Skip to main content
SpringerLink
Log in

15N-nitrate-labelling demonstrates a size symmetric competitive effect on belowground resource uptake

  • Published:
Plant Ecology Aims and scope Submit manuscript

Abstract

Strong hints exist that belowground competition is generally size-symmetric. While this has frequently been shown by use of integrative indicators like growth or biomass, resource-focussed approaches are still lacking, especially those investigating the competitive effect. Here, we present a correlation between neighbour plants’ root sizes and their competitive effect on their target plants’ nitrate uptake. This was derived from a controlled field experiment where intra- and interspecific combinations of five different herbaceous species from nutrient poor sand ecosystems were examined in an additive design. Short-term pulses of 15N-labelled nitrate were applied between competing pairs of plant individuals. The sizes of neighbour root systems had high explanatory power for the competitive effect on target plants’ nitrate uptake. Equally important, a curve fitting approach revealed that the competitive effect based on 15N-uptake matched predictions of a size-symmetric interaction. With 66% of the variation in competitive effect on nitrate uptake explained by root system size, the degree to which root size results in a belowground overlap of zones of influence is crucial. Within this overlap, further attributes like architecture or uptake capacity may be important. Our data represent experimental support for a size symmetric competitive effect for a specific belowground resource. Since this is not consistent with an overproportional size advantage when mobile soil resources are limiting, it suggests that the survival of small individuals or species should be facilitated by the symmetric nature of belowground competitive effects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aerts R, Boot RGA, van der Aart PJM (1991) The relation between above- and belowground biomass allocation patterns and competitive ability. Oecologia 87:551–559

    Article  Google Scholar 

  • Akaike H (1978) A Bayesian analysis of the minimum AIC procedure. Ann Inst Stat Math 30:9–14

    Article  Google Scholar 

  • Bartelheimer M, Steinlein T, Beyschlag W (2006) Aggregative root placement: a feature during interspecific competition in inland sand-dune habitats. Plant Soil 280:101–114

    Article  CAS  Google Scholar 

  • Berendse F (1990) Organic matter accumulation and nitrogen mineralization during secondary succession in heathland ecosystems. J Ecol 78:413–427

    Article  Google Scholar 

  • Berger AG, McDonald AJ, Riha SJ (2006) Scaling plant size to below-ground zone of influence in annuals under contrasting competitive environments. Funct Ecol 20:770–777

    Article  Google Scholar 

  • Berntson GM, Wayne PM (2000) Characterizing the size dependence of resource acquisition within crowded plant populations. Ecology 81:1072–1085

    Google Scholar 

  • Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83

    Article  CAS  Google Scholar 

  • Boorman LA (1982) Some plant growth patterns in relation to the sand dune habitat. J Ecol 70:607–614

    Article  Google Scholar 

  • Brady DJ, Gregory PJ, Fillery IRP (1993) The contribution of different regions of the seminal roots of wheat to uptake of nitrate from soil. Plant Soil 155:155–158

    Article  Google Scholar 

  • Cahill JF Jr (2003) Lack of relationship between below-ground competition and allocation to roots in 10 grassland species. J Ecol 91:532–540

    Article  Google Scholar 

  • Cahill JF Jr, Casper BB (2000) Investigating the relationship between neighbor root biomass and belowground competition: field evidence for symmetric competition belowground. OIKOS 90:311–320

    Article  Google Scholar 

  • Cahill JF Jr, Kembel SW, Gustafson DJ (2005) Differential genetic influences on competitive effect and response in Arabidopsis thaliana. J Ecol 93:958–967

    Article  Google Scholar 

  • Caldwell MM, Eissenstat DM, Richards JH, Allen FM (1985) Competition for phosphorus: differential uptake from dual-isotope-labeled soil interspaces between shrub and grass. Science 229:384–386

    Article  PubMed  CAS  Google Scholar 

  • Casper BB, Jackson RB (1997) Plant competition underground. Annu Rev Ecol Syst 28:545–570

    Article  Google Scholar 

  • Casper BB, Schenk HJ, Jackson RB (2003) Defining a plant’s belowground zone of influence. Ecology 84:2313–2321

    Article  Google Scholar 

  • Clarkson DT, Hanson JB (1980) The mineral nutrition of higher plants. Annu Rev Plant Physiol 31:239–298

    Article  CAS  Google Scholar 

  • Conolly J, Wayne P (1996) Asymmetric competition between plant species. Oecologia 108:311–320

    Google Scholar 

  • Craine JM, Fargione J, Sugita S (2005) Supply preemption, not concentration reduction, is the mechanism of competition for nutrients. New Phytol 166:933–940

    Article  PubMed  Google Scholar 

  • Enquist BJ, Niklas KJ (2002) Global allocation rules for patterns of biomass partitioning in seed plants. Science 295:1517–1520

    Article  PubMed  CAS  Google Scholar 

  • Fitter AH, Williamson L, Linkohr B, Leyser O (2002) Root system achitecture determines fitness in an Arabidopsis mutant in competition for immobile phosphat ions but not for nitrate ions. Proc R Soc Lond 269:2017–2022

