Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems
Abstract
Phosphorus (P) limitation of aboveground plant production is usually assumed to occur in tropical regions but rarely elsewhere. Here we report that such P limitation is more widespread and much stronger than previously estimated. In our global meta-analysis, almost half (46.2%) of 652 P-addition field experiments reveal a significant P limitation on aboveground plant production. Globally, P additions increase aboveground plant production by 34.9% in natural terrestrial ecosystems, which is 7.0–15.9% higher than previously suggested. In croplands, by contrast, P additions increase aboveground plant production by only 13.9%, probably because of historical fertilizations. The magnitude of P limitation also differs among climate zones and regions, and is driven by climate, ecosystem properties, and fertilization regimes. In addition to confirming that P limitation is widespread in tropical regions, our study demonstrates that P limitation often occurs in other regions. This suggests that previous studies have underestimated the importance of altered P supply on aboveground plant production in natural terrestrial ecosystems.
- Authors:
-
[1];
[3];
- Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China; Center of Plant Ecology, Core Botanical Gardens, Chinese Academy of Sciences, Guangzhou, 510650, China; Northern Arizona Univ., Flagstaff, AZ (United States). Center for Ecosystem Science and Society
- Northern Arizona Univ., Flagstaff, AZ (United States). Center for Ecosystem Science and Society
- Australian Rivers Institute, School of Environment and Science, Griffith University, Nathan, QLD, 4111, Australia
- Key Laboratory of Vegetation Restoration and Management of Degraded Ecosystems, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China; Center of Plant Ecology, Core Botanical Gardens, Chinese Academy of Sciences, Guangzhou, 510650, China
- Publication Date:
- Research Org.:
- Univ. of Florida, Gainesville, FL (United States); Northern Arizona Univ., Flagstaff, AZ (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC); National Natural Science Foundation of China (NSFC); National Science Foundation (NSF); ORNL; Northern Arizona University
- OSTI Identifier:
- 1624246
- Grant/Contract Number:
- SC0006982; SC0014085; 31870464; 41973076; 41471443; 41401326; DEB 1655499; 4000158404; 4000161830
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Communications
- Additional Journal Information:
- Journal Volume: 11; Journal Issue: 1; Journal ID: ISSN 2041-1723
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- Science & Technology - Other Topics
Citation Formats
Hou, Enqing, Luo, Yiqi, Kuang, Yuanwen, Chen, Chengrong, Lu, Xiankai, Jiang, Lifen, Luo, Xianzhen, and Wen, Dazhi. Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. United States: N. p., 2020.
Web. doi:10.1038/s41467-020-14492-w.
Hou, Enqing, Luo, Yiqi, Kuang, Yuanwen, Chen, Chengrong, Lu, Xiankai, Jiang, Lifen, Luo, Xianzhen, & Wen, Dazhi. Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems. United States. https://doi.org/10.1038/s41467-020-14492-w
Hou, Enqing, Luo, Yiqi, Kuang, Yuanwen, Chen, Chengrong, Lu, Xiankai, Jiang, Lifen, Luo, Xianzhen, and Wen, Dazhi. Fri .
"Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems". United States. https://doi.org/10.1038/s41467-020-14492-w. https://www.osti.gov/servlets/purl/1624246.
