Abstract
How species coexist despite competing for the same resources that are in limited supply is central to our understanding of the controls on biodiversity1,2. Resource partitioning may facilitate coexistence, as co-occurring species use different sources of the same limiting resource3,4. In plant communities, however, direct evidence for partitioning of the commonly limiting nutrient, phosphorus (P), has remained scarce due to the challenges of quantifying P acquisition from its different chemical forms present in soil5. To address this, we used 33P to directly trace P uptake from DNA, orthophosphate and calcium phosphate into monocultures and mixed communities of plants growing in grassland soil. We show that co-occurring plants acquire P from these important organic and mineral sources in different proportions, and that differences in P source use are consistent with the species’ root adaptations for P acquisition. Furthermore, the net benefit arising from niche plasticity (the gain in P uptake for a species in a mixed community compared to monoculture) correlates with species abundance in the wild, suggesting that niche plasticity for P is a driver of community structure. This evidence for P resource partitioning and niche plasticity may explain the high levels of biodiversity frequently found in P-limited ecosystems worldwide6,7.
This is a preview of subscription content, access via your institution
Access options
Access Nature and 54 other Nature Portfolio journals
Get Nature+, our best-value online-access subscription
$29.99 / 30 days
cancel any time
Subscribe to this journal
Receive 12 digital issues and online access to articles
$119.00 per year
only $9.92 per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
Data availability
The 33P uptake and plant abundance data that support the findings of this study are available at the NERC’s Environmental Information Data Centre with the identifier https://doi.org/10.5285/87cdc267-a8c7-4f59-83b4-1bceaae837ad
References
Schoener, T. Resource partitioning in ecological communities. Science 185, 27–39 (1974).
Silvertown, J. Plant coexistence and the niche. Trends Ecol. Evol. 19, 605–611 (2004).
McKane, R. B. et al. Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415, 68–71 (2002).
Pyke, G. H. Local geographic distributions of bumblebees near Crested Butte, Colorado: competition and community structure. Ecology 63, 555–573 (1982).
Ceulemans, T. et al. Phosphorus resource partitioning shapes phosphorus acquisition and plant species abundance in grasslands. Nat. Plants 3, 16224 (2017).
Lambers, H., Brundrett, M. C., Raven, J. A. & Hopper, S. D. Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 334, 11–31 (2010).
Wassen, M. J., Venterink, H. O., Lapshina, E. D. & Tanneberger, F. Endangered plants persist under phosphorus limitation. Nature 437, 547–550 (2005).
Ceulemans, T. et al. Soil phosphorus constrains biodiversity across European grasslands. Glob. Chang. Biol. 20, 3814–3822 (2014).
Turner, B. L. Resource partitioning for soil phosphorus: a hypothesis. J. Ecol. 96, 698–702 (2008).
Ahmad-Ramli, M. F., Cornulier, T. & Johnson, D. Partitioning of soil phosphorus regulates competition between Vaccinium vitis-idaea and Deschampsia cespitosa. Ecol. Evol. 3, 4243–4252 (2013).
Steidinger, B. S., Turner, B. L., Corrales, A. & Dalling, J. W. Variability in potential to exploit different soil organic phosphorus compounds among tropical montane tree species. Funct. Ecol. 29, 131–130 (2014).
Liu, X. et al. Partitioning of soil phosphorus among arbuscular and ectomycorrhizal trees in tropical and subtropical forests. Ecol. Lett. 21, 713–723 (2018).
Richardson, A. E. et al. Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349, 121–156 (2011).
Erel, R. et al. Soil type determines how root and rhizosphere traits relate to phosphorus acquisition in field-grown maize genotypes. Plant Soil 412, 115–132 (2017).
Critchley, C. N. R. et al. Plant species richness, functional type and soil properties of grasslands and allied vegetation in English Environmentally Sensitive Areas. Grass Forage Sci. 57, 82–92 (2002).
Harley, J. L. & Harley, E. L. A check-list of mycorrhiza in the British flora. New Phytol. 105, 1–102 (1987).
Smith, S. E. & Read, D. Mycorrhizal Symbiosis 3rd edn (Academic Press, 2008).
Joner, E. J., Ravnskov, S. & Jakobsen, I. Arbuscular mycorrhizal phosphate transport under monoxenic conditions using radio-labelled inorganic and organic phosphate. Biotechnol. Lett. 22, 1705–1708 (2000).
Koide, R. T. & Kabir, Z. Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytol. 148, 511–517 (2000).
Shane, M. W., Cawthray, G. R., Cramer, M. D., Kuo, J. & Lambers, H. Specialized ‘dauciform’ roots of Cyperaceae are structurally distinct, but functionally analogous with ‘cluster’ roots. Plant Cell Environ. 29, 1989–1999 (2006).
Tyler, G. & Ström, L. Differing organic acid exudation pattern explains calcifuge and acidifuge behaviour of plants. Ann. Bot. 75, 75–78 (1995).
Schöttelndreier, M., Norddahl, M. M., Ström, L. & Falkengren-Grerup, U. Organic acid exudation by wild herbs in response to elevated Al concentrations. Ann. Bot. 87, 769–775 (2001).
von Wandruszka, R. Phosphorus retention in calcareous soils and the effect of organic matter on its mobility. Geochem. Trans. 7, 6 (2006).
Bünemann, E. K. Assessment of gross and net mineralization rates of soil organic phosphorus – a review. Soil Biol. Biochem. 89, 82–98 (2015).
Carroll, J. A., Caporn, S. J. M., Johnson, D., Morecroft, M. D. & Lee, J. A. The interactions between plant growth, vegetation structure and soil processes in semi-natural acidic and calcareous grasslands receiving long-term inputs of simulated pollutant nitrogen deposition. Environ. Pollut. 121, 363–376 (2003).
Ashton, I. W., Miller, A. E., Bowman, W. D. & Suding, K. N. Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91, 3252–3260 (2010).
Li, L. et al. Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc. Natl Acad. Sci. USA 104, 11192–11196 (2007).
Hinsinger, P. et al. P for two, sharing a scarce resource: soil phosphorus acquisition in the rhizosphere of intercropped species. Plant Physiol. 156, 1078–1086 (2011).
Hunter, R., Hawkins, H. J. & Cramer, M. D. Cluster roots of Proteaceae exude acid phosphatase enzymes as an adaptation to low-P soils, facilitating access to soil organic phosphate. S. Afr. J. Bot. 75, 406 (2009).
Güsewell, S. Regulation of dauciform root formation and root phosphatase activities of sedges (Carex) by nitrogen and phosphorus. Plant Soil 415, 57–72 (2017).
Houle, D., Moore, J.-D., Ouimet, R. & Marty, C. Tree species partition N uptake by soil depth in boreal forests. Ecology 95, 1127–1133 (2014).
Lambers, H., Shane, M. W., Cramer, M. D., Pearse, S. J. & Veneklaas, E. J. Root structure and functioning for efficient acquisition of phosphorus: matching morphological and physiological traits. Ann. Bot. 98, 693–713 (2006).
Lambers, H., Raven, J. A., Shaver, G. R. & Smith, S. E. Plant nutrient acquisition strategies change with soil age. Trends Ecol. Evol. 23, 95–103 (2008).
Johnson, P. A. Soil Survey Record No. 4: Soils in Derbyshire 1 Ch. 3 (Rothamsted Experimental Station, 1971).
Turner, B., Mahieu, N. & Condron, L. M. Phosphorus-31 nuclear magnetic resonance spectral assignments of phosphorus compounds in soil NaOH–EDTA extracts. Soil Sci. Soc. Am. J. 67, 497–510 (2003).
Horswill, P., O’Sullivan, O., Phoenix, G. K., Lee, J. A. & Leake, J. R. Base cation depletion, eutrophication and acidification of species-rich grasslands in response to long-term simulated nitrogen deposition. Environ. Pollut. 155, 336–349 (2008).
Robertson, I. G. Organic Phosphorus (P) in Agricultural Soil and the Ability of Wheat to Use This as a P Source. PhD thesis, Univ. Sheffield (2018).
Feinberg, A. P. & Vogelstein, B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6–13 (1983).
Feinberg, A. P. & Vogelstein, B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Addendum. Anal. Biochem. 137, 266–267 (1984).
Murphy, J. & Riley, J. P. A modified single solution method for the determination of phosphate in natural waters. Anal. Chim. Acta 27, 31–36 (1962).
Acknowledgements
This research was supported by the NERC, UK (grant no. NE/H01179X/1, awarded to G.K.P., D.D.C. and J.R.L.). We thank I. Johnson for technical assistance.
