Grassland biodiversity bounces back from long-term nitrogen addition

Abstract

The negative effect of increasing atmospheric nitrogen (N) pollution on grassland biodiversity is now incontrovertible1,2,3. However, the recent introduction of cleaner technologies in the UK has led to reductions in the emissions of nitrogen oxides, with concomitant decreases in N deposition4. The degree to which grassland biodiversity can be expected to ‘bounce back’ in response to these improvements in air quality is uncertain, with a suggestion that long-term chronic N addition may lead to an alternative low biodiversity state5. Here we present evidence from the 160-year-old Park Grass Experiment at Rothamsted Research, UK6, that shows a positive response of biodiversity to reducing N addition from either atmospheric pollution or fertilizers. The proportion of legumes, species richness and diversity increased across the experiment between 1991 and 2012 as both wet and dry N deposition declined. Plots that stopped receiving inorganic N fertilizer in 1989 recovered much of the diversity that had been lost, especially if limed. There was no evidence that chronic N addition has resulted in an alternative low biodiversity state on the Park Grass plots, except where there has been extreme acidification, although it is likely that the recovery of plant communities has been facilitated by the twice-yearly mowing and removal of biomass. This may also explain why a comparable response of plant communities to reduced N inputs has yet to be observed in the wider landscape.

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Figure 1: Changes in atmospheric N deposition, pH and proportion of legumes on the limed and unlimed sub-plots of the Park Grass nil plot.
Figure 2: Change in N concentration measured on archived herbage samples taken from Park Grass sub-plot 3d between 1960 and 2012 that has never received any external inputs of lime or fertilizer.
Figure 3: Historical trends in Simpson’s plant diversity index between 1910 and 2012 for unlimed and limed sub-plots.
Figure 4: Temporal trends in plant communities, between 1991 and 2012, on selected Park Grass plots.

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Acknowledgements

We thank the large teams of people who were involved in the vegetation sampling and sorting between 1991 and 2012, and J. Lepš and P. Šmilauer for their advice on the multivariate analysis. Park Grass is supported by the UK Biotechnology and Biological Sciences Research Council (BBSRC) and the Lawes Agricultural Trust. The wet N deposition (precipitation chemistry) data set for 1992–2013 was provided courtesy of the UK Environmental Change Network (ECN). I.H.K. was supported by Deutsche Forschungsgemeinschaft (DFG SCHN 557/5-1).

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J.S., M.J.C. A.J.M., P.R.P. and T.S. co-ordinated and contributed to the vegetation sampling between 1991 and 2012. T.S. and K.W.T.G. were responsible for collecting and analysing nitrogen deposition data. I.H.K. and H.S. analysed nitrogen limitation of vegetation. J.S. was responsible for the statistical analysis and initial draft of the paper. All authors contributed to the final version.

Corresponding author

Correspondence to J. Storkey.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 The Bray–Curtis dissimilarity index.

ah, The response of Bray–Curtis dissimilarity for all sub-plots on plot 9 (ad) and plot 14 (eh). Community data from 1992–2012 have been compared to samples taken in 1991 for the transition plots (filled circles) and plots that continue to receive inorganic N fertilizer (open circles). Lines indicate a significant fit for a rectangular hyperbola function; where separate lines have been fitted in a single panel, a significant difference in the asymptote of the responses was observed.

Extended Data Figure 2 Change in time over the recent sampling period (1991–2012) of species richness, eH, and percentage legumes in the first herbage cut.

ai, Plot 3 (a, d, g), plot 9 (filled circles, 9/1; open circles, 9/2) (b, e, h) and plot 14 (filled circles, 14/1; open circles, 14/2) (c, f, i). The averages of sub-plots a, b and c are presented; sub-plot d was excluded to avoid the confounding effect of very low pH on plot 9/1d allowing a direct comparison between treatments at the main plot level.

Extended Data Figure 3 Comparison of the effect of decreasing atmospheric N inputs and the cessation of N fertilization on plant communities.

a, Partial canonical correspondence analysis (CCA) of the effect of withholding nitrogen fertilizer on plant communities on the transition plots 9/1 and 14/1 compared to the plots that continued to receive N, 9/2 and 14/2. Data from all sub-plots during the modern day sampling period (1991–2012) were used, and year was included as a categorical covariate. b, Partial CCA of the temporal response of plant communities on all sub-plots sampled during the modern day period, 1991–2012, excluding the transition plots 9/1 and 14/1, with year entered as a continuous variable and plot as a covariate. In both ordination plots, species were only included if they were in the top 20 species ranked by their weighting in the CCA and had a P value indicating their association with the constrained axis of <0.1. Agrca, Agrostis capillaris; Alopr, Alopecurus pratensis; Antsy, Anthriscus sylvestris; Arrel, Arrhenatherum elatius; Conma, Conopodium majus; Dacgl, Dactylis glomerata; Hersp, Heracleum sphondylium; Latpr, Lathyrus pratensis; Plala, Plantago lanceolata; Poapr, Poa pratensis; Poatr, Poa trivialis; Ranac, Racunculus acris; Rumac, Rumex acetosa; Trapr, Tragopogon pratense; Tripr, Trifolium pratense.

Extended Data Table 1 pH (in water) measured on soil cores, 0–23 cm, on seven occasions between 1991 and 2012
Extended Data Table 2 Species richness and eH observed in a total sample area of 0.75 m2 averaged over three biomass samples taken in 1991–1993 and 2010–2012
Extended Data Table 3 GLMs fitted to relative biomass data from the Park Grass nil plot, which has never received any external inputs of lime or fertilizer
Extended Data Table 4 Effect of declining N deposition (measured either as a 3- or 5-year moving average), pH and N or P fertilizers on metrics of plant diversity
Extended Data Table 5 GLMs fitted to relative biomass data from the Park Grass plot 9 (N2PKNaMg)
Extended Data Table 6 GLMs fitted to relative biomass data from the Park Grass plot 14, (N*2PKNaMg)
Extended Data Table 7 Significant responses of individual species to year at the level of the sub-plot

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Storkey, J., Macdonald, A., Poulton, P. et al. Grassland biodiversity bounces back from long-term nitrogen addition. Nature 528, 401–404 (2015). https://doi.org/10.1038/nature16444

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