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:

Mycorrhizal fungi influence global plant biogeography

Nature Ecology & Evolution volume 3, pages 424–429 (2019)Cite this article

Subjects

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.

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

Similar content being viewed by others

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.

References

  1. MacArthur, R. H. & Wilson, E. The Theory of Island Biogeography (Princeton Univ. Press, Princeton, 1967).

  2. Losos, J. B. & Schluter, D. Analysis of an evolutionary species–area relationship. Nature 408, 847–850 (2000).

    CAS  PubMed  Google Scholar 

  3. Kisel, Y. & Barraclough, T. G. Speciation has a spatial scale that depends on levels of gene flow. Am. Nat. 175, 316–334 (2010).

    PubMed  Google Scholar 

  4. Borregaard, M. K. et al. Oceanic island biogeography through the lens of the general dynamic model: assessment and prospect. Biol. Rev. 92, 830–853 (2017).

    PubMed  Google Scholar 

  5. Kreft, H., Jetz, W., Mutke, J., Kier, G. & Barthlott, W. Global diversity of island floras from a macroecological perspective. Ecol. Lett. 11, 116–127 (2008).

    PubMed  Google Scholar 

  6. Weigelt, P., Steinbauer, M. J., Cabral, J. S. & Kreft, H. Late Quaternary climate change shapes island biodiversity. Nature 532, 99–102 (2016).

    CAS  PubMed  Google Scholar 

  7. Whittaker, R. J., Triantis, K. A. & Ladle, R. J. A general dynamic theory of oceanic island biogeography. J. Biogeogr. 35, 977–994 (2008).

    Google Scholar 

  8. Losos, J. B. & Ricklefs, R. E. The theory of Island Biogeography Revisited (Princeton Univ. Press, Princeton, 2009).

  9. Onstein, R. E. et al. Frugivory-related traits promote speciation of tropical palms. Nat. Ecol. Evol. 1, 1903–1911 (2017).

    PubMed  Google Scholar 

  10. Fukami, T. Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu. Rev. Ecol. Evol. Syst. 46, 1–23 (2015).

    Google Scholar 

  11. Bever, J. D., Westover, K. M. & Antonovics, J. Incorporating the soil community into plant population dynamics: the utility of the feedback approach. Ecology 85, 561–573 (1997).

    Google Scholar 

  12. Van der Heijden, M. G., Bardgett, R. D. & van Straalen, N. M. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol. Lett. 11, 296–310 (2008).

    PubMed  Google Scholar 

  13. Delavaux, C. S., Smith‐Ramesh, L. M. & Kuebbing, S. E. Beyond nutrients: a meta‐analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils.Ecology 98, 2111–2119 (2017).

    PubMed  Google Scholar 

  14. Redecker, D., Kodner, R. & Graham, L. E. Glomalean fungi from the Ordovician. Science 289, 1920–1921 (2000).

    CAS  PubMed  Google Scholar 

  15. Maherali, H. et al. Mutualism persistence and abandonment during the evolution of the mycorrhizal symbiosis. Am. Nat. 188, E113–E125 (2016).

    PubMed  Google Scholar 

  16. Smith, S. E. & Read, D. J. Mycorrhizal Symbiosis (Academic Press, Oxford, UK, 2008).

  17. Davison, J. et al. Hierarchical assembly rules in arbuscular mycorrhizal (AM) fungal communities. Soil Biol. Biochem. 97, 63–70 (2016).

    CAS  Google Scholar 

  18. Dickie, I. A. et al. The emerging science of linked plant–fungal invasions. New Phytol. 215, 1314–1332 (2017).

    CAS  PubMed  Google Scholar 

  19. Miller, R. M., Smith, C. I., Jastrow, J. D. & Bever, J. D. Mycorrhizal status of the genus Carex (Cyperaceae). Am. J. Bot. 86, 547–553 (1999).

    CAS  PubMed  Google Scholar 

  20. Brundrett, M. C. Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320, 37–77 (2009).

    CAS  Google Scholar 

  21. Tedersoo, L. Biogeography of Mycorrhizal Symbiosis Vol. 230 (Springer, Cham, Switzerland, 2017).

  22. Brundrett, M. C. & Tedersoo, L. Evolutionary history of mycorrhizal symbioses and global host plant diversity.New Phytol. 220, 1108–1115 (2018).

    PubMed  Google Scholar 

  23. Lambers, H., Raven, J. A., Shaver, G. R. & Smith, S. E. Plant nutrient-acquisition strategies change with soil age. Trends Ecol. Evol. 23, 95–103 (2008).

    Google Scholar 

  24. Jiang, S. et al. Dynamics of arbuscular mycorrhizal fungal community structure and functioning along a nitrogen enrichment gradient in an alpine meadow ecosystem.New Phytol. 220, 1222–1235 (2018).

    PubMed  Google Scholar 

  25. Abbott, K. C. et al. Spatial heterogeneity in soil microbes alters outcomes of plant competition. PLoS ONE 10, e0125788 (2015).

    PubMed  PubMed Central  Google Scholar 

  26. Steidinger, B. S. & Bever, J. D. The coexistence of hosts with different abilities to discriminate against cheater partners: an evolutionary game-theory approach. Am. Nat. 183, 762–770 (2014).

    PubMed  Google Scholar 

  27. Davison, J. et al. Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349, 970–973 (2015).

    CAS  PubMed  Google Scholar 

  28. Tedersoo, L. et al. Global diversity and geography of soil fungi. Science 346, 1256688 (2014).

    PubMed  Google Scholar 

  29. Peay, K. G., Schubert, M. G., Nguyen, N. H. & Bruns, T. D. Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol. Ecol. 21, 4122–4136 (2012).

    PubMed  Google Scholar 

  30. Peay, K. G. Timing of mutualist arrival has a greater effect on Pinus muricata seedling growth than interspecific competition. J. Ecol. 106, 514–523 (2018).

    Google Scholar 

  31. Koziol, L. et al. The plant microbiome and native plant restoration: the example of native mycorrhizal fungi.BioScience 68, 996–1006 (2018).

    Google Scholar 

  32. Richardson, D. M., Allsopp, N., D’Antonio, C. M., Milton, S. J. & Rejmánek, M. Plant invasions—the role of mutualisms. Biol. Rev. 75, 65–93 (1999).

    Google Scholar 

  33. Callaway, R. M., Thelen, G. C., Rodriguez, A. & Holben, W. E. Soil biota and exotic plant invasion. Nature 427, 731–733 (2004).

    CAS  Google Scholar 

  34. Oehl, F. et al. Impact of land use intensity on the species diversity of arbuscular mycorrhizal fungi in agroecosystems of Central Europe. Appl. Environ. Microbiol. 69, 2816–2824 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Pringle, A. et al. Mycorrhizal symbioses and plant invasions. Annu. Rev. Ecol. Evol. Syst. 40, 699–715 (2009).

    Google Scholar 

  36. Bunn, R. A., Ramsey, P. W. & Lekberg, Y. Do native and invasive plants differ in their interactions with arbuscular mycorrhizal fungi? A meta-analysis. J. Ecol. 103, 1547–1556 (2015).

    CAS  Google Scholar 

  37. Reinhart, K. O., Lekberg, Y., Klironomos, J. & Maherali, H. Does responsiveness to arbuscular mycorrhizal fungi depend on plant invasive status?. Ecol. Evol. 7, 6482–6492 (2017).

    PubMed  PubMed Central  Google Scholar 

  38. Bueno, C. G. et al. Plant mycorrhizal status, but not type, shifts with latitude and elevation in Europe. Glob. Ecol. Biogeogr. 26, 690–699 (2017).

    Google Scholar 

  39. Hillebrand, H. On the generality of the latitudinal diversity gradient. Am. Nat. 163, 192–211 (2004).

    Google Scholar 

  40. Weigelt, P. & Kreft, H. Quantifying island isolation—insights from global patterns of insular plant species richness. Ecography 36, 417–429 (2013).

    Google Scholar 

  41. Koske, R., Gemma, J. & Flynn, T. Mycorrhizae in Hawaiian angiosperms: a survey with implications for the origin of the native flora.Am. J. Bot. 79, 853–862 (1992).

