The story of nutrient limitation originated from 1840s, when the famous German chemist Justus Freiherr von Liebig first proposed the Liebig’s Law of the Minimum based on experiments that added essential nutrients to improve crop productivity (von Liebig, 1843). One hundred years later, Chapin III et al. (1986) investigated the concept of nutrient limitation in natural plant communities and proposed several differences from that in agriculture, especially the diverse nutrient use strategies for different plant species. In 1991, Vitousek and Howarth (1991) concluded that “there is substantial evidence that nitrogen limits net primary production much of the time in most terrestrial biomes and many marine ecosystems”. Since the 2000s, numerous ecologists assessed nitrogen and phosphorus limitation based on meta-analyses of global nutrient addition experiments and they concluded a global distribution of nitrogen and phosphorus limitation in terrestrial ecosystems (Elser et al., 2007; LeBauer and Treseder, 2008; Fay et al., 2015). Meanwhile, many others have also estimated nitrogen and phosphorus limitation via indirect indicators (Koerselman and Meuleman, 1996; Güsewell, 2004; Vergutz et al. 2012; Han et al., 2013). Although these efforts have greatly improved our understanding of nutrient limitation, global patterns of terrestrial nitrogen and phosphorus limitation still remain a fundamental question for the fields of terrestrial ecology and biogeochemistry.
I have been thinking about the answer to this question since the time when I conducted a nitrogen addition experiment in a boreal forest for my Ph.D thesis in Peking University (2008-2013). I found that nutrient addition experiments are costly, and a variety of growth response indicators were used by different researchers, complicating the challenging goal of disentangling the spatial patterns of global nutrient limitation. After completing my Ph.D work in Peking University, I moved to Beijing Normal University for a postdoc during 2013 and 2015. I continued to work in Beijing Normal University and became an associated professor in 2016. Since then, I have returned to the issue to solve the puzzle of global nitrogen and phosphorus limitation.
Mass ratios of leaf nitrogen and phosphorus have been used to indicate nitrogen and phosphorus limitation (Koerselman and Meuleman, 1996; Güsewell, 2004), but this approach has been shown to have large uncertainties by a recent assessment (Yan et al., 2017). Some other studies have tried to link leaf nitrogen and phosphorus resorption efficiencies to nutrient limitation (Vergutz et al. 2012; Reed et al., 2012; Han et al., 2013), but a theoretical framework is still lacking. As inspired by the stoichiometric homeostasis theory and Liebig’s Law of the Minimum, I proposed a theoretical framework to test nutrient limitation based on the ratio of plant leaf nitrogen and phosphorus resorption efficiencies at the ecosystem scale (see more details in Du et al., 2020). In nearly two years of work, I collected data of paired leaf nitrogen resorption efficiency and phosphorus resorption efficiency from literature and made initial assessments of patterns in nitrogen and phosphorus limitation.
In October, 2017, I made a short visit to Professor Rob Jackson at Stanford University, where we collaborated to improve the work and finished a first draft of our manuscript. His lab has long been interested in nutrient limitation across ecosystems and the role of plants in both structuring and responding to global nutrient availability (e.g., Jobbágy and Jackson 2001; Vergutz et al. 2012; Terrer et al. 2019). Our team was strengthened when Rob introduced his postdocs César Terrer, Adam Pellegrini and Anders Ahlström to join in various aspects of the analyses. We also involved Dr. Caspar J. van Lissa, an assistant professor of Methods & Statistics at Utrecht University, to improve our statistical analyses. We discussed new ideas, reanalyzed data, validated predictions of global nitrogen and phosphorus limitation by comparing to a newly constructed database of field nutrient addition experiments, and revised the manuscript at least ten times. I have enjoyed working with this great team and I really thank Rob for organizing it. I believe that we will work together more in the future.
