General destabilizing effects of eutrophication on grassland productivity at multiple spatial scales

Yann Hautier¹, Pengfei Zhang^{2

3

4

5}, Michel Loreau⁶, Kevin R Wilcox⁷, Eric W Seabloom⁸, Elizabeth T Borer⁸, Jarrett E K Byrnes⁹, Sally E Koerner¹⁰, Kimberly J Komatsu¹¹, Jonathan S Lefcheck¹², Andy Hector¹³, Peter B Adler¹⁴, Juan Alberti¹⁵, Carlos A Arnillas¹⁶, Jonathan D Bakker¹⁷, Lars A Brudvig¹⁸, Miguel N Bugalho¹⁹, Marc Cadotte²⁰, Maria C Caldeira²¹, Oliver Carroll²², Mick Crawley²³, Scott L Collins²⁴, Pedro Daleo¹⁵, Laura E Dee²⁵, Nico Eisenhauer^{26

27}, Anu Eskelinen^{26

28

29}, Philip A Fay³⁰, Benjamin Gilbert³¹, Amandine Hansar³², Forest Isbell⁸, Johannes M H Knops³³, Andrew S MacDougall²², Rebecca L McCulley³⁴, Joslin L Moore³⁵, John W Morgan³⁶, Akira S Mori³⁷, Pablo L Peri³⁸, Edwin T Pos², Sally A Power³⁹, Jodi N Price⁴⁰, Peter B Reich^{39

41}, Anita C Risch⁴², Christiane Roscher^{26

43}, Mahesh Sankaran^{44

45}, Martin Schütz⁴², Melinda Smith^{46

47}, Carly Stevens⁴⁸, Pedro M Tognetti⁴⁹, Risto Virtanen²⁹, Glenda M Wardle⁵⁰, Peter A Wilfahrt⁷, Shaopeng Wang⁵¹

