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Empirical support for the biogeochemical niche hypothesis in forest trees

Nature Ecology & Evolution volume 5, pages 184–194 (2021)Cite this article

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Abstract

The possibility of using the elemental compositions of species as a tool to identify species/genotype niche remains to be tested at a global scale. We investigated relationships between the foliar elemental compositions (elementomes) of trees at a global scale with phylogeny, climate, N deposition and soil traits. We analysed foliar N, P, K, Ca, Mg and S concentrations in 23,962 trees of 227 species. Shared ancestry explained 60–94% of the total variance in foliar nutrient concentrations and ratios whereas current climate, atmospheric N deposition and soil type together explained 1–7%, consistent with the biogeochemical niche hypothesis which predicts that each species will have a specific need for and use of each bio-element. The remaining variance was explained by the avoidance of nutritional competition with other species and natural variability within species. The biogeochemical niche hypothesis is thus able to quantify species-specific tree niches and their shifts in response to environmental changes.

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Fig. 1: Phylogenetic diagram of foliar N concentration (percentage of dry weight) (25,112 datapoints) in the phylogenetic tree.
Fig. 2: Phylogenetic diagram of foliar P concentration (percentage of dry weight) (25,112 datapoints) in the phylogenetic tree.
Fig. 3: Phylogenetic diagram of foliar N/P ratio (25,112 datapoints) in the phylogenetic tree.
Fig. 4: Phylogenetic diagram of PC1 scores (25,112 datapoints) in the phylogenetic tree.
Fig. 5: Plot of the first two roots of functional discriminant analysis using P. pinaster, P. halepensis, Q. ilex, Q. petraea and Q. robur as dependent categorical grouping factors, and foliar N, P, K, S, Ca and Mg concentrations and pairwise ratios as continuous independent variables.
Fig. 6: Plot of PCA cases and variables superimposed, defined by the first two components of the PCA, with foliar N, P, K, Ca, Mg and S concentrations as variables and with soil orders as cases.

Data availability

All data are available at the Global Ecology Unit CREAF-CSIC-UAB (glonuteco.creaf.cat/data/).

Code availability

All code is available at the Global Ecology Unit CREAF-CSIC-UAB (glonuteco.creaf.cat/data/).

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Acknowledgements

The authors thank the European Research Council Synergy (grant no. ERC-SyG-2013-610028 IMBALANCE-P), the Spanish Government (grant no. PID2019-110521GB-I00) and the Catalan Government (grant no. SGR 2017-1005). M.F.-M. is a postdoctoral fellow of the Research Foundation–Flanders.

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Authors and Affiliations

  1. CSIC, Global Ecology Unit CREAF-CEAB-UAB, Bellaterra, Spain

    Jordi Sardans, Helena Vallicrosa, Paolo Zuccarini, Gerard Farré-Armengol, Guille Peguero, Albert Gargallo-Garriga & Josep Peñuelas

  2. CREAF, Cerdanyola del Vallès, Spain

    Jordi Sardans, Helena Vallicrosa, Paolo Zuccarini, Gerard Farré-Armengol, Guille Peguero, Albert Gargallo-Garriga & Josep Peñuelas

  3. PLECO (Plants and Ecosystems), Department of Biology, University of Antwerp, Wilrijk, Belgium

    Marcos Fernández-Martínez & Ivan A. Janssens

  4. Laboratoire des Sciences du Climat et de l’Environnement, IPSL, Gif-sur-Yvette, France

    Philippe Ciais

  5. International Institute for Applied Systems Analysis (IIASA), Ecosystems Services and Management, Laxenburg, Austria

    Michael Obersteiner

  6. Terrestrial Ecosystem Research, Department of Microbiology and Ecosystem Science, University of Vienna, Vienna, Austria

    Andreas Richter

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  1. Jordi Sardans
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Contributions

J.S. and J.P. conceived, designed and supervised the project. J.S., H.V., I.A.J., J.P. and P.Z. searched the bibliography and gathered data. J.S., H.V., P.Z., M.F.-M., A.R., P.C., M.O., I.A.J. and J.P. checked the data and contributed to data accuracy selection. J.S., H.V., G.F.-A., J.P. and M.F.-M. developed the statistical analyses. J.S., J.P., M.F.-M., H.V. and G.F.-A. created the tables and figures. J.S. wrote the paper. J.P., H.V., G.P., A.G.-G., M.F.-M., G.F.-A., A.R., P.C., M.O. and I.A.J. revised the manuscript. All authors read and revised the final version of the manuscript.