@article{osti_1624246,
title = {Global meta-analysis shows pervasive phosphorus limitation of aboveground plant production in natural terrestrial ecosystems},
author = {Hou, Enqing and Luo, Yiqi and Kuang, Yuanwen and Chen, Chengrong and Lu, Xiankai and Jiang, Lifen and Luo, Xianzhen and Wen, Dazhi},
abstractNote = {Phosphorus (P) limitation of aboveground plant production is usually assumed to occur in tropical regions but rarely elsewhere. Here we report that such P limitation is more widespread and much stronger than previously estimated. In our global meta-analysis, almost half (46.2%) of 652 P-addition field experiments reveal a significant P limitation on aboveground plant production. Globally, P additions increase aboveground plant production by 34.9% in natural terrestrial ecosystems, which is 7.0–15.9% higher than previously suggested. In croplands, by contrast, P additions increase aboveground plant production by only 13.9%, probably because of historical fertilizations. The magnitude of P limitation also differs among climate zones and regions, and is driven by climate, ecosystem properties, and fertilization regimes. In addition to confirming that P limitation is widespread in tropical regions, our study demonstrates that P limitation often occurs in other regions. This suggests that previous studies have underestimated the importance of altered P supply on aboveground plant production in natural terrestrial ecosystems.},
doi = {10.1038/s41467-020-14492-w},
journal = {Nature Communications},
number = 1,
volume = 11,
place = {United States},
year = {2020},
month = {1}
}
Free Publicly Available Full Text
Publisher's Version of Record
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems
journal, December 2007
- Elser, James J.; Bracken, Matthew E. S.; Cleland, Elsa E.
- Ecology Letters, Vol. 10, Issue 12
Nitrogen limitation on land and in the sea: How can it occur?
journal, January 1991
- Vitousek, PeterM.; Howarth, RobertW.
- Biogeochemistry, Vol. 13, Issue 2
Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions
journal, January 2010
- Vitousek, Peter M.; Porder, Stephen; Houlton, Benjamin Z.
- Ecological Applications, Vol. 20, Issue 1
Pervasive phosphorus limitation of tree species but not communities in tropical forests
journal, March 2018
- Turner, Benjamin L.; Brenes-Arguedas, Tania; Condit, Richard
- Nature, Vol. 555, Issue 7696
Nitrogen Limitation of net Primary Productivity in Terrestrial Ecosystems is Globally Distributed
journal, February 2008
- LeBauer, David S.; Treseder, Kathleen K.
- Ecology, Vol. 89, Issue 2
Soil parent material—A major driver of plant nutrient limitations in terrestrial ecosystems
journal, April 2017
- Augusto, Laurent; Achat, David L.; Jonard, Mathieu
- Global Change Biology, Vol. 23, Issue 9
Aggravated phosphorus limitation on biomass production under increasing nitrogen loading: a meta-analysis
journal, January 2016
- Li, Yong; Niu, Shuli; Yu, Guirui
- Global Change Biology, Vol. 22, Issue 2
Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the south-western Australia biodiversity hotspot
journal, March 2012
- Laliberté, Etienne; Turner, Benjamin L.; Costes, Thomas
- Journal of Ecology, Vol. 100, Issue 3
Understanding ecosystem retrogression
journal, November 2010
- Peltzer, Duane A.; Wardle, David A.; Allison, Victoria J.
- Ecological Monographs, Vol. 80, Issue 4
Ecosystem Properties and Forest Decline in Contrasting Long-Term Chronosequences
journal, July 2004
- Wardle, D. A.
- Science, Vol. 305, Issue 5683
Incorporating phosphorus cycling into global modeling efforts: a worthwhile, tractable endeavor
journal, June 2015
- Reed, Sasha C.; Yang, Xiaojuan; Thornton, Peter E.
- New Phytologist, Vol. 208, Issue 2
Future productivity and carbon storage limited by terrestrial nutrient availability
journal, April 2015
- Wieder, William R.; Cleveland, Cory C.; Smith, W. Kolby
- Nature Geoscience, Vol. 8, Issue 6
Influence of multiple global change drivers on terrestrial carbon storage: additive effects are common
journal, March 2017
- Yue, Kai; Fornara, Dario A.; Yang, Wanqin
- Ecology Letters, Vol. 20, Issue 5
ELEVATED CO 2 STIMULATES NET ACCUMULATIONS OF CARBON AND NITROGEN IN LAND ECOSYSTEMS: A META-ANALYSIS
journal, January 2006
- Luo, Yiqi; Hui, Dafeng; Zhang, Deqiang
- Ecology, Vol. 87, Issue 1
Statistical Issues in Ecological Meta-Analyses
journal, June 1999
- Gurevitch, Jessica; Hedges, Larry V.
