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The importance of species addition ‘versus’ replacement varies over succession in plant communities after glacier retreat

Nature Plants volume 10, pages 256–267 (2024)Cite this article

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Abstract

The mechanisms underlying plant succession remain highly debated. Due to the local scope of most studies, we lack a global quantification of the relative importance of species addition ‘versus’ replacement. We assessed the role of these processes in the variation (β-diversity) of plant communities colonizing the forelands of 46 retreating glaciers worldwide, using both environmental DNA and traditional surveys. Our findings indicate that addition and replacement concur in determining community changes in deglaciated sites, but their relative importance varied over time. Taxa addition dominated immediately after glacier retreat, as expected in harsh environments, while replacement became more important for late-successional communities. These changes were aligned with total β-diversity changes, which were more pronounced between early-successional communities than between late-successional communities (>50 yr since glacier retreat). Despite the complexity of community assembly during plant succession, the observed global pattern suggests a generalized shift from the dominance of facilitation and/or stochastic processes in early-successional communities to a predominance of competition later on.

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Fig. 1: Sampling design.
Fig. 2: β-diversity components obtained with eDNA and traditional methods.
Fig. 3: Patterns of β-diversity components over plant succession following glacier retreat.
Fig. 4: Proportion of early colonizers, persisters and late colonizers in glacier forelands.

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Data availability

Raw sequence data (Sper01 marker) generated using the protocols described in the ‘Methods’ section are deposited in the ‘Sper01_raw_sequences.zip’ folder available in Zenodo (https://zenodo.org/record/6620359#.Y8E1OP6ZO5d)95. The data that support the findings of this study are provided as Supplementary Tables 1–3.

Code availability

Scripts for reproducing the results in this study are available as Supplementary codes.

Supplementary Code 1. Code reproducing bioinformatics steps.

Supplementary Code 2. Code reproducing taxonomic assignation.

Supplementary Code 3. R code for the MOTU filtering after bioinformatic analyses to remove sequences with best identity <90% and detected at a low frequency that can be artefacts produced by PCR, contaminants and sequencing errors.

Supplementary Code 4. R code to calculate beta-diversity and its components, run the main models and illustrate results.

Supplementary Code 5. R code to test the ability of our sampling design to detect breakpoints in segmented regressions.

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Acknowledgements

This study was funded by the European Research Council under the European Community’s Horizon 2020 Programme, Grant Agreement no. 772284 (IceCommunities) to I.C., A.C., A.G., S.M., A.B., R.A., R.S.A., F.G., L.G., N.K., G.A.D., J.P., W.T., M.C. and G.F.F. This research was also funded by Biodiversa+, the European Biodiversity Partnership under the 2021–2022 BiodivProtect joint call for research proposals, co-funded by the European Commission (grant agreement no. 101052342 ‘PrioritIce-Vanishing habitats: conservation priorities for glacier-related biodiversity threatened by climate change’) to I.C., R.A., W.T., M.C., M.G. and G.F.F. and with the funding organizations MUR and ANR. We thank R. Kaufmann, A. Guisan, K. Sieron and M. A. Morales-Martínez for help and discussions at various phases of this project.

Author information

Author notes

  1. Deceased: Justiniano Alejo Cochachín Rapre.

Authors and Affiliations

  1. Dipartimento di Scienze e Politiche Ambientali, Università degli Studi di Milano, Milano, Italy

    Isabel Cantera, Alexis Carteron, Alessia Guerrieri, Silvio Marta, Aurélie Bonin, Roberto Ambrosini, Roberto Sergio Azzoni, Fabrizio Gili, Guglielmina Adele Diolaiuti & Gentile Francesco Ficetola

  2. Université de Toulouse, Ecole d’Ingénieurs de Purpan, UMR INRAE-INPT DYNAFOR, Toulouse, France

    Alexis Carteron

  3. Argaly, Bâtiment CleanSpace, Sainte-Hélène-du-Lac, France

    Alessia Guerrieri & Aurélie Bonin

  4. Institute of Geosciences and Earth Resources, CNR, Pisa, Italy

    Silvio Marta

  5. Laboratory AMAP, IRD, University of Montpellier, CIRAD, CNRS, INRA, Montpellier, France

    Fabien Anthelme

  6. Dipartimento di Scienze della Terra ‘Ardito Desio’, Milano, Italy

    Roberto Sergio Azzoni, Chiara Compostella & Andrea Zerboni

  7. Department of Soil and Physical Sciences, Lincoln University, Lincoln, New Zealand

    Peter Almond

  8. Departamento de Ciencias Biológicas y Biodiversidad, Universidad de Los Lagos, Osorno, Chile

    Pablo Alviz Gazitúa

  9. INRAE, UR RIVERLY, Centre de Lyon-Villeurbanne, Villeurbanne, France

    Sophie Cauvy-Fraunié

  10. Instituto de Hidrología, Meteorología y Estudios Ambientales IDEAM, Bogotá, Colombia

    Jorge Luis Ceballos Lievano

  11. Department of Geography, School of Environment and Earth Sciences, Central University of Punjab, VPO- Ghudda, Bathinda, Punjab, India

    Pritam Chand

  12. Centre for the Study of Regional Development - School of Social Sciences, Jawaharlal Nehru University, New Delhi, India

    Milap Chand Sharma

  13. Department of Earth Sciences, Simon Fraser University, Burnaby, British Columbia, Canada

    John Clague

  14. Área de Evaluación de Glaciares y Lfagunas, Autoridad Nacional del Agua, Huaraz, Peru

    Justiniano Alejo Cochachín Rapre & Rolando Cruz Encarnación

  15. CEFE, Univ Montpellier, CNRS, EPHE, IRD, Univ Paul Valéry Montpellier 3, Montpellier, France

    Olivier Dangles & Jerome Poulenard

  16. Mannaki Whenua - Landcare Research, Soils and Landscapes, Lincoln, New Zealand

    Andre Eger

  17. Institute of Water Problems and Hydro-Energy, Kyrgyz National Academy of Sciences, Bishkek, Kyrgyzstan

    Sergey Erokhin & Nurai Urseitova

  18. Department of Earth and Environmental Sciences (DISAT), - University of Milano-Bicocca, Milano, Italy

    Andrea Franzetti & Francesca Pittino

  19. Univ. Grenoble Alpes, Univ. Savoie Mont Blanc, CNRS, LECA, Grenoble, France

    Ludovic Gielly, Pierre Taberlet, Wilfried Thuiller & Gentile Francesco Ficetola

  20. Department of Life Sciences and Systems Biology, University of Turin, Turin, Italy

    Fabrizio Gili

  21. Research and Museum Collections Office, Climate and Ecology Unit, MUSE-Science Museum, Trento, Italy

    Mauro Gobbi

  22. Faculty of Environmental Sciences and Natural Resource Management (INA), Norwegian University of Life Sciences, Ås, Norway

    Sigmund Hågvar

  23. UiT – The Arctic University of Norway, Tromsø Museum, Tromsø, Norway

    Sigmund Hågvar & Pierre Taberlet

  24. Univ. Savoie Mont Blanc, Univ. Grenoble Alpes, EDYTEM, Chambéry, France

    Norine Khedim

  25. Herbario Nacional de Bolivia: La Paz, La Paz, Bolivia

    Rosa Isela Meneses

  26. Universidad Católica del Norte, Antofagasta, Chile

    Rosa Isela Meneses

  27. Department of Civil and Environmental Engineering, University of the Andes, Bogotá, Colombia

    Gwendolyn Peyre

  28. Univ. Grenoble Alpes, CNRS, IRD, Grenoble-INP, Institut des Géosciences de l’Environnement (IGE, UMR 5001), Grenoble, France

    Antoine Rabatel

  29. Institute of Mountain Hazards and Environment, Chinese Academy of Sciences, Chengdu, China

    Yan Yang

  30. Mountain Societies Research Institute, University of Central Asia, Bishkek, Kyrgyzstan

    Vitalii Zaginaev

  31. Department of Geography and the Environment, University of Texas at Austin, Austin, TX, USA

    Anaïs Zimmer

  32. Dipartimento di Bioscienze, Università degli Studi di Milano, Milano, Italy

    Marco Caccianiga

Authors
  1. Isabel Cantera
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  2. Alexis Carteron
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  3. Alessia Guerrieri
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Contributions

I.C., M.C. and G.F.F. conceived, developed and wrote the paper, with input from A.C., R. A., F.A., S.C.-F., M.G., A.R., A. Zerboni, P.T., J.P. and W.T.; I.C. performed the statistical analyses; A.G., S.M., A.B., F.G. and G.F.F. contributed to data preparation and curation; A.G., A.B. and L.G. performed laboratory analyses; A.G., S.M., A.B., R.A., F.A., R.S.A., P.A., P.A.G., S.C.-F., J.L.C.L, P.C., M.C.S., J.C., J.A.C.R., C.C., R.C.E., O.D., A.E., S.E., A.F., L.G., F.G., M.G, S.H., N.K., R.I.M., G.P., F.P., A.R., N.U., Y.Y., V.Z., A. Zerboni, A. Zimmer, G.A.D., J.P. M.C. and G.F.F. participated in sampling and the initial development of the study. All authors reviewed and/or provided input on the manuscript.

Corresponding author

Correspondence to Isabel Cantera.

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The authors declare no competing interests.

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Nature Plants thanks Ingolf Kühn, Robert Junker and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Patterns of β-diversity and its components over time measured with temporal data to support the conclusions based on the chronosequence approach.

Data was obtained from Fickert & Grüninger94, which sampled vascular plants with traditional methods in permanent plots during the first decade after the deglaciation of two glaciers in the Alps (N = 30 comparisons). a. β-diversity components. Boxplots indicate median (middle line), 25th, 75th percentiles (box), as well as 1.5 * interquartile range (whiskers) and outliers (dots). Diamonds indicate the mean values. b. Results of the Bayesian generalized mixed models assessing the effects of mean age and age differences between compared sites on the different β-diversity measures. Glacier identity and identity of sites involved in the comparisons were included as random factors. Parameters with 95% CI non-overlapping zero are highlighted in bold.

Supplementary information

Supplementary Information

Supplementary Tables 1–8 and Figs. 1–11.

Reporting Summary

Supplementary Table 1

Supplementary Tables 1–3, with legends indicated in the Supplementary information file ‘Cantera_SI.pdf’.

Supplementary Code 1

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Supplementary Code 2

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Supplementary Code 3

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Cantera, I., Carteron, A., Guerrieri, A. et al. The importance of species addition ‘versus’ replacement varies over succession in plant communities after glacier retreat. Nat. Plants 10, 256–267 (2024). https://doi.org/10.1038/s41477-023-01609-4

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