Affiliations

¹ Ecology and Biodiversity Group, Department of Biology, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands. y.hautier@uu.nl.
² Ecology and Biodiversity Group, Department of Biology, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands.
³ State Key Laboratory of Grassland and Agro-Ecosystems, School of Life Science, Lanzhou University, 730000, Lanzhou, Gansu Province, People's Republic of China.
⁴ Institute of Eco-Environmental Forensics of Shandong University, 266237, Jinan, Shandong Province, People's Republic of China.
⁵ Ministry of Justice Hub for Research & Practice in Eco-Environmental Forensics, 266237, Qingdao, Shandong Province, People's Republic of China.
⁶ Centre for Biodiversity Theory and Modelling, Theoretical and Experimental Ecology Station, CNRS, 2 route du CNRS, 09200, Moulis, France.
⁷ Department of Ecosystem Science and Management, University of Wyoming, Laramie, WY, USA.
⁸ Department of Ecology, Evolution, and Behavior, University of MN, St. Paul, MN, 55108, USA.
⁹ Department of Biology, University of Massachusetts Boston, Boston, MA, 02125, USA.
¹⁰ Department of Biology, University of North Carolina Greensboro, Greensboro, NC, USA.
¹¹ Smithsonian Environmental Research Center, Edgewater, MD, 21037, USA.
¹² Tennenbaum Marine Observatories Network, MarineGEO, Smithsonian Environmental Research Center, Edgewater, MD, 21037, USA.
¹³ University of Oxford Department of Plant Sciences, Oxford, OX1 3RB, UK.
¹⁴ Department of Wildland Resources and the Ecology Center, Utah State University, Logan, UT, 84322, USA.
¹⁵ Instituto de Investigaciones Marinas y Costeras (IIMyC), FCEyN, UNMdP-CONICET, CC 1260 Correo Central, B7600WAG, Mar del Plata, Argentina.
¹⁶ Department of Physical and Environmental Sciences, University of Toronto at Scarborough, Scarborough, ON, Canada.
¹⁷ School of Environmental and Forest Sciences, University of Washington, Seattle, WA, 98195-4115, USA.
¹⁸ Department of Plant Biology and Program in Ecology, Evolutionary Biology, and Behavior, Michigan State University, East Lansing, MI, USA.
¹⁹ Centre for Applied Ecology "Prof. Baeta Neves" (CEABN-InBIO), School of Agriculture, University of Lisbon, Lisbon, Portugal.
²⁰ Department of Biological Sciences, University of Toronto at Scarborough, Scarborough, ON, Canada.
²¹ Forest Research Centre, School of Agriculture, University of Lisbon, Lisbon, Portugal.
²² Department of Integrative Biology, University of Guelph, Guelph, ON, N1G2W1, Canada.
²³ Life Sciences, Imperial College London, Silwood Park, Ascot, SL5 7PY, UK.
²⁴ University of New Mexico, Department of Biology, Albuquerque, NM, 87131, USA.
²⁵ Department of Ecology and Evolutionary Biology, University of Colorado at Boulder, 1560 30th Street, Boulder, CO, 80309-0450, USA.
²⁶ German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103, Leipzig, Germany.
²⁷ Leipzig University, Institute of Biology, Deutscher Platz 5e, 04103, Leipzig, Germany.
²⁸ Department of Physiological Diversity, Helmholtz Centre for Environmental Research - UFZ, Leipzig, Germany.
²⁹ Department of Ecology and Genetics, University of Oulu, Oulu, Finland.
³⁰ USDA-ARS Grassland, Soil, and Water Research Laboratory, Temple, TX, 76502, USA.
³¹ Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, M5S3B2, Canada.
³² Centre de recherche en écologie expérimentale et prédictive (CEREEP-Ecotron IleDeFrance), Département de biologie, Ecole normale supérieure, CNRS, PSL University, 77140, St-Pierre-les-Nemours, France.
³³ Department of Heatth and Environmental Sciences, Xi'an Jiaotong liverpool University, 214123, Suzhou, Jiangsu, China.
³⁴ University of Kentucky, Plant & Soil Science, 1405 Veterans Drive, Lexington, KY, 40546-0312, USA.
³⁵ School of Biological Sciences, Monash University, Clayton Campus, Clayton, VIC, 3800, Australia.
³⁶ Department of Ecology, Environment & Evolution, La Trobe University, Bundoora, VIC, 3086, Australia.
³⁷ Graduate School of Environment and Information Sciences, Yokohama National University, 79-7 Tokiwadai, Hodogaya, Yokohama, Kanagawa, 240-8501, Japan.
³⁸ INTA (National Institute of Agricultural Research)- UNPA (Southern Patagonia National University)-CONICET, Santa Cruz, Argentina.
³⁹ Hawkesbury Institute for the Environment, Western Sydney University, Locked Bag 1797, Penrith, NSW, 2751, Australia.
⁴⁰ Institute of Land, Water and Society, Charles Sturt University, Albury, NSW, 2640, Australia.
⁴¹ Department of Forest Resources, University of Minnesota, Saint Paul, MN, USA.
⁴² Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Zuercherstrasse 111, 8903, Birmensdorf, Switzerland.
⁴³ UFZ, Helmholtz Centre for Environmental Research, Physiological Diversity, Permoserstrasse 15, 04318, Leipzig, Germany.
⁴⁴ Ecology & Evolution Group, National Centre for Biological Sciences, TIFR, Bangalore, Karnataka, 560065, India.
⁴⁵ School of Biology, University of Leeds, Leeds, LS2 9JT, UK.
⁴⁶ Department of Biology, Colorado State University, Fort Collins, CO, 80523, USA.
⁴⁷ Graduate Degree Program in Ecology, Colorado State University, Fort Collins, CO, 80523, USA.
⁴⁸ Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, UK.
⁴⁹ IFEVA-Facultad de Agronomia, Universidad de Buenos Aires - CONICET, Av San Martin 4453, C1417DSE, Ciudad Autonoma de Buenos Aires, Argentina.
⁵⁰ School of Life and Environmental Sciences, University of Sydney, Sydney, NSW, 2006, Australia.
⁵¹ Institute of Ecology, College of Urban and Environmental Science, and Key Laboratory for Earth Surface Processes of the Ministry of Education, Peking University, 100871, Beijing, China. shaopeng.wang@pku.edu.cn.

PMID: 33097736
PMCID: PMC7585434
DOI: 10.1038/s41467-020-19252-4

General destabilizing effects of eutrophication on grassland productivity at multiple spatial scales

Yann Hautier et al. Nat Commun. 2020.

