Effects of plant diversity on productivity strengthen over time due to trait-dependent shifts in species overyielding

Liting Zheng; Kathryn E Barry; Nathaly R Guerrero-Ramírez; Dylan Craven; Peter B Reich; Kris Verheyen; Michael Scherer-Lorenzen; Nico Eisenhauer; Nadia Barsoum; Jürgen Bauhus; Helge Bruelheide; Jeannine Cavender-Bares; Jiri Dolezal; Harald Auge; Marina V Fagundes; Olga Ferlian; Sebastian Fiedler; David I Forrester; Gislene Ganade; Tobias Gebauer; Josephine Haase; Peter Hajek; Andy Hector; Bruno Hérault; Dirk Hölscher; Kristin B Hulvey; Bambang Irawan; Hervé Jactel; Julia Koricheva; Holger Kreft; Vojtech Lanta; Jan Leps; Simone Mereu; Christian Messier; Florencia Montagnini; Martin Mörsdorf; Sandra Müller; Bart Muys; Charles A Nock; Alain Paquette; William C Parker; John D Parker; John A Parrotta; Gustavo B Paterno; Michael P Perring; Daniel Piotto; H Wayne Polley; Quentin Ponette; Catherine Potvin; Yann Hautier

doi:10.1038/s41467-024-46355-z

Effects of plant diversity on productivity strengthen over time due to trait-dependent shifts in species overyielding

Liting Zheng^*
, Kathryn E Barry
, Nathaly R Guerrero-Ramírez
, Dylan Craven
, Peter B Reich
, Kris Verheyen
, Michael Scherer-Lorenzen
, Nico Eisenhauer
, Nadia Barsoum
, Jürgen Bauhus
, Helge Bruelheide
, Jeannine Cavender-Bares
, Jiri Dolezal
, Harald Auge
, Marina V Fagundes
, Olga Ferlian
, Sebastian Fiedler
, David I Forrester
, Gislene Ganade
, Tobias Gebauer

Josephine Haase, Peter Hajek, Andy Hector, Bruno Hérault, Dirk Hölscher, Kristin B Hulvey, Bambang Irawan, Hervé Jactel, Julia Koricheva, Holger Kreft, Vojtech Lanta, Jan Leps, Simone Mereu, Christian Messier, Florencia Montagnini, Martin Mörsdorf, Sandra Müller, Bart Muys, Charles A Nock, Alain Paquette, William C Parker, John D Parker, John A Parrotta, Gustavo B Paterno, Michael P Perring, Daniel Piotto, H Wayne Polley, Quentin Ponette, Catherine Potvin, Yann Hautier

^*Corresponding author for this work

University of Göttingen
GEMA Center for Genomics
University of Michigan-Dearborn
Ghent University
University of Freiburg
German Centre for Integrative Biodiversity Research (IDiv) Halle-Jena-Leipzig
Centre for Ecosystems
University of Minnesota Rochester
University of South Bohemia
Departamento de Ecología
CSIRO Environment
University of Oxford
CIRAD
Working Lands Conservation
University of Jambi
Université de Bordeaux
Royal Holloway University of London
Weill-Cornell Medical College, Cornell University, New York, New York, United States; ICRM-CNR Istituto di Chimica del Riconoscimento Molecolare, Consiglio Nazionale delle Ricerche, Milano, Italy. Electronic address: [email protected].
Département des sciences biologiques
Yale University
Department of Earth and Environmental Sciences
Ontario Ministry of Natural Resources and Forestry
Smithsonian Environmental Research Center
Research and Development
UKCEH (UK Centre for Ecology & Hydrology)
Centro de Formação em Ciências Agroflorestais
USDA FS
Earth and Life Institute
McGill University
extern

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Plant diversity effects on community productivity often increase over time. Whether the strengthening of diversity effects is caused by temporal shifts in species-level overyielding (i.e., higher species-level productivity in diverse communities compared with monocultures) remains unclear. Here, using data from 65 grassland and forest biodiversity experiments, we show that the temporal strength of diversity effects at the community scale is underpinned by temporal changes in the species that yield. These temporal trends of species-level overyielding are shaped by plant ecological strategies, which can be quantitatively delimited by functional traits. In grasslands, the temporal strengthening of biodiversity effects on community productivity was associated with increasing biomass overyielding of resource-conservative species increasing over time, and with overyielding of species characterized by fast resource acquisition either decreasing or increasing. In forests, temporal trends in species overyielding differ when considering above- versus belowground resource acquisition strategies. Overyielding in stem growth decreased for species with high light capture capacity but increased for those with high soil resource acquisition capacity. Our results imply that a diversity of species with different, and potentially complementary, ecological strategies is beneficial for maintaining community productivity over time in both grassland and forest ecosystems.

Original language	English
Article number	2078
Number of pages	14
Journal	Nature Communications
Volume	15
Issue number	1
DOIs	https://doi.org/10.1038/s41467-024-46355-z
Publication status	Published - 7 Mar 2024

Bibliographical note

Publisher Copyright:
© The Author(s) 2024.

Funding

This study was supported by the State Key Program of the National Natural Science Foundation of China (no. 32030068 to E.Y.). We recognize the invaluable contributions of all the researchers who initially developed the ideas and hypotheses, and who designed the BEF experiments in this study, maintained them, and ensured their regular measurements. We thank the platform provided by the TreeDivNet ( https://www.treedivnet.ugent.be ). We thank the Synthesis Centre of the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig (DFG FZT 118). The Jena and MyDiv experiments in this study were supported by the German Research Foundation (Jena Experiment: FOR 456, FOR 1451, FOR 5000; MyDiv: DFG–FZT; Ei 862/29-1). The Cedar Creek biodiversity experiments were supported by the NSF Cedar Creek Long-Term Ecological Research grant (DEB: 1831944) and the NSF ASCEND Biology Integration Institute (DBI:2021898). The Lanta_drt and Lanta_nutr experiments (led by V. L. and J.D.) were supported by the Czech Academy of Sciences (23-07533S, 24-11954S, RVO 67985939). The Wageningen Biodiversity Experiment was partly supported by a grant from the Dutch Organisation for Scientific Research (NWO) within the framework of the Biodiversity Program. The BIOTREE experiment has been established by the Max-Planck-Institute for Biogeochemistry Jena, Germany, and received funding through the Chair of Geobotany, Faculty of Biology, University of Freiburg, and a grant by the German Research Foundation (no. 439223434 to M.S.-L.; for data collection in 2019). We thank Prof. Dr. E. D. Schulze for initiating and supporting this project; and D. Mackensen and K. Hahner (Federal Forestry Office Thüringer Wald – Bundesforstamt Thüringer Wald, Bad Salzungen) for their support and BIOTREE site maintenance. The Kreinitz experiment is a cooperative research project funded by the Helmholtz-Centre for Environmental Research—UFZ. The EFForTS-project was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) – project ID 192626868 – SFB 990. The B-Tree set-up was funded by the University of Natural Resources and Life Sciences, Vienna. B-tree was supported by the BiodivERsA3 and BiodivClim ERA-Net COFOUND program (Dr. Forest, MixForChange), and with the funding organization Österreichischer Wissenschaftsfonds [grant numbers I 4372-B, I 50086-B]. BR and DLG were supported by the EU Horizon project Excellentia [no. 101087262]. We thank the Sardinian Forest Authority “Forestas” for hosting the IDENT-Macomer experiment and contributing to its establishment and management. IDENT-Freiburg has been financially supported by the University of Freiburg, including a grant to M.S.-L. from the “Innovationsfonds Forschung”. IDENT sites in North-America were supported by the National Research and Engineering Council of Canada. BiodiversiTREE has been supported by the Smithsonian Institution and the US National Science Foundation (NSF DEB 2044406 & Macrosystems 2106014). The Ridgefield was instigated thanks to the award of an Australian Research Council Laureate Fellowship (FL0992007) to R.J.H. The Sardinilla experiment benefited from the support of the National Research and Engineering Council of Canada, a Canada Research Chair (Tier 1) to C.Potvin and from the Smithsonian Tropical Research Institute. We thank D. Binkley, A. Weigelt and W. Weisser for contributing data, and H.Y.H. Chen, I. Ibáñez, D. He, and K. Zhu for helping with data analysis, and thank T.F. Au for editorial comments. We also thank Takehiro Sasaki and the other reviewers for their comments on the improvement of the manuscript. This study was supported by the State Key Program of the National Natural Science Foundation of China (no. 32030068 to E.Y.). We recognize the invaluable contributions of all the researchers who initially developed the ideas and hypotheses, and who designed the BEF experiments in this study, maintained them, and ensured their regular measurements. We thank the platform provided by the TreeDivNet (https://www.treedivnet.ugent.be). We thank the Synthesis Centre of the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig (DFG FZT 118). The Jena and MyDiv experiments in this study were supported by the German Research Foundation (Jena Experiment: FOR 456, FOR 1451, FOR 5000; MyDiv: DFG–FZT; Ei 862/29-1). The Cedar Creek biodiversity experiments were supported by the NSF Cedar Creek Long-Term Ecological Research grant (DEB: 1831944) and the NSF ASCEND Biology Integration Institute (DBI:2021898). The Lanta_drt and Lanta_nutr experiments (led by V. L. and J.D.) were supported by the Czech Academy of Sciences (23-07533S, 24-11954S, RVO 67985939). The Wageningen Biodiversity Experiment was partly supported by a grant from the Dutch Organisation for Scientific Research (NWO) within the framework of the Biodiversity Program. The BIOTREE experiment has been established by the Max-Planck-Institute for Biogeochemistry Jena, Germany, and received funding through the Chair of Geobotany, Faculty of Biology, University of Freiburg, and a grant by the German Research Foundation (no. 439223434 to M.S.-L.; for data collection in 2019). We thank Prof. Dr. E. D. Schulze for initiating and supporting this project; and D. Mackensen and K. Hahner (Federal Forestry Office Thüringer Wald – Bundesforstamt Thüringer Wald, Bad Salzungen) for their support and BIOTREE site maintenance. The Kreinitz experiment is a cooperative research project funded by the Helmholtz-Centre for Environmental Research—UFZ. The EFForTS-project was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) – project ID 192626868 – SFB 990. The B-Tree set-up was funded by the University of Natural Resources and Life Sciences, Vienna. B-tree was supported by the BiodivERsA3 and BiodivClim ERA-Net COFOUND program (Dr. Forest, MixForChange), and with the funding organization Österreichischer Wissenschaftsfonds [grant numbers I 4372-B, I 50086-B]. BR and DLG were supported by the EU Horizon project Excellentia [no. 101087262]. We thank the Sardinian Forest Authority “Forestas” for hosting the IDENT-Macomer experiment and contributing to its establishment and management. IDENT-Freiburg has been financially supported by the University of Freiburg, including a grant to M.S.-L. from the “Innovationsfonds Forschung”. IDENT sites in North-America were supported by the National Research and Engineering Council of Canada. BiodiversiTREE has been supported by the Smithsonian Institution and the US National Science Foundation (NSF DEB 2044406 & Macrosystems 2106014). The Ridgefield was instigated thanks to the award of an Australian Research Council Laureate Fellowship (FL0992007) to R.J.H. The Sardinilla experiment benefited from the support of the National Research and Engineering Council of Canada, a Canada Research Chair (Tier 1) to C.Potvin and from the Smithsonian Tropical Research Institute. We thank D. Binkley, A. Weigelt and W. Weisser for contributing data, and H.Y.H. Chen, I. Ibáñez, D. He, and K. Zhu for helping with data analysis, and thank T.F. Au for editorial comments. We also thank Takehiro Sasaki and the other reviewers for their comments on the improvement of the manuscript.

Funders	Funder number
EU Horizon project Excellentia	101087262
Federal Forestry Office Thüringer Wald – Bundesforstamt Thüringer Wald, Bad Salzungen
Helmholtz-Centre for Environmental Research
Innovationsfonds Forschung
NSF Cedar Creek Long-Term Ecological Research	1831944
Sardinian Forest Authority
Synthesis Centre of the German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig	FZT 118
University of Natural Resources and Life Sciences
National Science Foundation	DEB 2044406, 2106014
National Science Foundation
Smithsonian Institution
Smithsonian Tropical Research Institute
Australian Research Council	FL0992007
Australian Research Council
Deutsche Forschungsgemeinschaft	Ei 862/29-1, FOR 1451, 192626868 – SFB 990, FOR 456
Deutsche Forschungsgemeinschaft
Canada Research Chairs
National Natural Science Foundation of China	32030068
National Natural Science Foundation of China
Austrian Science Fund	I 4372-B
Austrian Science Fund
Albert-Ludwigs-Universität Freiburg	439223434
Albert-Ludwigs-Universität Freiburg
Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada
Nederlandse Organisatie voor Wetenschappelijk Onderzoek
Akademie Věd České Republiky	RVO 67985939, 23-07533S, 24-11954S
Akademie Věd České Republiky
Helmholtz-Zentrum für Umweltforschung

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s41467-024-46355-zFinal published version, 9.57 MBLicence: CC BY

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Zheng, L., Barry, K. E., Guerrero-Ramírez, N. R., Craven, D., Reich, P. B., Verheyen, K., Scherer-Lorenzen, M., Eisenhauer, N., Barsoum, N., Bauhus, J., Bruelheide, H., Cavender-Bares, J., Dolezal, J., Auge, H., Fagundes, M. V., Ferlian, O., Fiedler, S., Forrester, D. I., Ganade, G., ... Hautier, Y. (2024). Effects of plant diversity on productivity strengthen over time due to trait-dependent shifts in species overyielding. Nature Communications, 15(1), Article 2078. https://doi.org/10.1038/s41467-024-46355-z

@article{a67f4118775140f6b9a95d3d334a7017,

title = "Effects of plant diversity on productivity strengthen over time due to trait-dependent shifts in species overyielding",

abstract = "Plant diversity effects on community productivity often increase over time. Whether the strengthening of diversity effects is caused by temporal shifts in species-level overyielding (i.e., higher species-level productivity in diverse communities compared with monocultures) remains unclear. Here, using data from 65 grassland and forest biodiversity experiments, we show that the temporal strength of diversity effects at the community scale is underpinned by temporal changes in the species that yield. These temporal trends of species-level overyielding are shaped by plant ecological strategies, which can be quantitatively delimited by functional traits. In grasslands, the temporal strengthening of biodiversity effects on community productivity was associated with increasing biomass overyielding of resource-conservative species increasing over time, and with overyielding of species characterized by fast resource acquisition either decreasing or increasing. In forests, temporal trends in species overyielding differ when considering above- versus belowground resource acquisition strategies. Overyielding in stem growth decreased for species with high light capture capacity but increased for those with high soil resource acquisition capacity. Our results imply that a diversity of species with different, and potentially complementary, ecological strategies is beneficial for maintaining community productivity over time in both grassland and forest ecosystems.",

author = "Liting Zheng and Barry, \{Kathryn E\} and Guerrero-Ram{\'i}rez, \{Nathaly R\} and Dylan Craven and Reich, \{Peter B\} and Kris Verheyen and Michael Scherer-Lorenzen and Nico Eisenhauer and Nadia Barsoum and J{\"u}rgen Bauhus and Helge Bruelheide and Jeannine Cavender-Bares and Jiri Dolezal and Harald Auge and Fagundes, \{Marina V\} and Olga Ferlian and Sebastian Fiedler and Forrester, \{David I\} and Gislene Ganade and Tobias Gebauer and Josephine Haase and Peter Hajek and Andy Hector and Bruno H{\'e}rault and Dirk H{\"o}lscher and Hulvey, \{Kristin B\} and Bambang Irawan and Herv{\'e} Jactel and Julia Koricheva and Holger Kreft and Vojtech Lanta and Jan Leps and Simone Mereu and Christian Messier and Florencia Montagnini and Martin M{\"o}rsdorf and Sandra M{\"u}ller and Bart Muys and Nock, \{Charles A\} and Alain Paquette and Parker, \{William C\} and Parker, \{John D\} and Parrotta, \{John A\} and Paterno, \{Gustavo B\} and Perring, \{Michael P\} and Daniel Piotto and \{Wayne Polley\}, H and Quentin Ponette and Catherine Potvin and Yann Hautier",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

year = "2024",

month = mar,

day = "7",

doi = "10.1038/s41467-024-46355-z",

language = "English",

volume = "15",

journal = "Nature Communications",

issn = "2041-1723",

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Zheng, L, Barry, KE, Guerrero-Ramírez, NR, Craven, D, Reich, PB, Verheyen, K, Scherer-Lorenzen, M, Eisenhauer, N, Barsoum, N, Bauhus, J, Bruelheide, H, Cavender-Bares, J, Dolezal, J, Auge, H, Fagundes, MV, Ferlian, O, Fiedler, S, Forrester, DI, Ganade, G, Gebauer, T, Haase, J, Hajek, P, Hector, A, Hérault, B, Hölscher, D, Hulvey, KB, Irawan, B, Jactel, H, Koricheva, J, Kreft, H, Lanta, V, Leps, J, Mereu, S, Messier, C, Montagnini, F, Mörsdorf, M, Müller, S, Muys, B, Nock, CA, Paquette, A, Parker, WC, Parker, JD, Parrotta, JA, Paterno, GB, Perring, MP, Piotto, D, Wayne Polley, H, Ponette, Q, Potvin, C & Hautier, Y 2024, 'Effects of plant diversity on productivity strengthen over time due to trait-dependent shifts in species overyielding', Nature Communications, vol. 15, no. 1, 2078. https://doi.org/10.1038/s41467-024-46355-z

TY - JOUR

T1 - Effects of plant diversity on productivity strengthen over time due to trait-dependent shifts in species overyielding

AU - Zheng, Liting

AU - Barry, Kathryn E

AU - Guerrero-Ramírez, Nathaly R

AU - Craven, Dylan

AU - Reich, Peter B

AU - Verheyen, Kris

AU - Scherer-Lorenzen, Michael

AU - Eisenhauer, Nico

AU - Barsoum, Nadia

AU - Bauhus, Jürgen

AU - Bruelheide, Helge

AU - Cavender-Bares, Jeannine

AU - Dolezal, Jiri

AU - Auge, Harald

AU - Fagundes, Marina V

AU - Ferlian, Olga

AU - Fiedler, Sebastian

AU - Forrester, David I

AU - Ganade, Gislene

AU - Gebauer, Tobias

AU - Haase, Josephine

AU - Hajek, Peter

AU - Hector, Andy

AU - Hérault, Bruno

AU - Hölscher, Dirk

AU - Hulvey, Kristin B

AU - Irawan, Bambang

AU - Jactel, Hervé

AU - Koricheva, Julia

AU - Kreft, Holger

AU - Lanta, Vojtech

AU - Leps, Jan

AU - Mereu, Simone

AU - Messier, Christian

AU - Montagnini, Florencia

AU - Mörsdorf, Martin

AU - Müller, Sandra

AU - Muys, Bart

AU - Nock, Charles A

AU - Paquette, Alain

AU - Parker, William C

AU - Parker, John D

AU - Parrotta, John A

AU - Paterno, Gustavo B

AU - Perring, Michael P

AU - Piotto, Daniel

AU - Wayne Polley, H

AU - Ponette, Quentin

AU - Potvin, Catherine

AU - Hautier, Yann

PY - 2024/3/7

Y1 - 2024/3/7

N2 - Plant diversity effects on community productivity often increase over time. Whether the strengthening of diversity effects is caused by temporal shifts in species-level overyielding (i.e., higher species-level productivity in diverse communities compared with monocultures) remains unclear. Here, using data from 65 grassland and forest biodiversity experiments, we show that the temporal strength of diversity effects at the community scale is underpinned by temporal changes in the species that yield. These temporal trends of species-level overyielding are shaped by plant ecological strategies, which can be quantitatively delimited by functional traits. In grasslands, the temporal strengthening of biodiversity effects on community productivity was associated with increasing biomass overyielding of resource-conservative species increasing over time, and with overyielding of species characterized by fast resource acquisition either decreasing or increasing. In forests, temporal trends in species overyielding differ when considering above- versus belowground resource acquisition strategies. Overyielding in stem growth decreased for species with high light capture capacity but increased for those with high soil resource acquisition capacity. Our results imply that a diversity of species with different, and potentially complementary, ecological strategies is beneficial for maintaining community productivity over time in both grassland and forest ecosystems.

AB - Plant diversity effects on community productivity often increase over time. Whether the strengthening of diversity effects is caused by temporal shifts in species-level overyielding (i.e., higher species-level productivity in diverse communities compared with monocultures) remains unclear. Here, using data from 65 grassland and forest biodiversity experiments, we show that the temporal strength of diversity effects at the community scale is underpinned by temporal changes in the species that yield. These temporal trends of species-level overyielding are shaped by plant ecological strategies, which can be quantitatively delimited by functional traits. In grasslands, the temporal strengthening of biodiversity effects on community productivity was associated with increasing biomass overyielding of resource-conservative species increasing over time, and with overyielding of species characterized by fast resource acquisition either decreasing or increasing. In forests, temporal trends in species overyielding differ when considering above- versus belowground resource acquisition strategies. Overyielding in stem growth decreased for species with high light capture capacity but increased for those with high soil resource acquisition capacity. Our results imply that a diversity of species with different, and potentially complementary, ecological strategies is beneficial for maintaining community productivity over time in both grassland and forest ecosystems.

UR - https://www.scopus.com/pages/publications/85187178453

U2 - 10.1038/s41467-024-46355-z

DO - 10.1038/s41467-024-46355-z

M3 - Article

C2 - 38453933

SN - 2041-1723

VL - 15

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 2078

ER -

Effects of plant diversity on productivity strengthen over time due to trait-dependent shifts in species overyielding

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