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Correspondence to Jordi Sardans.

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Extended data

Extended Data Fig. 1 Map of plot situation.

Map of the plot locations.

Extended Data Fig. 2 Phylogenetic diagram of foliar K concentration.

Phylogenetic diagrams of the foliar K concentration (25 112 datapoints) along the phylogeny tree obtained by using function phylosig of the package phytools in R (Revell59) representing the value structure used to estimate phylogenetic signal in the different variables. The function contmap estimates the ancestral characters at internal nodes using maximum likelihood and assuming Brownian motion as a model for trait evolution (Felsenstein63), and then interpolates ancestral condition along the branches of the tree (Revell64).

Extended Data Fig. 3 Phylogenetic diagram of foliar S concentration.

Phylogenetic diagrams of the foliar S concentration (25 112 datapoints) along the phylogeny tree obtained by using function phylosig of the package phytools in R (Revell59) representing the value structure used to estimate phylogenetic signal in the different variables. The function contmap estimates the ancestral characters at internal nodes using maximum likelihood and assuming Brownian motion as a model for trait evolution (Felsenstein63), and then interpolates ancestral condition along the branches of the tree (Revell64).

Extended Data Fig. 4 Phylogenetic diagram of foliar Ca concentration.

Phylogenetic diagrams of the foliar Ca concentration (25 112 datapoints) along the phylogeny tree obtained by using function phylosig of the package phytools in R (Revell59) representing the value structure used to estimate phylogenetic signal in the different variables. The function contmap estimates the ancestral characters at internal nodes using maximum likelihood and assuming Brownian motion as a model for trait evolution (Felsenstein63), and then interpolates ancestral condition along the branches of the tree (Revell64).

Extended Data Fig. 5 Phylogenetic diagram of foliar Mg concentration.

Phylogenetic diagrams of the foliar Mg concentration (25 112 datapoints) along the phylogeny tree obtained by using function phylosig of the package phytools in R (Revell59) representing the value structure used to estimate phylogenetic signal in the different variables. The function contmap estimates the ancestral characters at internal nodes using maximum likelihood and assuming Brownian motion as a model for trait evolution (Felsenstein63), and then interpolates ancestral condition along the branches of the tree (Revell64).

Extended Data Fig. 6 Foliar N, P and K concentrations of the trees growing on different soil types.

Foliar N, P and K concentrations (Mean ± S.E., % dry weight) (25 112 datapoints) of the trees growing on different soil types. Different letters represent significantly (P<0.005) disticnt values among different soil types (Soil Taxonomy soil Orders) analyzed using Bayesian phylogenetic linear mixed models with soil orders as fixed effects using the MCMCglmm package66 in R.

Extended Data Fig. 7 Foliar N/P, N/K and P/K concentrations ratios of the trees growing on different soil types.

Foliar N/P, N/K and P/K concentrations ratio (Mean ± S.E) (25 112 datapoints) of the trees growing on different soil types. Different letters represent significantly (P<0.005) disticnt values among different soil types (Soil Taxonomy soil Orders) analyzed using Bayesian phylogenetic linear mixed models with soil orders as fixed effects using the MCMCglmm package66 in R.

Extended Data Fig. 8 European area of distribution and distribution area overlap.

Representation of the European area of distribution and distribution area overlap with the corresponding sampled sites by the ICP Forest iniciative of Picea abies and Quercus robur (A), Abies alba and Quercus petraea (B) and Pinus sylvestris and Fagus sylvativa (C).

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Sardans, J., Vallicrosa, H., Zuccarini, P. et al. Empirical support for the biogeochemical niche hypothesis in forest trees. Nat Ecol Evol 5, 184–194 (2021). https://doi.org/10.1038/s41559-020-01348-1

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