. 2020 Oct 23;11(1):5375.

doi: 10.1038/s41467-020-19252-4.

Authors

Affiliations

¹ Ecology and Biodiversity Group, Department of Biology, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands. y.hautier@uu.nl.
² Ecology and Biodiversity Group, Department of Biology, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands.
³ State Key Laboratory of Grassland and Agro-Ecosystems, School of Life Science, Lanzhou University, 730000, Lanzhou, Gansu Province, People's Republic of China.
⁴ Institute of Eco-Environmental Forensics of Shandong University, 266237, Jinan, Shandong Province, People's Republic of China.
⁵ Ministry of Justice Hub for Research & Practice in Eco-Environmental Forensics, 266237, Qingdao, Shandong Province, People's Republic of China.
⁶ Centre for Biodiversity Theory and Modelling, Theoretical and Experimental Ecology Station, CNRS, 2 route du CNRS, 09200, Moulis, France.
⁷ Department of Ecosystem Science and Management, University of Wyoming, Laramie, WY, USA.
⁸ Department of Ecology, Evolution, and Behavior, University of MN, St. Paul, MN, 55108, USA.
⁹ Department of Biology, University of Massachusetts Boston, Boston, MA, 02125, USA.
¹⁰ Department of Biology, University of North Carolina Greensboro, Greensboro, NC, USA.
¹¹ Smithsonian Environmental Research Center, Edgewater, MD, 21037, USA.
¹² Tennenbaum Marine Observatories Network, MarineGEO, Smithsonian Environmental Research Center, Edgewater, MD, 21037, USA.
¹³ University of Oxford Department of Plant Sciences, Oxford, OX1 3RB, UK.
¹⁴ Department of Wildland Resources and the Ecology Center, Utah State University, Logan, UT, 84322, USA.
¹⁵ Instituto de Investigaciones Marinas y Costeras (IIMyC), FCEyN, UNMdP-CONICET, CC 1260 Correo Central, B7600WAG, Mar del Plata, Argentina.
¹⁶ Department of Physical and Environmental Sciences, University of Toronto at Scarborough, Scarborough, ON, Canada.
¹⁷ School of Environmental and Forest Sciences, University of Washington, Seattle, WA, 98195-4115, USA.
¹⁸ Department of Plant Biology and Program in Ecology, Evolutionary Biology, and Behavior, Michigan State University, East Lansing, MI, USA.
¹⁹ Centre for Applied Ecology "Prof. Baeta Neves" (CEABN-InBIO), School of Agriculture, University of Lisbon, Lisbon, Portugal.
²⁰ Department of Biological Sciences, University of Toronto at Scarborough, Scarborough, ON, Canada.
²¹ Forest Research Centre, School of Agriculture, University of Lisbon, Lisbon, Portugal.
²² Department of Integrative Biology, University of Guelph, Guelph, ON, N1G2W1, Canada.
²³ Life Sciences, Imperial College London, Silwood Park, Ascot, SL5 7PY, UK.
²⁴ University of New Mexico, Department of Biology, Albuquerque, NM, 87131, USA.
²⁵ Department of Ecology and Evolutionary Biology, University of Colorado at Boulder, 1560 30th Street, Boulder, CO, 80309-0450, USA.
²⁶ German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103, Leipzig, Germany.
²⁷ Leipzig University, Institute of Biology, Deutscher Platz 5e, 04103, Leipzig, Germany.
²⁸ Department of Physiological Diversity, Helmholtz Centre for Environmental Research - UFZ, Leipzig, Germany.
²⁹ Department of Ecology and Genetics, University of Oulu, Oulu, Finland.
³⁰ USDA-ARS Grassland, Soil, and Water Research Laboratory, Temple, TX, 76502, USA.
³¹ Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, M5S3B2, Canada.
³² Centre de recherche en écologie expérimentale et prédictive (CEREEP-Ecotron IleDeFrance), Département de biologie, Ecole normale supérieure, CNRS, PSL University, 77140, St-Pierre-les-Nemours, France.
³³ Department of Heatth and Environmental Sciences, Xi'an Jiaotong liverpool University, 214123, Suzhou, Jiangsu, China.
³⁴ University of Kentucky, Plant & Soil Science, 1405 Veterans Drive, Lexington, KY, 40546-0312, USA.
³⁵ School of Biological Sciences, Monash University, Clayton Campus, Clayton, VIC, 3800, Australia.
³⁶ Department of Ecology, Environment & Evolution, La Trobe University, Bundoora, VIC, 3086, Australia.
³⁷ Graduate School of Environment and Information Sciences, Yokohama National University, 79-7 Tokiwadai, Hodogaya, Yokohama, Kanagawa, 240-8501, Japan.
³⁸ INTA (National Institute of Agricultural Research)- UNPA (Southern Patagonia National University)-CONICET, Santa Cruz, Argentina.
³⁹ Hawkesbury Institute for the Environment, Western Sydney University, Locked Bag 1797, Penrith, NSW, 2751, Australia.
⁴⁰ Institute of Land, Water and Society, Charles Sturt University, Albury, NSW, 2640, Australia.
⁴¹ Department of Forest Resources, University of Minnesota, Saint Paul, MN, USA.
⁴² Swiss Federal Institute for Forest, Snow and Landscape Research WSL, Zuercherstrasse 111, 8903, Birmensdorf, Switzerland.
⁴³ UFZ, Helmholtz Centre for Environmental Research, Physiological Diversity, Permoserstrasse 15, 04318, Leipzig, Germany.
⁴⁴ Ecology & Evolution Group, National Centre for Biological Sciences, TIFR, Bangalore, Karnataka, 560065, India.
⁴⁵ School of Biology, University of Leeds, Leeds, LS2 9JT, UK.
⁴⁶ Department of Biology, Colorado State University, Fort Collins, CO, 80523, USA.
⁴⁷ Graduate Degree Program in Ecology, Colorado State University, Fort Collins, CO, 80523, USA.
⁴⁸ Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, UK.
⁴⁹ IFEVA-Facultad de Agronomia, Universidad de Buenos Aires - CONICET, Av San Martin 4453, C1417DSE, Ciudad Autonoma de Buenos Aires, Argentina.
⁵⁰ School of Life and Environmental Sciences, University of Sydney, Sydney, NSW, 2006, Australia.
⁵¹ Institute of Ecology, College of Urban and Environmental Science, and Key Laboratory for Earth Surface Processes of the Ministry of Education, Peking University, 100871, Beijing, China. shaopeng.wang@pku.edu.cn.

PMID: 33097736
PMCID: PMC7585434
DOI: 10.1038/s41467-020-19252-4

Erratum in

Author Correction: General destabilizing effects of eutrophication on grassland productivity at multiple spatial scales.
Hautier Y, Zhang P, Loreau M, Wilcox KR, Seabloom EW, Borer ET, Byrnes JEK, Koerner SE, Komatsu KJ, Lefcheck JS, Hector A, Adler PB, Alberti J, Arnillas CA, Bakker JD, Brudvig LA, Bugalho MN, Cadotte M, Caldeira MC, Carroll O, Crawley M, Collins SL, Daleo P, Dee LE, Eisenhauer N, Eskelinen A, Fay PA, Gilbert B, Hansar A, Isbell F, Knops JMH, MacDougall AS, McCulley RL, Moore JL, Morgan JW, Mori AS, Peri PL, Pos ET, Power SA, Price JN, Reich PB, Risch AC, Roscher C, Sankaran M, Schütz M, Smith M, Stevens C, Tognetti PM, Virtanen R, Wardle GM, Wilfahrt PA, Wang S. Hautier Y, et al. Nat Commun. 2021 Jan 21;12(1):630. doi: 10.1038/s41467-021-20997-9. Nat Commun. 2021. PMID: 33479239 Free PMC article. No abstract available.