- Ecology, Vol. 80, Issue 4
Meta-analysis and the science of research synthesis
journal, March 2018
- Gurevitch, Jessica; Koricheva, Julia; Nakagawa, Shinichi
- Nature, Vol. 555, Issue 7695
Uses and misuses of meta-analysis in plant ecology
journal, June 2014
- Koricheva, Julia; Gurevitch, Jessica
- Journal of Ecology, Vol. 102, Issue 4
A working guide to boosted regression trees
journal, July 2008
- Elith, J.; Leathwick, J. R.; Hastie, T.
- Journal of Animal Ecology, Vol. 77, Issue 4
Global patterns of plant leaf N and P in relation to temperature and latitude
journal, June 2004
- Reich, P. B.; Oleksyn, J.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 30
Global-scale latitudinal patterns of plant fine-root nitrogen and phosphorus
journal, June 2011
- Yuan, Z. Y.; Chen, Han Y. H.; Reich, Peter B.
- Nature Communications, Vol. 2, Issue 1
Litterfall, Nutrient Cycling, and Nutrient Limitation in Tropical Forests
journal, February 1984
- Vitousek, Peter M.
- Ecology, Vol. 65, Issue 1
Effects of climate on soil phosphorus cycle and availability in natural terrestrial ecosystems
journal, March 2018
- Hou, Enqing; Chen, Chengrong; Luo, Yiqi
- Global Change Biology, Vol. 24, Issue 8
The Nature of Nutrient Limitation in Plant Communities
journal, January 1986
- Chapin, F. Stuart; Vitousek, Peter M.; Van Cleve, Keith
- The American Naturalist, Vol. 127, Issue 1
A plant–microbe interaction framework explaining nutrient effects on primary production
journal, September 2018
- Čapek, Petr; Manzoni, Stefano; Kaštovská, Eva
- Nature Ecology & Evolution, Vol. 2, Issue 10
Vegetation, soils, and forest productivity in selected forest types in interior Alaska
journal, October 1983
- Viereck, Leslie A.; Dyrness, C. T.; Cleve, Keith Van
- Canadian Journal of Forest Research, Vol. 13, Issue 5
Contribution of anthropogenic phosphorus to agricultural soil fertility and food production
journal, July 2014
- Ringeval, B.; Nowak, B.; Nesme, T.
- Global Biogeochemical Cycles, Vol. 28, Issue 7
Global nitrogen and phosphorus fertilizer use for agriculture production in the past half century: shifted hot spots and nutrient imbalance
journal, January 2017
- Lu, Chaoqun; Tian, Hanqin
- Earth System Science Data, Vol. 9, Issue 1
Soil phosphorus sorption capacity after three decades of intensive fertilization in Mato Grosso, Brazil
journal, November 2017
- Roy, Eric D.; Willig, Edwin; Richards, Peter D.
- Agriculture, Ecosystems & Environment, Vol. 249
Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials
journal, July 2011
- Sterne, J. A. C.; Sutton, A. J.; Ioannidis, J. P. A.
- BMJ, Vol. 343, Issue jul22 1
Plant nutrient-acquisition strategies change with soil age
journal, February 2008
- Lambers, H.; Raven, J.; Shaver, G.
- Trends in Ecology & Evolution, Vol. 23, Issue 2
Organic phosphorus in the terrestrial environment: a perspective on the state of the art and future priorities
journal, October 2017
- George, T. S.; Giles, C. D.; Menezes-Blackburn, D.
- Plant and Soil, Vol. 427, Issue 1-2
Soil pH predominantly controls the forms of organic phosphorus in topsoils under natural broadleaved forests along a 2500 km latitudinal gradient
journal, April 2018
- Hou, Enqing; Wen, Dazhi; Kuang, Yuanwen
- Geoderma, Vol. 315
The role of soil organic matter in sustaining soil fertility
journal, October 1994
- Tiessen, H.; Cuevas, E.; Chacon, P.
- Nature, Vol. 371, Issue 6500
Nutrient co-limitation of primary producer communities: Community co-limitation
journal, July 2011
- Harpole, W. Stanley; Ngai, Jacqueline T.; Cleland, Elsa E.
- Ecology Letters, Vol. 14, Issue 9
Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe
journal, December 2013
- Peñuelas, Josep; Poulter, Benjamin; Sardans, Jordi
- Nature Communications, Vol. 4, Issue 1
Very high resolution interpolated climate surfaces for global land areas
journal, January 2005
- Hijmans, Robert J.; Cameron, Susan E.; Parra, Juan L.
- International Journal of Climatology, Vol. 25, Issue 15
Phosphorus transformations as a function of pedogenesis: A synthesis of soil phosphorus data using Hedley fractionation method
journal, January 2011
- Yang, X.; Post, W. M.
- Biogeosciences, Vol. 8, Issue 10
Phosphorus dynamics in soils and landscapes
journal, December 1985
- Smeck, Neil E.
- Geoderma, Vol. 36, Issue 3-4
A global dataset of phosphorus addition experiments in terrestrial ecosystems
dataset, January 2020
- Hou, Enqing; Luo, Yiqi; Kuang, Yuanwen
- figshare
A basic introduction to fixed-effect and random-effects models for meta-analysis
journal, April 2010
- Borenstein, Michael; Hedges, Larry V.; Higgins, Julian P. T.
- Research Synthesis Methods, Vol. 1, Issue 2
A global dataset of phosphorus addition experiments in terrestrial ecosystems
dataset, January 2020
- Hou, Enqing; Luo, Yiqi; Kuang, Yuanwen
- figshare
Phosphorus transformations as a function of pedogenesis: a synthesis of soil phosphorus data using Hedley fractionation method
journal, January 2011
- Yang, X.; Post, W. M.
- Biogeosciences Discussions, Vol. 8, Issue 3
A global dataset of phosphorus addition experiments in terrestrial ecosystems
dataset, January 2019
- Hou, Enqing; Luo, Yiqi; Kuang, Yuanwen
- figshare
A global dataset of phosphorus addition experiments in terrestrial ecosystems
dataset, January 2019
- Hou, Enqing; Luo, Yiqi; Kuang, Yuanwen
- figshare
Comment on “Safety of systemic hormone replacement therapy in breast cancer survivors: a systematic review and meta‑analysis”
journal, June 2022
- Poggio, Francesca; Ceppi, Marcello; Fregatti, Piero
- Breast Cancer Research and Treatment, Vol. 194, Issue 3
Organic phosphorus in the terrestrial environment: a perspective on the state of the art and future priorities
journal, October 2017
- George, T. S.; Giles, C. D.; Menezes-Blackburn, D.
- Plant and Soil, Vol. 427, Issue 1-2
Phosphorus dynamics in soils and landscapes
journal, December 1985
- Smeck, Neil E.
- Geoderma, Vol. 36, Issue 3-4
Soil phosphorus sorption capacity after three decades of intensive fertilization in Mato Grosso, Brazil
journal, November 2017
- Roy, Eric D.; Willig, Edwin; Richards, Peter D.
- Agriculture, Ecosystems & Environment, Vol. 249
Soil pH predominantly controls the forms of organic phosphorus in topsoils under natural broadleaved forests along a 2500 km latitudinal gradient
journal, April 2018
- Hou, Enqing; Wen, Dazhi; Kuang, Yuanwen
- Geoderma, Vol. 315
Plant nutrient-acquisition strategies change with soil age
journal, February 2008
- Lambers, H.; Raven, J.; Shaver, G.
- Trends in Ecology & Evolution, Vol. 23, Issue 2
The role of soil organic matter in sustaining soil fertility
journal, October 1994
- Tiessen, H.; Cuevas, E.; Chacon, P.
