J. Host‐associated bacterial community succession during amphibian development. Mol. Ecol. 27, 1992–2006 (2018).

    Article  CAS  PubMed  Google Scholar 

  54. Bahram, M. et al. Structure and function of the global topsoil microbiome. Nature 560, 233–237 (2018).

    Article  CAS  PubMed  Google Scholar 

  55. Staddon, W. J., Trevors, J. T., Duchesne, L. C. & Colombo, C. A. Soil microbial diversity and community structure across a climatic gradient in western Canada. Biodivers. Conserv. 7, 1081–1092 (1998).

    Article  Google Scholar 

  56. Loudon, A. H. et al. Microbial community dynamics and effect of environmental microbial reservoirs on red-backed salamanders (Plethodon cinereus). ISME. J. 8, 830–840 (2014).

    Article  CAS  PubMed  Google Scholar 

  57. Walke, J. B. et al. Amphibian skin may select for rare environmental microbes. ISME. J. 8, 2207–2217 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Belden, L. K. et al. Panamanian frog species host unique skin bacterial communities. Front. Microbiol. 6, 1171 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  59. Sabino-Pinto, J. et al. Composition of the cutaneous bacterial community in Japanese amphibians: effects of captivity, host species, and body region.Microb. Ecol. 72, 460–469 (2016).

    Article  PubMed  Google Scholar 

  60. Rebollar, A. A. et al. Skin bacterial diversity of Panamanian frogs is associated with host susceptibility and presence of Batrachochytrium dendrobatidis.ISME J. 10, 1682–1695 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Bagley, S. T. Habitat association of Klebsiella species. Infect. Control. 6, 52–58 (1985).

    Article  CAS  PubMed  Google Scholar 

  62. Locey, K. J., Fisk, M. C. & Lennon, J. T. Microscale insight into microbial seed banks. Front. Microbiol. 7, 2040 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  63. Stubbendieck, R. M., Vargas-Bautista, C. & Straight, P. D. Bacterial communities: interactions to scale. Front. Microbiol. 7, 1–19 (2016).

    Article  Google Scholar 

  64. Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).

    Article  Google Scholar 

  65. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Amir, A. et al. Deblur rapidly resolves single-nucleotide community sequence patterns. mSystems 2, 00191-16 (2017).

  67. Cooper, N., Bielby, J., Thomas, G. H. & Purvis, A. Macroecology and extinction risk correlates of frogs. Glob. Ecol. Biogeogr. 17, 211–221 (2008).

    Article  Google Scholar 

  68. Hedges, S. B., Dudley, J. & Kumar, S. TimeTree: a public knowledge-base of divergence times among organisms. Bioinformatics 22, 2971–2972 (2006).

    Article  CAS  PubMed  Google Scholar 

  69. R Core Team, R: A Language and Environment for Statistical Computing (R Core Team, 2016).

  70. Bates, D. M., Machler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2014).

    Google Scholar 

  71. Lüdecke, D. Data visualization for statistics in social science. R package https://doi.org/10.5281/zenodo.1308157 (2017).

  72. Oksanen, J. et al. vegan: community ecology package. R package V.2, 4–2 (R Core Team, 2017).

  73. Hothorn, T., Hornik, K., Van De Wiel, M. A. & Zeileis, A. Implementing a class of permutation tests: the coin package. J. Stat. Softw. 28, 1–23 (2008).

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by grants of National Science Foundation (DEB-1146284 to V.J.M.; IOS-1121758 to L.R.-S.; DEB-1310036 to A.V.L.), Templeton Foundation to V.J.M., Deutsche Forschungsgemeinschaft (DFG) to M.V. (VE247/9-1), CAPES to M.V. and C.F.B.H., FAPESP (#2013/50741-7) and CNPq to C.F.B.H., Simons Foundation (429440, WTW) to J.G.K., Deutscher Akademischer Austauschdienst (DAAD) to M.C.B., University of Costa Rica (Project 801-B2-029) and Costa Rican Ministry of Science and Technology (849-PINN-2015)-I to J.G.A., the Portuguese National Funds through FCT (Exploratory Research Project: IF/00209/2014/CP1256/CT0011) to A.C. and the National Research Foundation of Korea (2015R1D1A1A01057282) to B.W. We are indebted to M. Kondermann for her assistance with laboratory work, A. Borzee, R. Kakehashi and T. Kosch for their support in sample collection, and the Organization for Tropical Studies, La Selva Biological Station and G. Alvarado for field support in Costa Rica. All new sampling was done with the appropriate permits of national authorities, where required; in Costa Rica, of the Institutional Biodiversity Commission of the University of Costa Rica (Resolution 371 014) and the Costa Rican Ministry of Environment and Energy (Resolution 091-2012-SINAC).

Author information

Author notes

  1. These authors have contributed equally: Jordan G. Kueneman, Molly C. Bletz.

Authors and Affiliations

  1. Smithsonian Tropical Research Institute, Panama City, Republic of Panama

    Jordan G. Kueneman & Douglas C. Woodhams

  2. Department of Biology, University of Massachusetts Boston, Boston, MA, USA

    Molly C. Bletz, Robert Stevenson & Douglas C. Woodhams

  3. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA

    Valerie J. McKenzie, Holly Archer & Ana Lisette Arellano

  4. Department of Biological Sciences, The University of Alabama, Tuscaloosa, AL, USA

    C. Guilherme Becker

  5. Earth Lab, University of Colorado, Boulder, CO, USA

    Maxwell B. Joseph

  6. Center for Research in Microscopic Structures, University of Costa Rica, San José, Costa Rica

    Juan G. Abarca, Adrián Pinto-Tomás, Gabriel Vargas Asensio & Ibrahim Zúñiga Chaves

  7. School of Biological Sciences, Seoul National University, Seoul, South Korea

    Arnaud Bataille & Bruce Waldman

  8. Department of Biology and Chemistry, Liberty University, Lynchburg, VA, USA

    Matthew Becker

  9. Department of Biological Sciences, Virginia Tech, Blacksburg, VA, USA

    Lisa K. Belden & Daniel Medina

  10. CIBIO, Research Centre in Biodiversity and Genetic Resources, Universidade do Porto, Vairao, Portugal

    Angelica Crottini

  11. Department of Genome Analytics, Helmholtz Centre for Infection Research, Braunschweig, Germany

    Robert Geffers & Michael Jarek

  12. Departamento de Zoologia e Centro de Aquicultura, I.B., UNESP, Rio Claro, SP, Brazil

    Célio. F. B. Haddad

  13. Department of Biology, James Madison University, Harrisonburg, VA, USA

    Reid N. Harris

  14. Department of Pathology, Microbiology and Immunology, Vanderbilt University School of Medicine, Nashville, TN, USA

    Whitney M. Holden & Louise Rollins-Smith

  15. Department of Biology, Vassar College, Poughkeepsie, NY, USA

    Myra Hughey

  16. Department of Biology, Tufts University, Medford, MA, USA

    Patrick J. Kearns

  17. Biology Department, University of South Dakota, Vermillion, SD, USA

    Jacob L. Kerby

  18. Department of Biology, University of Copenhagen, and Center for Macroecology, Evolution and Climate Natural History Museum of Denmark, Copenhagen, Denmark

    Jos Kielgast

  19. Department of Bio-Science, Nagahama Institute of Bio-Science and Technology, Nagahama, Japan

    Atsushi Kurabayashi

  20. Amphibian Research Center, Hiroshima University, Higashi-Hiroshima, Japan

    Atsushi Kurabayashi

  21. Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa

    Atsushi Kurabayashi

  22. Department of Biology, University of Florida, Gainesville, FL, USA

    Ana V. Longo

  23. Department of Zoology and Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada

    Andrew Loudon

  24. Conservation and Science, Cleveland Metroparks Zoo, Cleveland, OH, USA

    Andrew Loudon

  25. Institute of Marine and Limnological Sciences, Sciences Faculty, Universidad Austral de Chile, Valdivia, Chile

    José J. Nuñez

  26. School of Marine Sciences, Ruppin Academic Center, Mikhmoret, Israel

    R. G. Bina Perl

  27. Biochemistry Department, School of Medicine; Center for Research in Cell and Molecular Biology and Center for Research in Microscopic Structures, University of Costa Rica, San José, Costa Rica

    Adrián Pinto-Tomás

  28. Department of Animal Biology, University of Antananarivo, Antananarivo, Madagascar

    Falitiana C. E. Rabemananjara

  29. Centro de Ciencias Genómicas, Universidad Nacional Autónoma de México, Cuernavaca, Mexico

    Eria A. Rebollar

  30. Institute of Zoology, Tierärztliche Hochschule Hannover, Hannover, Germany

    Ariel Rodríguez

  31. Thünen Institute of Biodiversity, Braunschweig, Germany

    Christoph C. Tebbe

  32. Department of Integrative Biology, Oklahoma State University, Stillwater, OK, USA

    Bruce Waldman

  33. Department of Biology, Eastern Washington University, Cheney, WA, USA

    Jenifer B. Walke

  34. Conservation and Research Department, Zoo Miami, Miami, FL, USA

    Steven M. Whitfield

  35. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA

    Kelly R. Zamudio

  36. Zoologisches Institut, Technische Universität Braunschweig, Braunschweig, Germany

    Miguel Vences

Authors
  1. Jordan G. Kueneman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Molly C. Bletz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Valerie J. McKenzie
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Guilherme Becker
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Maxwell B. Joseph
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Juan G. Abarca
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Holly Archer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ana Lisette Arellano
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Arnaud Bataille
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Matthew Becker
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Lisa K. Belden
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Angelica Crottini
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Robert Geffers
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Célio. F. B. Haddad
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Reid N. Harris
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Whitney M. Holden
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Myra Hughey
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Michael Jarek
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Patrick J. Kearns
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Jacob L. Kerby
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Jos Kielgast
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Atsushi Kurabayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Ana V. Longo
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Andrew Loudon
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Daniel Medina
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. José J. Nuñez
    View author publications

    You can also search for this author in PubMed Google Scholar

  27. R. G. Bina Perl
    View author publications

    You can also search for this author in PubMed Google Scholar

  28. Adrián Pinto-Tomás
    View author publications

    You can also search for this author in PubMed Google Scholar

  29. Falitiana C. E. Rabemananjara
    View author publications

    You can also search for this author in PubMed Google Scholar

  30. Eria A. Rebollar
    View author publications

    You can also search for this author in PubMed Google Scholar

  31. Ariel Rodríguez
    View author publications

    You can also search for this author in PubMed Google Scholar

  32. Louise Rollins-Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  33. Robert Stevenson
    View author publications

    You can also search for this author in PubMed Google Scholar

  34. Christoph C. Tebbe
    View author publications

    You can also search for this author in PubMed Google Scholar

  35. Gabriel Vargas Asensio
    View author publications

    You can also search for this author in PubMed Google Scholar

  36. Bruce Waldman
    View author publications

    You can also search for this author in PubMed Google Scholar

  37. Jenifer B. Walke
    View author publications

    You can also search for this author in PubMed Google Scholar

  38. Steven M. Whitfield
    View author publications

    You can also search for this author in PubMed Google Scholar

  39. Kelly R. Zamudio
    View author publications

    You can also search for this author in PubMed Google Scholar

  40. Ibrahim Zúñiga Chaves
    View author publications

    You can also search for this author in PubMed Google Scholar

  41. Douglas C. Woodhams
    View author publications

    You can also search for this author in PubMed Google Scholar

  42. Miguel Vences
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

J.G.K., M.C.B., V.J.M., D.C.W. and M.V. conceived the study, coordinated the analyses and wrote the manuscript. J.G.K., M.C.B., D.C.W., G.B. and M.J. designed and performed data analysis. J.G.A., A.B., M.B., L.B., A.C., C.F.B.H., R.N.H., W.H., M.H., J.L.K., J.K., A.K., A.L., A.H.L., D.M., J.J.N., R.G.B.P., A.P.T., F.C.E.R., E.A.R., A.R., L.R.S., G.V.A., B.W., J.B.W., S.M.W., K.Z., I.Z.C. contributed materials and data. H.A., L.A., R.G. and M.J. performed laboratory work. P.J.K., R.S. and C.C.T. contributed to data analysis. All authors contributed to the development and revision of the manuscript.

Corresponding authors

Correspondence to Douglas C. Woodhams or Miguel Vences.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Results, Supplementary Figures 1–12, Supplementary Tables 1–17 and Supplementary References

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kueneman, J.G., Bletz, M.C., McKenzie, V.J. et al. Community richness of amphibian skin bacteria correlates with bioclimate at the global scale. Nat Ecol Evol 3, 381–389 (2019). https://doi.org/10.1038/s41559-019-0798-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-019-0798-1

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology