Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Niche differentiation and plasticity in soil phosphorus acquisition among co-occurring plants

Nature Plants volume 6, pages 349–354 (2020)Cite this article

Subjects

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

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Relative use of different P sources.
Fig. 2: Niche shifts in P source use between monocultures and mixed communities.
Fig. 3: Relationship between species abundance and the benefit of niche plasticity for P uptake.

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

  1. Schoener, T. Resource partitioning in ecological communities. Science 185, 27–39 (1974).

    Article  CAS  Google Scholar 

  2. Silvertown, J. Plant coexistence and the niche. Trends Ecol. Evol. 19, 605–611 (2004).

    Article  Google Scholar 

  3. 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).

    Article  CAS  Google Scholar 

  4. Pyke, G. H. Local geographic distributions of bumblebees near Crested Butte, Colorado: competition and community structure. Ecology 63, 555–573 (1982).

    Article  Google Scholar 

  5. Ceulemans, T. et al. Phosphorus resource partitioning shapes phosphorus acquisition and plant species abundance in grasslands. Nat. Plants 3, 16224 (2017).

    Article  Google Scholar 

  6. 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).

    Article  CAS  Google Scholar 

  7. Wassen, M. J., Venterink, H. O., Lapshina, E. D. & Tanneberger, F. Endangered plants persist under phosphorus limitation. Nature 437, 547–550 (2005).

    Article  CAS  Google Scholar 

  8. Ceulemans, T. et al. Soil phosphorus constrains biodiversity across European grasslands. Glob. Chang. Biol. 20, 3814–3822 (2014).

    Article  Google Scholar 

  9. Turner, B. L. Resource partitioning for soil phosphorus: a hypothesis. J. Ecol. 96, 698–702 (2008).

    Article  CAS  Google Scholar 

  10. 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).

    Article  Google Scholar 

  11. 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).

    Google Scholar 

  12. Liu, X. et al. Partitioning of soil phosphorus among arbuscular and ectomycorrhizal trees in tropical and subtropical forests. Ecol. Lett. 21, 713–723 (2018).

    Article  Google Scholar 

  13. Richardson, A. E. et al. Plant and microbial strategies to improve the phosphorus efficiency of agriculture. Plant Soil 349, 121–156 (2011).

    Article  CAS  Google Scholar 

  14. 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).

    Article  CAS  Google Scholar 

  15. 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).

    Article  Google Scholar 

  16. Harley, J. L. & Harley, E. L. A check-list of mycorrhiza in the British flora. New Phytol. 105, 1–102 (1987).

    Article  Google Scholar 

  17. Smith, S. E. & Read, D. Mycorrhizal Symbiosis 3rd edn (Academic Press, 2008).

  18. 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).

    Article  CAS  Google Scholar 

  19. Koide, R. T. & Kabir, Z. Extraradical hyphae of the mycorrhizal fungus Glomus intraradices can hydrolyse organic phosphate. New Phytol. 148, 511–517 (2000).

    Article  CAS  Google Scholar 

  20. 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).

    Article  CAS  Google Scholar 

  21. Tyler, G. & Ström, L. Differing organic acid exudation pattern explains calcifuge and acidifuge behaviour of plants. Ann. Bot. 75, 75–78 (1995).

    Article  CAS  Google Scholar 

  22. 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).

    Article  Google Scholar 

  23. von Wandruszka, R. Phosphorus retention in calcareous soils and the effect of organic matter on its mobility. Geochem. Trans. 7, 6 (2006).

    Article  Google Scholar 

  24. Bünemann, E. K. Assessment of gross and net mineralization rates of soil organic phosphorus – a review. Soil Biol. Biochem. 89, 82–98 (2015).

    Article  Google Scholar 

  25. 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).

    Article  CAS  Google Scholar 

  26. 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).

    Article  Google Scholar 

  27. 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).

    Article  CAS  Google Scholar 

  28. 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).

    Article  CAS  Google Scholar 

  29. 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).

    Article  Google Scholar 

  30. Güsewell, S. Regulation of dauciform root formation and root phosphatase activities of sedges (Carex) by nitrogen and phosphorus. Plant Soil 415, 57–72 (2017).

    Article  Google Scholar 

  31. 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).

    Article  CAS  Google Scholar 

  32. 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).

    Article  Google Scholar 

  33. 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).

    Article  Google Scholar 

  34. Johnson, P. A. Soil Survey Record No. 4: Soils in Derbyshire 1 Ch. 3 (Rothamsted Experimental Station, 1971).

  35. 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).

    Article  CAS  Google Scholar 

  36. 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).

    Article  CAS  Google Scholar 

  37. 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).

  38. Feinberg, A. P. & Vogelstein, B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6–13 (1983).

    Article  CAS  Google Scholar 

  39. Feinberg, A. P. & Vogelstein, B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Addendum. Anal. Biochem. 137, 266–267 (1984).

    Article  CAS  Google Scholar 

  40. 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).

    Article  CAS  Google Scholar 

Download references

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

  1. Department of Animal and Plant Sciences, University of Sheffield, Sheffield, UK

    Gareth K. Phoenix, David A. Johnson, Stephen P. Muddimer, Jonathan R. Leake & Duncan D. Cameron

Authors
  1. Gareth K. Phoenix
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David A. Johnson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephen P. Muddimer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jonathan R. Leake
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Duncan D. Cameron
    View author publications

    You can also search for this author in PubMed Google Scholar

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

Correspondence to Gareth K. Phoenix.

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.

Source data

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.

Source data

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).

Source data

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).

Source data

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.

Source data

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-020-0624-4

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing