The greater bioavailability of nitrogen (N), phosphorus (P) and potassium (K) in the Anthropocene has strongly impacted terrestrial plant communities. In northwest Europe, because high N deposition is considered the main driver of plant diversity loss, European Union (EU) legislation to reduce N deposition is expected to promote plant species recovery. However, this expectation is simplistic: it ignores the role of other macronutrients. Analysing the relationship between plant species pools and species stoichiometric niches along nutrient gradients across northern Eurasia’s herbaceous ecosystems, we found that both absolute and relative P availability are more critical than N or K availability. This result is consistent with stoichiometric niche theory, and with findings from studies of hyperdiverse forests and shrublands at lower latitudes. We show that ecosystems with low absolute and relative P availability harbour a unique set of threatened species that have narrower nutrient-based niche widths than non-threatened species. Such ecosystems represent a conservation priority, but may be further threatened by latent effects of relative P enrichment arising from reduction of N availability without simultaneous reduction of P. The narrow focus of EU legislation on reducing N, but not P, may therefore inadvertently increase the threat to many of Europe’s already threatened plant species. An EU Phosphate Directive is needed.
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Source data underlying this manuscript can be accessed from the Yoda Data Repository of Utrecht University at https://doi.org/10.24416/UU01-I815KS. The data available include the plot data of nutrient concentrations and ratios and calculated species pools using Beal’s smoothing index, as used in Fig. 1 and Extended Data Figs. 1 and 2 (https://geo.public.data.uu.nl/vault-npk-plants/Supplementary_Data_Wassen_et_al_2020_Nat_Ecol_Evol/original/plot_data_Fig_1&Ext_Data_Fig_1_2.csv), the species data of niches (median and variance of nutrient contents and nutrient ratios of species recorded in all plots of occurrence of that species) and threatened status of all species used in Fig. 2 and Extended Data Fig. 3 (estimates using the species pool method) (https://geo.public.data.uu.nl/vault-npk-plants/Supplementary_Data_Wassen_et_al_2020_Nat_Ecol_Evol/original/species_data_Fig_2&Ext_Data_Fig_3.csv), the number of niches captured in Fig. 3 (https://geo.public.data.uu.nl/vault-npk-plants/Supplementary_Data_Wassen_et_al_2020_Nat_Ecol_Evol/original/niche_number_data_Fig_3.csv), the species data (median and variance of nutrient contents and nutrient ratios of species recorded in all plots of occurrence of that species) and threatened status of all species used in Extended Data Figs. 7 and 8 (using observed species occurrences) (https://geo.public.data.uu.nl/vault-npk-plants/Supplementary_Data_Wassen_et_al_2020_Nat_Ecol_Evol/original/species_data_Ext_Data_Fig_7_8.csv) and the generalized addition model statistical parameters estimated from generalized linear mixed-effect models (Gaussian distribution) used in Fig. 1 (https://geo.public.data.uu.nl/vault-npk-plants/Supplementary_Data_Wassen_et_al_2020_Nat_Ecol_Evol/original/GAM_Parameter_Fig_1.csv).
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We thank N. Hölzel, E. Jabłonska, W. Kotowski, P. Pawlikowski and H. Olde Venterink for permission to use their data, I. Roeling and W. Ozinga for help with organizing and analysing the data, T. Markus for improving the figures, P. de Ruiter for proofreading and J. Burrough for author editing.
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Extended Data Fig. 1 Plots showing the difference between estimated species pool size and observed species number (pool minus observed) for each plot in the dataset, along all the absolute and relative nutrient gradients considered.
Differences are shown for all species (purple) and all threatened species (red). Regression lines are estimates obtained using generalized additive models, with standard errors of model estimates indicated as grey bands. Solid lines indicate significant smoothing factors. Light grey rectangles indicate ranges of nutrient limitation derived from thresholds given in the literature: a, N limitation when N < 14 mg g−1; b, P limitation when P < 1 mg g−1; c, K limitation when K < 8 mg g−1. d, N limitation relative to P occurs when N/P < 13.5; N and P co-limitation when 13.5 ≤ N/P ≤ 16 (dark grey); P limitation relative to N when N/P > 16 (grey); e, K limitation relative to N when N/K > 2.1; f, P limitation relative to K when K/P > 3.4 (see Methods for definitions of nutrient limitations).
Extended Data Fig. 2 Observed species numbers for 673 herbaceous vegetation plots in northern Eurasia, counting all species (purple) or all threatened species (red) for each plot along nutrient gradients.
The figure follows the same layout as Fig. 1 of the main text and reveals the same species richness patterns across the absolute and relative nutrient gradients. Regression lines are estimates obtained using generalized additive models, with standard errors of model estimates indicated as grey bands. Solid lines indicate significant smoothing factors. Light grey rectangles indicate ranges of nutrient limitation derived from thresholds given in the literature: a, N limitation when N < 14 mg g−1; b, P limitation when P < 1 mg g−1; c, K limitation when K < 8 mg g−1. d, N limitation relative to P occurs when N/P < 13.5; N and P co-limitation when 13.5 ≤ N/P ≤ 16 (dark grey); P limitation relative to N when N/P > 16 (grey); e, K limitation relative to N when N/K > 2.1; f, P limitation relative to K when K/P > 3.4 (see Methods for definitions of nutrient limitations).
Extended Data Fig. 3 Boxplots of niche widths of non-threatened (purple) and threatened species (red). Niche widths of threatened species are significantly smaller for all nutrient gradients (significance levels: **: P ≤ 0.01; ***: P ≤ 0.001).
Boxplots show median, upper and lower quartiles and whiskers indicate the upper and lower quartiles plus or minus 1.5 times the interquartile range. Data points considered outliers are indicated by dots. Niche width was calculated using the variance of the species along the nutrient gradients (nutrient ratios were log-transformed). Species were included in the analyses if at least 10 data points were obtained (yielding n = 330 species).
N:P ratio of the aboveground biomass plotted against P concentration in mg g−1 dry weight (a) and N concentration in mg g−1 dry weight (b). The dotted line in a) indicates the N:P ratios expected if N:P is solely determined by the variation in P concentration (that is if N equals the average N of the full dataset) and the dotted line in b) indicates the N:P ratios expected if N:P is solely determined by the variation in N concentration (that is if P equals the average P of the full dataset).
The letters indicate the following regions: a, Poolewe, Scotland (n=12 plots); b, Noord-Holland, Netherlands (n = 125); c, Zuid-Holland, Netherlands (n = 60); d, Noordwest Overijssel, Netherlands (n = 48); e, Dommel catchment, Netherlands (n = 54); f, Zwarte Beek catchment, Belgium (n=20); g, Upper Rhine area, Germany (n=43); h, Bavarian Alpine foothills (n=47); i, Degerö Stormyr, Sweden (n=16); j, Kampinowska, Poland (n=38); k, Rospuda valley, Poland (n=41); l, Biebrza catchment, Poland (n=76); m, Neman valley downstream, Belarus (n=5); Neman valley upstream, Belarus (n=5); o, Ob valley, Siberia (n=51); p, Great Vasyugan mire, Siberia (n=32).
Extended Data Fig. 6 Ordination diagram based on a Detrended Correspondence Analysis (DCA) of the species composition of the species pool (based on co-occurrence analysis) of 673 herbaceous vegetation plots in northern Eurasia.
Scaling focused on inter-sample distances, so plots with similar species composition cluster together. Different symbols indicate different geographical locations (as indicated in the legend). The main nutrient gradients, as indicated by absolute and relative nutrient availabilities, were plotted as supplementary variables and are indicated by black arrows. The cumulative variance in species composition explained by the first 4 axes was 32.4%. Axis 1 explained 18.8% of the variance, axis 2 explained an additional 7.5%. The supplementary variables accounted for 15.6% of the variation in species composition.
Extended Data Fig. 7 Observed plant species occurrences along nutrient gradients, distinguishing between non-threatened (purple) and threatened species (red).
Left-hand panels (a, c, e, g, i and k): each boxplot indicates one species. The species median is indicated by the line in the middle of the bars. Species bars correspond to the upper and lower quartiles. Right-hand panels (b, d, f, h, j and l): Boxplots indicate that threatened species had their niche optimum at significantly lower absolute P availability, and at significantly higher N:P ratios (significance level: n.s.: non-significant; *: P ≤ 0.05; **: P < 0.01). Right-hand panels (b, d, f, h, j and l): boxplots show median, upper and lower quartiles and whiskers indicate the upper and lower quartiles plus or minus 1.5 times the interquartile range. Species were included in the analyses if they occurred in at least 10 plots (yielding n = 250 species). Grey backgrounds indicate nutrient limitation ranges. Numbers of species with their niche optimum in nutrient-limited conditions (light grey backgrounds): 97 for N limitation (a), 10 for P limitation (c) and 22 for K limitation (e). Species counts of niche optima were also conducted along relative nutrient gradients. Along the N/P gradient, 146 species had a niche optimum in the N-limited regime (g; no grey background), 85 species in the P-limited regime (g; grey background), and 19 species in the N and P co-limitation regime (g; dark grey background). Along the N/K gradient, 9 species had a niche optimum in the K-limited regime (i). Along the K/P gradient, 244 species had a niche optimum in the P-limited regime (k). Species counts are based on the median of all plot nutrient values or ratios in which the given species occurred. See Methods for definitions of nutrient limitations.
Extended Data Fig. 8 Boxplots of niche widths of non-threatened (purple) and threatened species (red).
Niche widths were calculated not by the species pool method described in the main text but from observed species occurrences in plots and have been used in the corresponding Extended Data Fig. 3. Similar to the results shown in Extended Data Fig. 3, niche widths of threatened species are significantly narrower for all nutrient gradients (significance levels: **: P ≤ 0.01; ***: P ≤ 0.001). Boxplots show median, upper and lower quartiles and whiskers indicate the upper and lower quartiles plus or minus 1.5 times the interquartile range. Data points considered outliers are indicated by dots. Niche width was calculated using the variance of the species along the nutrient gradients (nutrient ratios were log-transformed). Species were included in the analyses if they occurred in at least 10 plots of the dataset (yielding n = 250 species).
Extended Data Fig. 9 Species pool sizes of all species and all threatened species (left-hand panel), and the proportion of threatened species in the total pool (right-hand panel), calculated using the criterion that all species occur on at least two national Red Lists.
The criterion used was that all species occur on at least two national Red Lists, unlike Fig. 1 of the main text where we used the criterion that species occur on at least one national Red List.
Extended Data Fig. 10 Estimated plant species niches, distinguishing between non-threatened (purple) and threatened species (red) and sorted by niche optimum along nutrient gradients using the criterion that all species occur on at least two national Red Lists.
The criterion used was that all species occur on at least two national Red Lists, unlike Fig. 2 of the main text where we used the criterion that species occur on at least one national Red List. Left-hand panels: each bar indicates one species. The species median is indicated by the line in the middle of the bars. Species bars correspond to the upper and lower quartiles. Right-hand panels: Boxplots show median, upper and lower quartiles and whiskers indicate the upper and lower quartiles plus or minus 1.5 times the interquartile range. (significance levels: *: P ≤ 0.1; ***: P ≤ 0.001).
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Wassen, M.J., Schrader, J., van Dijk, J. et al. Phosphorus fertilization is eradicating the niche of northern Eurasia’s threatened plant species. Nat Ecol Evol 5, 67–73 (2021). https://doi.org/10.1038/s41559-020-01323-w
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