    Google Scholar 

  42. Vellinga, E. C., Wolfe, B. E. & Pringle, A. Global patterns of ectomycorrhizal introductions. New Phytol. 181, 960–973 (2009).

    PubMed  Google Scholar 

  43. Cornelissen, J., Aerts, R., Cerabolini, B., Werger, M. & Van Der Heijden, M. Carbon cycling traits of plant species are linked with mycorrhizal strategy. Oecologia 129, 611–619 (2001).

    CAS  PubMed  Google Scholar 

  44. Powell, J. R., Riley, R. C. & Cornwell, W. Relationships between mycorrhizal type and leaf flammability in the Australian flora. Pedobiologia 65, 43–49 (2017).

    Google Scholar 

  45. Van Kleunen, M. et al. Global exchange and accumulation of non-native plants. Nature 525, 100–103 (2015).

    CAS  PubMed  Google Scholar 

  46. Weigelt, P., König, C. & Kreft, H. GIFT- A Global Inventory of Floras and Traits; https://doi.org/10.1101/535005 (2019).

  47. Van Kleunen, M. et al. Global exchange and accumulation of non-native plants.Nature 525, 100–103 (2015).

    CAS  PubMed  Google Scholar 

  48. Byng, J. W. et al. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 181, 1–20 (2016).

    Google Scholar 

  49. Gerdemann, J. Vesicular-arbuscular mycorrhiza and plant growth. Annu. Rev. Phytopathol. 6, 397–418 (1968).

    Google Scholar 

  50. Karger, D. N. et al. Climatologies at high resolution for the Earth’s land surface areas. Sci. Data 4, 170122 (2017).

    PubMed  PubMed Central  Google Scholar 

  51. Danielson, J. J. & Gesch, D. B. Global Multi-resolution Terrain Elevation Data 2010 (GMTED2010) Report 2331-1258 (US Geological Survey, 2011).

  52. Socioeconomic Data and Applications Center (SEDAC).Gridded Population of the World, (GPW), v3; https://doi.org/10.7927/H4639MPP (Center for International Earth Science Information Network, 2015).

  53. Tuanmu, M. N. & Jetz, W. A global 1‐km consensus land‐cover product for biodiversity and ecosystem modelling. Glob. Ecol. Biogeogr. 23, 1031–1045 (2014).

    Google Scholar 

  54. Kueffer, C. et al. A global comparison of plant invasions on oceanic islands. Perspect. Plant Ecol. Evol. Syst. 12, 145–161 (2010).

    Google Scholar 

  55. Triantis, K. A., Economo, E. P., Guilhaumon, F. & Ricklefs, R. E. Diversity regulation at macro‐scales: species richness on oceanic archipelagos. Glob. Ecol. Biogeogr. 24, 594–605 (2015).

    Google Scholar 

  56. Crase, B., Liedloff, A. C. & Wintle, B. A. A new method for dealing with residual spatial autocorrelation in species distribution models. Ecography 35, 879–888 (2012).

    Google Scholar 

  57. Bivand, R. & Piras, G. Comparing Implementations of Estimation Methods for Spatial Econometrics (American Statistical Association, Alexandria, VA, USA, 2015).

  58. R Core Team. R: A language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria. 2016).

  59. Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

    Google Scholar 

Download references

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

Authors and 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

Authors
  1. Camille S. Delavaux
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patrick Weigelt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wayne Dawson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jessica Duchicela
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Franz Essl
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mark van Kleunen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Christian König
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jan Pergl
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Petr Pyšek
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Anke Stein
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Marten Winter
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Peggy Schultz
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Holger Kreft
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. James D. Bever
    View author publications

    You can also search for this author in PubMed Google Scholar

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.

Corresponding author

Correspondence to Camille S. Delavaux.

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

Reporting Summary

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.

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Delavaux, C.S., Weigelt, P., Dawson, W. et al. Mycorrhizal fungi influence global plant biogeography. Nat Ecol Evol 3, 424–429 (2019). https://doi.org/10.1038/s41559-019-0823-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

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

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

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