Author information
Authors and Affiliations
Contributions
G.K.P., D.D.C. and J.R.L. designed the study. D.A.J. and S.P.M. undertook the experimental work with the assistance of G.K.P., J.R.L. and D.D.C. G.K.P. analysed the data and wrote the manuscript with assistance from D.D.C., J.R.L., D.A.J. and S.P.M.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Peer review information Nature Plants thanks Tobias Ceulemans and the other, anonymous, reviewers for their contribution to the peer review of this work.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data
Extended Data Fig. 1 Total biomass (dry weight) of each species per pot in monocultures and mixed communities receiving P sources.
a – c. P sources supplied were (a) orthophosphate, (b) calcium phosphate, and (c) DNA. Large symbols are mean biomass, error bars are standard error (n=7). Different P sources do not influence biomass production since sources were added in the last 6 days of 30 weeks of growth. Dotted line represents 1:7 line; assuming that biomass produced in a mixed community of 7 species will be 1/7th the biomass in monoculture. Species that produce more biomass in mixed communities than expected from their monoculture biomass are above this line.
Extended Data Fig. 2 Uptake from 33P sources over 6 days following injection into soil.
a – c. Uptake from 33P labelled orthophosphate (a), calcium phosphate (b), and DNA (c) determined from daily monitoring of grassland community swards using a Geiger counter. Main (large) data points are means, error bars are one standard error of the mean (n=7 independent plant community pot, except for (a) where n=6 for the mixed community data due to an over-application of 33P error for one pot). For clarity, individual data points are offset from means and error bars.
Extended Data Fig. 3 Uptake of 33P per unit biomass from high and low specific activity calcium phosphate.
a,b. 33P shoot concentrations of species grown in (a) monocultures and (b) mixed communities. Main (large) data points are means, error bars are one standard error of the mean. Dashed line represents 1:1 line of equal uptake between low and high specific activity calcium phosphate sources. * indicates significant difference (t-test, 2 tailed, log10+1 transformed data, false error rate adjusted, n=5 biomass samples) in uptake by that species between high and low specific activity sources in (a) only for P. lanceolata (t8=-7.74, P<0.001) and R. acetosa (t8=6.15, P<0.001).
Extended Data Fig. 4 Recalculated dataset on relative use of different 33P sources of orthophosphate, calcium phosphate and DNA in (a) monocultures, and (b) in mixed communities.
Uptake from each P source is expressed as a % (its relative use or ‘preference’) calculated as the 33P per g plant tissue from that source as a % of the summed 33P per gram plant tissue from all three sources. Bars are means and error bars are one standard error of the mean (n=7 independent biomass samples for each species receiving any one P source; exceptions where n=6 or 5 are given in Fig. 1).
Extended Data Fig. 5 Recalculated relationship between species abundance in the wild and the benefit of niche plasticity for P uptake (that is change in 33P uptake from all forms for a species in monocultures and mixed communities).
Dotted line indicates linear regression (R2 = 16.5; P < 0.001). Main (large) data points are means, error bars are one standard error of the mean. % cover data taken from 30 surveyed quadrats at the limestone grassland where the soil for the experiment was sourced, hence n=30 independent survey samples for each species.
Supplementary information
Source data
Source Data Fig. 1
Statistical source data.
Source Data Fig. 2
Statistical source data.
Source Data Fig. 3
Statistical source data.
Source Data Extended Data Fig. 1
Statistical source data.
Source Data Extended Data Fig. 2
Statistical source data.
Source Data Extended Data Fig. 3
Statistical source data.
Source Data Extended Data Fig. 4
Statistical source data.
Source Data Extended Data Fig. 5
Statistical source data.
Rights and permissions
About this article
Cite this article
Phoenix, G.K., Johnson, D.A., Muddimer, S.P. et al. Niche differentiation and plasticity in soil phosphorus acquisition among co-occurring plants. Nat. Plants 6, 349–354 (2020). https://doi.org/10.1038/s41477-020-0624-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/s41477-020-0624-4
This article is cited by
-
Soil phosphorus availability affects niche characteristics of dominant C3 perennial and sub-dominant C4 annual species in a typical temperate grassland of northern China
Plant and Soil (2024)
-
Root traits and plasticity differences explain complementarity between co-existing species in phosphorus-limited grassland
Plant and Soil (2024)
-
Varying soil moisture and pH with alpine meadow degradation affect nitrogen preference of dominant species
Biology and Fertility of Soils (2024)
-
Grassland management regimes regulate soil phosphorus fractions and conversion between phosphorus pools in semiarid steppe ecosystems
Biogeochemistry (2023)
-
Metabolic footprints in phosphate-starved plants
Physiology and Molecular Biology of Plants (2023)