Abstract
Ecological models predict that the effects of mammalian herbivore exclusion on plant diversity depend on resource availability and plant exposure to ungulate grazing over evolutionary time. Using an experiment replicated in 57 grasslands on six continents, with contrasting evolutionary history of grazing, we tested how resources (mean annual precipitation and soil nutrients) determine herbivore exclusion effects on plant diversity, richness and evenness. Here we show that at sites with a long history of ungulate grazing, herbivore exclusion reduced plant diversity by reducing both richness and evenness and the responses of richness and diversity to herbivore exclusion decreased with mean annual precipitation. At sites with a short history of grazing, the effects of herbivore exclusion were not related to precipitation but differed for native and exotic plant richness. Thus, plant species’ evolutionary history of grazing continues to shape the response of the world’s grasslands to changing mammalian herbivory.
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Data availability
The data presented in the current study and R code used to analyse the data are available in the Environmental Data Initiative (EDI) repository with the identifier https://doi.org/10.6073/pasta/96436e301c9578230a0fa851ea13af77. The WorldClim database (v.1.4) is available at http://www.worldclim.org/bioclim. Source data are provided with this paper.
Code availability
R code to reproduce all statistical analyses is available in the EDI repository with the identifier https://doi.org/10.6073/pasta/96436e301c9578230a0fa851ea13af77.
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Acknowledgements
This work was generated using data from the Nutrient Network (http://www.nutnet.org) experiment, funded at the site scale by individual researchers. Author contributions are detailed in the ‘Author contributions’ section and Supplementary Table 9; Supplementary Table 10 lists all data contributors who are not authors. Coordination and data management have been supported by funding to E.T.B and E.W.S. from the National Science Foundation Research Coordination Network (NSF-DEB-1042132) and Long-Term Ecological Research (NSF-DEB-1234162 and NSF-DEB-1831944 to Cedar Creek LTER) programmes and the Institute on the Environment (DG-0001-13). Soil analyses were supported, in part, by USDA-ARS grant no. 58-3098-7-007 to E.T.B. We also thank the Minnesota Supercomputer Institute for hosting project data and the Institute on the Environment for hosting Network meetings. J.S. was supported by The Research Foundation Flanders (FWO), grant no. 12N2618N. I.C.B. and I.S.J. were supported by University of Iceland Research Fund (2015), Soil Conservation Service of Iceland and Orkurannsóknasjóður Landsvirkjunnar (NÝR-09-2017, NÝR-14-2018, NÝR-12-2019). P.T. acknowledges C. Silvoso, C. Molina and S. Campana for field assistance, the familia Bordeu for allowing long-term research on their property and Agro Servicios Pampeanos A.S. for providing the fertilizers. S.M.P. thanks G. Wiehl for assistance with data collection, D. and M. French for supporting the Mt Caroline NutNet site on their property and support through the Terrestrial Ecosystems Research Network (TERN) Great Western Woodlands Supersite. C.A.A. thanks A. Rivero, K. Brinsko, J. Garrett, H. Lee and Agroecology Research Interns for field and laboratory support. L.S.L. thanks F. and S. Papel e Celulose for field support. R.L.M. thanks J. Nelson and E. Carlisle for field support. M.C.C. acknowledges Companhia das Lezirias for hosting the site and Fundação para a Ciência e Tecnologia (FCT) funding for the Forest Research Centre (CEF) (UID/00239/2020). G.M.W. thanks B. Tamayo for technical assistance and Bush Heritage Australia for hosting the site on their property. This is publication no. 7387 of the Netherlands Institute of Ecology (NIOO-KNAW) and KBS contribution 2315.
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Contributions
J.N.P. and J.S. developed and framed research questions, analysed the data and wrote the paper. T.O. and P.T. developed and framed research questions and contributed to data analyses. C.S.B, S.M.P. and E.S.B. developed and framed research questions and established and managed the grazing history database. E.W.S. and E.T.B. developed and framed research questions and coordinate the Nutrient Network collaboration. S.B. contributed to analyses. J.N.P., J.S., C.S.B., E.W.S., E.T.B., S.M.P., E.S.B., A.S.M., L.Y., D.S.G., H.O.V., I.C.B., P.G., C.A.A., J.D.B., D.M.B., E.H.B., L.A.B., M.N.B., M.W.C., M.C.C., C.R.D., I.D., S.G., Y.H., I.S.J., L.S.L., R.L.M., J.L.M., S.A.P., A.C.R., M.S., R.S., C.J.S., G.F.V., R.V. and G.M.W. contributed data. All authors contributed to paper writing.
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Extended data
Extended Data Fig. 1 Effect of herbivore exclusion and fertilization on plant diversity, richness and evenness.
Effect of herbivore exclusion (+H: herbivores present; −H: herbivores excluded) and fertilization (+F: fertilized with NPKμ; −F: unfertilized) on (a) plant diversity (b) richness and (c) evenness in sites with a long or short evolutionary history of grazing. Shown are sample points and bars representing means ± 1 SE (n = 76 for long-history sites and n = 103 for short-history sites per bar). Different letters indicate significant differences among the treatment means based on LMMs with herbivore exclusion and fertilization as fixed factors, and block nested within site as random effect.
Extended Data Fig. 2 Herbivore exclusion effects on plant richness related to changes in light availability.
Relationship between the LRR of light availability to herbivore exclusion and the LRR of native (orange points) and exotic (grey points) species richness to herbivore exclusion. Sites had a long or short evolutionary history of grazing and included unfertilized control plots and plots fertilized with NPKµ. Per plant provenance category, n = 119 for long-history sites and n = 182 for short-history sites. For native richness, there was a significant linear regression in both long- (P = 0.0008, R2 = 0.08) and short-history sites (P = 0.0004, R2 = 0.06), so trendlines were produced using geom_smooth (ggplot2 package in R). The coloured bands represent the 95% confidence intervals.
Extended Data Fig. 3 Relationship between grazing intensity and herbivore exclusion effects on plant diversity, richness and evenness.
Relationship between the log-transformed grazing intensity index and the LRR of (a) plant diversity, (b) richness and (c) evenness to herbivore exclusion (ln(fence/control)) in sites with a long (n = 20) or short (n = 23) evolutionary history of grazing. Sites included unfertilized control plots (green points) and plots fertilized with NPKµ (purple points). Trendlines were added when there were significant linear regressions between the LRRs and the grazing index and were produced using geom_smooth (ggplot2 package in R) regardless of fertilization, as this experimental treatment did not have a significant effect. The coloured bands represent the 95% confidence intervals.
Extended Data Fig. 4 Relationship between grazing intensity and herbivore exclusion effects on native and exotic plant richness.
Relationship between the log-transformed grazing intensity index and the LRR of native (orange points) and exotic (grey points) species richness to herbivore exclusion (ln(fence/control)) in sites with a long (n = 20) or short (n = 23) evolutionary history of grazing. A significant linear regression was found for exotic species richness in short-history sites and a trendline was produced using geom_smooth (ggplot2 package in R). The coloured band represents the 95% confidence intervals.
Extended Data Fig. 5 Relationship between productivity and herbivore exclusion on light availability.
Relationship between the LRR of light availability to herbivore exclusion and (a) mean annual precipitation and (b) aboveground plant biomass in sites with a long (n = 119) or short (n = 182) evolutionary history of grazing. Plant biomass is from the fenced ungrazed plots. Sites included unfertilized control plots (green points) and plots fertilized with NPKµ (purple points). Trendlines were added when there were significant linear regressions between the LRRs and the aboveground plant biomass and were produced using geom_smooth (ggplot2 package in R). The coloured bands represent the 95% confidence intervals.
Supplementary information
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Price, J.N., Sitters, J., Ohlert, T. et al. Evolutionary history of grazing and resources determine herbivore exclusion effects on plant diversity. Nat Ecol Evol 6, 1290–1298 (2022). https://doi.org/10.1038/s41559-022-01809-9
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DOI: https://doi.org/10.1038/s41559-022-01809-9
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