Our results suggest that 18% of Earth’s land area, excluding cropland, urban, and glacial areas, is strongly limited by N alone, whereas 43 % is strongly P limited. The remaining 39% of natural terrestrial land area could be co-limited by N and P or weakly limited by either nutrient alone. Nitrogen limitation is more common in boreal forests, tundra, temperate coniferous forests and montane grasslands and shrublands, whereas phosphorous limitation is more common in tropical and subtropical forests, temperate broadleaf and mixed forests, deserts, Mediterranean biomes and grasslands, savannas and shrublands in tropical, subtropical and temperate regions. Our work provides a new framework for testing nutrient limitation and an empirical benchmark of N and P limitation for models to constrain predictions of the terrestrial C sink. It will help to improve representation of nutrient limitation in Earth system models and identify hotspots of future land C sinks in response to climate change and rising carbon dioxide concentrations. Although we looked at nutrient limitation in relatively natural ecosystems, there is a potential to extend our approach to human-dominated or managed ecosystems, such as commercial plantations and urban forests. This will lead to better nutrient management by diagnosing the limiting nutrients in these ecosystems.
Global patterns of terrestrial nitrogen and phosphorus limitation (Du et al., 2020, Nature Geoscience)
At the ecosystem scale, the ratio of average leaf nitrogen resorption efficiency (NRE) to phosphorus resorption efficiency (PRE) weighted by the leaf mass of all species is a theoretical indicator of N or P limitation. Because species-specific leaf mass is rarely reported together with NRE and PRE, in the current analysis we had to use the ratio of site-averaged NRE to site-averaged PRE of dominant species as an approximate indicator. Future studies would benefit from additional data to support analyses using ecosystem mean NRE/PRE weighted by species-specific leaf mass or abundance. We recommend researchers conducting field studies measure such variables whenever possible and compare results to those of nutrient fertilization experiments.
Combining paired field measurements and fertilization experiments to understand ecosystem nutrient limitation (Credit to Enzai Du).
To find out more, read the paper following the link: https://www.nature.com/articles/s41561-019-0530-4
Chapin III, F. S., Vitousek, P. M., & Van Cleve, K. The nature of nutrient limitation in plant communities. Am. Nat. 127, 48–58 (1986).
Du, E., et al. Global patterns of terrestrial nitrogen and phosphorus limitation. Nat. Geosci. https://www.nature.com/articles/s41561-019-0530-4 (2020).
Elser, J.J. et al. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 10, 1135–1142 (2007).
Fay, P. A. et al. Grassland productivity limited by multiple nutrients. Nat. Plants 1, 15080 (2015).
Güsewell, S. N:P ratios in terrestrial plants: variation and functional significance. New Phytol. 164, 243–266 (2004).
Han, W., Tang, L., Chen, Y. & Fang, J. Relationship between the relative limitation and resorption efficiency of nitrogen vs phosphorus in woody plants. PLoS One 8, e83366 (2013).
Jobbágy, E.G. & Jackson, R.B. The distribution of soil nutrients with depth: global patterns and the imprint of plants. Biogeochemistry 53:51-77 (2001).
Koerselman, W. & Meuleman, A.F. The vegetation N: P ratio: a new tool to detect the nature of nutrient limitation. J. Appl. Ecol. 33, 1441–1450 (1996).
LeBauer, D.S. & Treseder, K.K. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89, 371–379 (2008).
Reed, S.C., Townsend, A.R., Davidson, E.A. & Cleveland, C.C. Stoichiometric patterns in foliar nutrient resorption across multiple scales. New Phytol. 196, 173–180 (2012).
Terrer, C. et al. Nitrogen and phosphorus constrain the CO2 fertilization of global plant biomass. Nat. Clim. Change 9, 684-689 (2019).
Vergutz, L., Manzoni, S. Porporato, A., Novais, R.F. & Jackson, R.B. Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol. Monogr. 82, 205-220 (2012).
Vitousek, P. M., & Howarth, R. W. Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13, 87–115 (1991).
von Liebig, J. Die Chemie in ihrer Anwendung auf Agricultur und Physiologie. 3e Aufl., Braunschweig: F. Vieweg und Sohn (1843).
Yan, Z., Tian, D., Han, W., Tang, Z. & Fang, J. An assessment on the uncertainty of the nitrogen to phosphorus ratio as a threshold for nutrient limitation in plants. Ann. Bot-London 120, 937–942 (2017).