Abstract

Eutrophication is a widespread environmental change that usually reduces the stabilizing effect of plant diversity on productivity in local communities. Whether this effect is scale dependent remains to be elucidated. Here, we determine the relationship between plant diversity and temporal stability of productivity for 243 plant communities from 42 grasslands across the globe and quantify the effect of chronic fertilization on these relationships. Unfertilized local communities with more plant species exhibit greater asynchronous dynamics among species in response to natural environmental fluctuations, resulting in greater local stability (alpha stability). Moreover, neighborhood communities that have greater spatial variation in plant species composition within sites (higher beta diversity) have greater spatial asynchrony of productivity among communities, resulting in greater stability at the larger scale (gamma stability). Importantly, fertilization consistently weakens the contribution of plant diversity to both of these stabilizing mechanisms, thus diminishing the positive effect of biodiversity on stability at differing spatial scales. Our findings suggest that preserving grassland functional stability requires conservation of plant diversity within and among ecological communities.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1. Conceptual figure illustrating the nonexclusive processes by which species stability, species asynchrony, and spatial asynchrony may contribute to stabilize functioning (such as productivity) within (alpha stability) and among communities (gamma stability).
a Low stability and asynchrony of species within communities result in low alpha stability that in turn results in low gamma stability under low degree of asynchronous dynamics among communities (spatial asynchrony). Relatively high alpha and gamma stability may result from b high species stability and c high species asynchrony. d Relatively high gamma stability may additionally result from high spatial asynchrony. e Path analysis used to assess the relationship of local and beta diversity with the mechanisms promoting stability at multiple spatial scales under unmanipulated control or fertilized condition. Note that species names belong to a given community, they could or could not be the same species among communities. Adapted from Wilcox et al..

**Fig. 2. Impact of fertilization on biodiversity–stability relationships across spatial scales.**
Stability was measured as the temporal mean of primary productivity divided by its temporal standard deviation. Relationships were generally consistent among the periods of experimental duration considered (Supplementary Table 1). Species richness was positively associated with a alpha (slope and 95% CIs across time = 0.17 (0.08–0.26)) and b gamma stability (0.27 (0.15–0.39)) in the unmanipulated communities, but unrelated to c alpha (0.01 (−0.07 to 0.10)) and d gamma stability (−0.02 (−0.09 to 0.14)) in the fertilized communities. Beta diversity was positively related to e spatial asynchrony (0.18 (0.06–0.30)) and f gamma stability (0.47 (0.19–0.74)) in the unmanipulated communities, but unrelated to g spatial asynchrony (−0.01 (−0.13 to 0.12)) and h gamma stability (0.21 (−0.07 to 0.50)) in the fertilized communities. Note the scale of y-axis differ across panels and this needs to be considered when visually inspecting slopes. Each dot represents the collective subplots across the three replicated 1-m² subplots for each site, treatment and duration period (n = 160). Colors represent the periods of experimental duration.

**Fig. 3. Summary of meta-analysis results.**
Direct and indirect pathways through which biodiversity, asynchrony, and stability at multiple spatial scales determines gamma stability under a unmanipulated control or b fertilized condition. Boxes represent measured variables and arrows represent relationships among variables. Numbers next to the arrows are averaged effect sizes as standardized path coefficients. Solid green and purple arrows represent significant (P ≤ 0.05) positive and negative coefficients, respectively, and dashed green and purple arrows represent nonsignificant coefficients. Widths of paths are scaled by standardized path coefficients. Percentages next to endogenous variables indicate the range of variance explained by the model (R²) across period of experimental duration.

See this image and copyright information in PMC

References

1. Erisman, J. W. et al. Consequences of human modification of the global nitrogen cycle. Philos. Trans. R. Soc. B Biol. Sci.368, 20130116 (2013). - PMC - PubMed
1. Galloway JN. The global nitrogen cycle: past, present and future. Sci. China Ser. C. Life Sci. 2005;48:669–677. - PubMed
1. Tilman D, et al. Forecasting agriculturally driven global environmental change. Science. 2001;292:281–284. doi: 10.1126/science.1057544. - DOI - PubMed
1. Hautier Y, et al. Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature. 2014;508:521–525. doi: 10.1038/nature13014. - DOI - PubMed
1. Xu ZW, et al. Environmental changes drive the temporal stability of semi-arid natural grasslands through altering species asynchrony. J. Ecol. 2015;103:1308–1316. doi: 10.1111/1365-2745.12441. - DOI

Publication types

Actions
Actions

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions

LinkOut - more resources

Full Text Sources

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

General destabilizing effects of eutrophication on grassland productivity at multiple spatial scales

Affiliations

General destabilizing effects of eutrophication on grassland productivity at multiple spatial scales

Authors

Affiliations

Erratum in

Abstract

Conflict of interest statement

Figures

References

Publication types

MeSH terms

LinkOut - more resources

Full Text Sources