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Environment and host as large-scale controls of ectomycorrhizal fungi

Nature volume 558, pages 243–248 (2018)Cite this article

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An Author Correction to this article was published on 04 July 2018

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Abstract

Explaining the large-scale diversity of soil organisms that drive biogeochemical processes—and their responses to environmental change—is critical. However, identifying consistent drivers of belowground diversity and abundance for some soil organisms at large spatial scales remains problematic. Here we investigate a major guild, the ectomycorrhizal fungi, across European forests at a spatial scale and resolution that is—to our knowledge—unprecedented, to explore key biotic and abiotic predictors of ectomycorrhizal diversity and to identify dominant responses and thresholds for change across complex environmental gradients. We show the effect of 38 host, environment, climate and geographical variables on ectomycorrhizal diversity, and define thresholds of community change for key variables. We quantify host specificity and reveal plasticity in functional traits involved in soil foraging across gradients. We conclude that environmental and host factors explain most of the variation in ectomycorrhizal diversity, that the environmental thresholds used as major ecosystem assessment tools need adjustment and that the importance of belowground specificity and plasticity has previously been underappreciated.

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Fig. 1: Map of Europe showing sampled level II plots from the United Nations Economic Commission for Europe International Co-operative Programme on Assessment and Monitoring of Air Pollution Effects on Forests (UNECE ICP Forests).
Fig. 2: Krona chart of taxonomic affiliation of ectomycorrhizas and their relative abundance.
Fig. 3: Variation-partitioning Venn diagram.
Fig. 4: Threshold indicator taxa analyses.

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Change history

  • 04 July 2018

    In the HTML version of this Article, author ‘Filipa Cox’ had no affiliation in the author list, although she was correctly associated with affiliation 3 (Earth & Environmental Sciences, University of Manchester, Manchester, UK) in the PDF. In addition, the blue circles for ‘oak’ were missing from Extended Data Fig. 1. These errors have been corrected online.

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Acknowledgements

We acknowledge funding from NERC grant NE/K006339/1 to M.I.B. and C.D.L.O. Analysis was partly based on the ICP Forests PCC Database (http://icp-forests.net). ICP Forests FSCC provided the first level II soil survey data. ICP Forests PCC and observers, technicians and scientists performed long-term sampling, analyses and environmental data handling largely funded by national institutions and ministries, supported by governmental bodies, services and landowners, and partially EU-funded under Regulation (EC) No. 2152/2003 (Forest Focus), project LIFE07ENV/D/000218 (FutMon), and through SWETHRO. Co-financing for D.Ž. and T.G. was provided by P4-0107 (RS Higher Education, Science and Technology Ministry). We thank D. Devey and L. Csiba for laboratory assistance; S. Boersma, F. van der Linde, H. van der Linde, J. van der Linde, C. Gonzales, A. Lenz, R. Lenz, S. Wipf, L. Garfoot, B. Spake, W. Rimington, J. Kowal, T. Solovieva, D. Gane, M. Terrington, J. Alden, A. Otway, V. Kemp, M. Edgar, Y. Lin, A. Drew, E. Booth, P. Cachera, R. De-Kayne, J. Downie, A. Tweedy, E. Moratto, E. Ek, P. Helminen, R. Lievonen, P. Närhi, A. Ryynänen, M. Rupel, J. Draing and F. Heun for field and laboratory work; R. Castilho for bioinformatics; K.-H. Larsson, P.-A. Moreau, J. Nuytinck and M. Ryberg for taxonomy; and N. Barsoum, E. Lilleskov, D. Read and T. Kuyper for discussions throughout.

Reviewer information

Nature thanks A. Dahlberg, P. Kennedy, F. Teste and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Author information

Author notes

  1. Sietse van der Linde

    Present address: Forest Research, Alice Holt Lodge, Farnham, UK

Authors and Affiliations

  1. Life Sciences, Imperial College London, Ascot, UK

    Sietse van der Linde, C. David L. Orme, Bonnie Atkinson, Christopher Carroll, Yuxin Zhang & Martin I. Bidartondo

  2. Comparative Plant and Fungal Biology, Royal Botanic Gardens, Kew, London, UK

    Sietse van der Linde, Laura M. Suz, Bonnie Atkinson & Martin I. Bidartondo

  3. Earth & Environmental Sciences, University of Manchester, Manchester, UK

    Filipa Cox

  4. Public Enterprise Sachsenforst, Kompetenzzentrum Wald und Forstwirtschaft, Pirna, Germany

    Henning Andreae

  5. Estonian Environment Agency, Tallinn, Estonia

    Endla Asi

  6. Forest Research, Alice Holt Lodge, Farnham, UK

    Sue Benham & Elena Vanguelova

  7. Nature and Forest Research Institute, Environment and Climate, Geraardsbergen, Belgium

    Nathalie Cools, Bruno De Vos & Arne Verstraeten

  8. Bavarian State Forestry Institute, Freising, Germany

    Hans-Peter Dietrich

  9. Northwest German Forest Research Institute, Göttingen, Germany

    Johannes Eichhorn & Henning Meesenburg

  10. Landesamt für Natur Umwelt und Verbraucherschutz Nordrhein-Westfalen, Recklinghausen, Germany

    Joachim Gehrmann

  11. Slovenian Forestry Institute, Ljubljana, Slovenia

    Tine Grebenc & Daniel Žlindra

  12. Biological Sciences, University of Reading, Reading, UK

    Hyun S. Gweon

  13. Centre for Ecology & Hydrology, Wallingford, UK

    Hyun S. Gweon

  14. IVL Swedish Environmental Research Institute, Stockholm, Sweden

    Karin Hansen

  15. Staatsbetrieb Sachsenforst, Pirna, Germany

    Frank Jacob

  16. Federal Research and Training Centre for Forests, Natural Hazards and Landscape (BFW), Wien, Austria

    Ferdinand Kristöfel

  17. Forest Research Institute, Sękocin Stary, Poland

    Paweł Lech

  18. NARIC Forest Research Institute, Sárvár, Hungary

    Miklós Manninger

  19. Landesforstanstalt M-V BT: FVI, Schwerin, Germany

    Jan Martin

  20. Natural Resources Institute Finland, Oulu, Finland

    Päivi Merilä

  21. Office National des Forêts, Recherche-Développement-Innovation, Fontainebleau, France

    Manuel Nicolas

  22. National Forest Centre, Zvolen, Slovakia

    Pavel Pavlenda

  23. Natural Resources Institute Finland, Rovaniemi, Finland

    Pasi Rautio

  24. WSL Swiss Federal Institute for Forest, Snow and Landscape Research, Birmensdorf, Switzerland

    Marcus Schaub, Anne Thimonier & Peter Waldner

  25. Forschungsanstalt für Waldökologie und Forstwirtschaft, Trippstadt, Germany

    Hans-Werner Schröck

  26. Thünen Institute of Forest Ecosystems, Eberswalde, Germany

    Walter Seidling

  27. Forestry and Game Management Research Institute, Jíloviště, Czech Republic

    Vít Šrámek

  28. Department of Geosciences and Natural Resource Management, University of Copenhagen, Frederiksberg, Denmark

    Iben Margrete Thomsen & Lars Vesterdal

  29. University of Louvain, Earth and Life Institute, Louvain-la-Neuve, Belgium

    Hugues Titeux

  30. Swedish Forest Agency, Jönköping, Sweden

    Sture Wijk

Authors
  1. Sietse van der Linde
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  2. Laura M. Suz
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  3. C. David L. Orme
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  4. Filipa Cox
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  5. Henning Andreae
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  6. Endla Asi
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  7. Bonnie Atkinson
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  8. Sue Benham
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  9. Christopher Carroll
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  10. Nathalie Cools
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  11. Bruno De Vos
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  12. Hans-Peter Dietrich
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  14. Joachim Gehrmann
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  15. Tine Grebenc
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  18. Frank Jacob
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  19. Ferdinand Kristöfel
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  23. Henning Meesenburg
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  32. Anne Thimonier
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  33. Iben Margrete Thomsen
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  38. Peter Waldner
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  39. Sture Wijk
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  40. Yuxin Zhang
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  41. Daniel Žlindra
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  42. Martin I. Bidartondo
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Contributions

M.I.B. conceived the study. S.v.d.L., M.I.B., F.C., L.M.S. and B.A. led most sampling design and fieldwork. S.v.d.L., B.A., L.M.S., F.C., Y.Z. and M.I.B. processed and analysed samples. H.A., E.A., S.B., N.C., B.D.V., H.-P.D., J.E., J.G., T.G., K.H., F.J., F.K., P.L., M.M., J.M., H.M., P.M., M.N., P.P., P.R., M.S., H.-W.S., W.S., V.Š., A.T., I.M.T., H.T., E.V., A.V., L.V., P.W., S.W. and D.Ž. assisted with fieldwork and collected, collated and validated long-term environmental data. S.v.d.L., H.S.G. and C.D.L.O. performed bioinformatics. S.v.d.L., C.D.L.O. and L.M.S. performed data analysis. C.C. summarized literature. S.v.d.L. drafted the manuscript, M.I.B. provided chief contributions, and C.D.L.O. and L.M.S. contributed extensively. All authors wrote and reviewed the manuscript. S.v.d.L., L.M.S., C.D.L.O. and M.I.B. led revision of the manuscript.

Corresponding author

Correspondence to Sietse van der Linde.

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The authors declare no competing interests.

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Extended data figures and tables

Extended Data Fig. 1 Global non-metric multidimensional scaling ordination of community composition.

Plots shown with host trees: brown squares, beech; blue circles, oak; green triangles, pine; yellow diamonds, spruce. Isoclines depict the forest-floor pH and arrows show the direction and strength of correlation of the most-influential environmental variables according to their R2 values (>0.4). A, MAT; B, mean minimum annual air temperature; C, growing season length; D, NH4 throughfall deposition; E, NTFD.

Extended Data Fig. 2 Threshold indicator taxa analyses.

a, c, e, g, Analyses of individual OTU abundances in response to N:PF (a), forest-floor pH (c), KTFD (e) and MAT (g). Black symbols correspond to taxa declining with the increasing variable (z−) and open symbols depict increasing taxa (z+). Symbol size is proportional to magnitude of response (z-score). Horizontal lines represent 5th and 95th quantiles of values resulting in the largest change in taxon z-scores among 1,000 bootstrap replicates. Tree shapes indicate host generalist, conifer- or broad-leaf-specific. b, d, f, h, Community-level output of accumulated z-scores per plot is shown in response to N:PF (b), forest-floor pH (d), KTFD (f) and MAT (h).

Extended Data Fig. 3 Threshold indicator taxa analysis at the genus level.

a, c, e, g, i, Analyses in response to NTFD (a), N:PF (c), forest-floor pH (e), KTFD (g) and MAT (i). Black symbols correspond to taxa that declined with the increasing variable (z−) and open symbols depict increasing taxa (z+). Symbol size is proportional to magnitude of response (z-score). Horizontal lines represent 5th and 95th quantiles of values resulting in the largest change in taxon z-scores among 1,000 bootstrap replicates. b, d, f, h, j, The community-level output of the accumulated z-scores per plot is shown in response to NTFD (b), N:PF (d), forest-floor pH (f), KTFD (h) and MAT (j).

Extended Data Table 1 Envfit results for the environmental variables used in the non-metric multi-dimensional scaling ordination
Full size table
Extended Data Table 2 Observed and expected frequencies of hyphae and rhizomorph presence
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Extended Data Table 3 Effects of key variables on hyphal plasticity
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Extended Data Table 4 Effects of key variables on rhizomorph plasticity
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Extended Data Table 5 Effects of key variables on hyphal and rhizomorph presence on the total ectomycorrhizal community
Full size table

Supplementary information

Supplementary Figure 1

This file contains an html5 file with an interactive version of the Krona chart in Figure 2.

Reporting Summary

Supplementary Tables

This file contains Supplementary Tables 1-2. Supplementary Table 1 contains a summary of recent large scale biogeograhical ectomycorrhiza publications and Supplementary Table 2 contains a summary of the variables measured on the ICP Forests Level II plots, that were used in this study.

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van der Linde, S., Suz, L.M., Orme, C.D.L. et al. Environment and host as large-scale controls of ectomycorrhizal fungi. Nature 558, 243–248 (2018). https://doi.org/10.1038/s41586-018-0189-9

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