- Nature, Vol. 371, Issue 6500
Human-induced nitrogen–phosphorus imbalances alter natural and managed ecosystems across the globe
journal, December 2013
- Peñuelas, Josep; Poulter, Benjamin; Sardans, Jordi
- Nature Communications, Vol. 4, Issue 1
Future productivity and carbon storage limited by terrestrial nutrient availability
journal, April 2015
- Wieder, William R.; Cleveland, Cory C.; Smith, W. Kolby
- Nature Geoscience, Vol. 8, Issue 6
A plant–microbe interaction framework explaining nutrient effects on primary production
journal, September 2018
- Čapek, Petr; Manzoni, Stefano; Kaštovská, Eva
- Nature Ecology & Evolution, Vol. 2, Issue 10
Functional group analyses of herpetofauna in South Korea using a large dataset
journal, January 2023
- Jeon, Jong Yoon; Lee, Dong Kun; Kim, Jae Hyun
- Scientific Data, Vol. 10, Issue 1
Global organization of terrestrial plant–nutrient interactions
journal, July 2004
- Hedin, Lars O.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 30
The Nature of Nutrient Limitation in Plant Communities
journal, January 1986
- Chapin, F. Stuart; Vitousek, Peter M.; Van Cleve, Keith
- The American Naturalist, Vol. 127, Issue 1
Soil parent material—A major driver of plant nutrient limitations in terrestrial ecosystems
journal, April 2017
- Augusto, Laurent; Achat, David L.; Jonard, Mathieu
- Global Change Biology, Vol. 23, Issue 9
A working guide to boosted regression trees
journal, July 2008
- Elith, J.; Leathwick, J. R.; Hastie, T.
- Journal of Animal Ecology, Vol. 77, Issue 4
Experimental assessment of nutrient limitation along a 2-million-year dune chronosequence in the south-western Australia biodiversity hotspot
journal, March 2012
- Laliberté, Etienne; Turner, Benjamin L.; Costes, Thomas
- Journal of Ecology, Vol. 100, Issue 3
Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems
journal, December 2007
- Elser, James J.; Bracken, Matthew E. S.; Cleland, Elsa E.
- Ecology Letters, Vol. 10, Issue 12
Recommendations for examining and interpreting funnel plot asymmetry in meta-analyses of randomised controlled trials
journal, July 2011
- Sterne, J. A. C.; Sutton, A. J.; Ioannidis, J. P. A.
- BMJ, Vol. 343, Issue jul22 1
Vegetation, soils, and forest productivity in selected forest types in interior Alaska
journal, October 1983
- Viereck, Leslie A.; Dyrness, C. T.; Cleve, Keith Van
- Canadian Journal of Forest Research, Vol. 13, Issue 5
Comparing Implementations of Estimation Methods for Spatial Econometrics
journal, January 2015
- Bivand, Roger; Piras, Gianfranco
- Journal of Statistical Software, Vol. 63, Issue 18
ELEVATED CO 2 STIMULATES NET ACCUMULATIONS OF CARBON AND NITROGEN IN LAND ECOSYSTEMS: A META-ANALYSIS
journal, January 2006
- Luo, Yiqi; Hui, Dafeng; Zhang, Deqiang
- Ecology, Vol. 87, Issue 1
Nitrogen Limitation of net Primary Productivity in Terrestrial Ecosystems is Globally Distributed
journal, February 2008
- LeBauer, David S.; Treseder, Kathleen K.
- Ecology, Vol. 89, Issue 2
Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions
journal, January 2010
- Vitousek, Peter M.; Porder, Stephen; Houlton, Benjamin Z.
- Ecological Applications, Vol. 20, Issue 1
Understanding ecosystem retrogression
journal, November 2010
- Peltzer, Duane A.; Wardle, David A.; Allison, Victoria J.
- Ecological Monographs, Vol. 80, Issue 4
Litterfall, Nutrient Cycling, and Nutrient Limitation in Tropical Forests
journal, February 1984
- Vitousek, Peter M.
- Ecology, Vol. 65, Issue 1
Phosphorus transformations as a function of pedogenesis: A synthesis of soil phosphorus data using Hedley fractionation method
journal, January 2011
- Yang, X.; Post, W. M.
- Biogeosciences, Vol. 8, Issue 10