Abstract

Island biogeography has traditionally focused primarily on abiotic drivers of colonization, extinction and speciation. However, establishment on islands could also be limited by biotic drivers, such as the absence of symbionts. Most plants, for example, form symbioses with mycorrhizal fungi, whose limited dispersal to islands could act as a colonization filter for plants. We tested this hypothesis using global-scale analyses of ~1.4 million plant occurrences, including ~200,000 plant species across ~1,100 regions. We find evidence for a mycorrhizal filter (that is, the filtering out of mycorrhizal plants on islands), with mycorrhizal associations less common among native island plants than native mainland plants. Furthermore, the proportion of native mycorrhizal plants in island floras decreased with isolation, possibly as a consequence of a decline in symbiont establishment. We also show that mycorrhizal plants contribute disproportionately to the classic latitudinal gradient of plant species diversity, with the proportion of mycorrhizal plants being highest near the equator and decreasing towards the poles. Anthropogenic pressure and land use alter these plant biogeographical patterns. Naturalized floras show a greater proportion of mycorrhizal plant species on islands than in mainland regions, as expected from the anthropogenic co-introduction of plants with their symbionts to islands and anthropogenic disturbance of symbionts in mainland regions. We identify the mycorrhizal association as an overlooked driver of global plant biogeographical patterns with implications for contemporary island biogeography and our understanding of plant invasions.

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Data availability

The data used in this manuscript are available on request (GIFT and GloNAF databases). The GloNAF database has been published and available for use at https://esajournals.onlinelibrary.wiley.com/doi/abs/10.1002/ecy.2542. The code for plotting data from GIFT is available at https://github.com/BioGeoMacro/GIFT-export. All family mycorrhizal proportion data are available in Supplementary Table 2, and data summarizing the proportions of mycorrhizal and non-mycorrhizal species per region are supplied in Supplementary Table 4.

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Acknowledgements

We acknowledge W. Jetz, D. Sax, A. Mehring and M. Heard for introducing us to collaborators, and S. Queenborough for statistical support at the start of the project. We also acknowledge support from the US NSF (DEB-1556664 to J.D.B., P.S. and C.S.D.), National Geographical Society (WW-036ER-17 to C.S.D.), German DFG (MvK: project 264740629; MW project FZT 118), Czech Centre of Excellence Plant Diversity Analysis and Synthesis Centre (14–36079G to J.P. and P.P.), Czech Academy of Sciences (RVO 67985939 to J.P. and P.P.) and Austrian Science Foundation (I2086B16 to F.E.).

Author information

Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, KS, USA

    • Camille S. Delavaux
    • , Peggy Schultz
    •  & James D. Bever
  2. Kansas Biological Survey, University of Kansas, Lawrence, KS, USA

    • Camille S. Delavaux
    •  & James D. Bever
  3. Department of Biodiversity, Macroecology and Biogeography, University of Goettingen, Göttingen, Germany

    • Patrick Weigelt
    • , Christian König
    •  & Holger Kreft
  4. Department of Biosciences, University of Durham, Durham, UK

    • Wayne Dawson
  5. Departamento de Ciencias de la Vida, Universidad de las Fuerzas Armadas ESPE, Sangolquí, Ecuador

    • Jessica Duchicela
  6. Division of Conservation Biology, Vegetation and Landscape Ecology, University of Vienna, Vienna, Austria

    • Franz Essl
  7. Department of Biology, University of Konstanz, Konstanz, Germany

    • Mark van Kleunen
    •  & Anke Stein
  8. Zhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou University, Taizhou, China

    • Mark van Kleunen
  9. Institute of Botany, Department of Invasion Ecology, Czech Academy of Sciences, Průhonice, Czech Republic

    • Jan Pergl
    •  & Petr Pyšek
  10. Department of Ecology, Faculty of Science, Charles University, Prague, Czech Republic

    • Petr Pyšek
  11. German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany

    • Petr Pyšek
    •  & Marten Winter
  12. Centre of Biodiversity and Sustainable Land Use, University of Goettingen, Göttingen, Germany

    • Holger Kreft

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Contributions

C.S.D. and J.D.B. designed the study. C.S.D. and J.D.B. led the statistical analysis and writing, with continued contributions from P.W. and H.K. C.S.D. collected all of the mycorrhizal data. All other authors collected the remaining plant and environmental data and edited the manuscript.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Camille S. Delavaux.

Supplementary information

  1. Supplementary Information

    Supplementary Tables 1 and 3, Supplementary Figures 1–7 and Supplementary Note 1

  2. Reporting Summary

  3. Supplementary Table 2

    Plant family with assigned corresponding AMF status and reference(s) cited. This table specifies consensus proportions of known plants within each family that are either mycorrhizal, non-mycorrhizal or ambiguous (AMNM). This is done first for each reference separately and then as an average (used in this study) across available references for each mycorrhizal status.

  4. Supplementary Table 4

    Summary of proportions of mycorrhizal and non-mycorrhizal species per region for both native and naturalized plant species. Proportions of mycorrhizal and non-mycorrhizal species within native and naturalized species per region along with the latitude and longitude of the regions’ mass centroids before subsetting or exclusion of zero count data.

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https://doi.org/10.1038/s41559-019-0823-4