    Article  CAS  Google Scholar 

  • Forde BG (2000) Nitrate transporters in plants: structure, function and regulation. Biochim Biophys Acta 165:219–235

    Google Scholar 

  • Fransen B, De Kroon H, Berendse F (2001) Soil nutrient heterogeneity alters competition between two perennial grass species. Ecology 82:2534–2546

    Article  Google Scholar 

  • Freckleton RP, Watkinson AR (2001) Asymmetric competition between plant species. Funct Ecol 15:615–623

    Article  Google Scholar 

  • Gages DJ, Westcott M (1978) Zone of influence models for competition in plantations. Adv Appl Probab 10:499–537

    Article  Google Scholar 

  • Goldberg DE (1990) Components of resource competition in plant communities. In: Grace JB, Tilman D (eds) Perspectives on plant competition. Academic Press, San Diego, London

    Google Scholar 

  • Goldberg DE, Fleetwood L (1987) Competitive effect and response in four annual plants. J Ecol 75:1131–1143

    Article  Google Scholar 

  • Goldberg DE, Landa K (1991) Competitive effect and response: hierarchies and correlated traits in the early stages of competition. J Ecol 79:1013–1030

    Article  Google Scholar 

  • Goldberg DE, Werner PA (1983) Equivalence of competitors in plant communities: a null-hypothesis and a field experimental approach. Am J Bot 70:1098–1104

    Article  Google Scholar 

  • Hegi G (1979) Illustrierte Flora von Mittel-europa. Verlag Paul Parey, Berlin, Hamburg

    Google Scholar 

  • Hikosaka K, Hirose T (2001) Nitrogen uptake and use by competing individuals in a Xanthium canadense stand. Oecologia 126:174–181

    Article  Google Scholar 

  • Hodge A (2006) Plastic plants and patchy soils. J Exp Bot 57:401–411

    Article  PubMed  CAS  Google Scholar 

  • Hodge A, Robinson D, Griffiths B, Fitter AH (1999) Why plants bother: root proliferation results in increased nitrogen capture from an organic patch when two grasses compete. Plant Cell Environ 22:811–820

    Article  Google Scholar 

  • Keddy PA, Twolan-Strutt L, Wisheu IC (1994) Competitive effect and response rankings in 20 wetland plants: are they consistent across three environments? J Ecol 82:635–643

    Article  Google Scholar 

  • Law R, Watkinson AR (1987) Response-surface analysis of two-species competition: an experiment on Phleum arenarium and Vulpia fasciculata. J Ecol 75:871–886

    Article  Google Scholar 

  • Markham JH, Chanway CP (1996) Measuring plant neighbour effects. Funct Ecol 10:548–549

    Google Scholar 

  • Munoz AE, Weaver RW (1999) Competition between subterranean clover and ryegrass for uptake of 15N-labeled fertilizer. Plant Soil 211:173–178

    Article  CAS  Google Scholar 

  • Näsholm T, Huss-Danell K, Högberg M (2000) Uptake of organic nitrogen in the field by four agriculturally important plant species. Ecology 81:1155–1161

    Google Scholar 

  • Newbery DM, Newman EI (1978) Competition between grassland plants of different initial sizes. Oecologia 33:361–380

    Article  Google Scholar 

  • Pless H (1995) Pflanzensoziologische Untersuchungen der Trockenrasen an den Hängen des Odertales zwischen Seelow und Frankfurt (Oder). Naturschutz und Landschaftspflege in Brandenburg 3:27–31

    Google Scholar 

  • Rajaniemi T (2003) Evidence for size asymmetry of belowground competition. Basic Appl Ecol 4:239–247

    Article  Google Scholar 

  • Remans T, Nacry P, Pervent M, Girin T, Tillard P, Lepetit M, Gojon A (2006) A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis. Plant Physiol 140:909–921

    Article  PubMed  CAS  Google Scholar 

  • Robe WE, Griffiths H, Sleep D, Quarmby C (1994) Nitrogen partitioning and assimitlation: methods for the extraction, separation and mass spectrometric analysis of nitrate, amino acid and soluble protein pools from individual plant following 15N labelling. Plant Cell Environ 17:1073–1079

    Article  CAS  Google Scholar 

  • Robinson D, Hodge A, Griffiths B, Fitter AH (1999) Plant root proliferation in nitrogen-rich patches confers competitive advantage. Proc R Soc Lond 266:431–435

    Article  Google Scholar 

  • Schwinning S, Weiner J (1998) Mechanisms determining the degree of size asymmetry in competition among plants. Oecologia 113:447–455

    Article  Google Scholar 

  • Stevens CJ, Dise NB, Mountford JO, Gowing DJG (2004) Impact of nitrogen deposition on the species richness of grasslands. Science 303:1876–1879

    Article  PubMed  CAS  Google Scholar 

  • Tilman D, Wedin D (1991) Plant traits and resource reduction for five grasses growing on a nitrogen gradient. Ecology 72:685–700

    Article  Google Scholar 

  • Tilman D, Wedin D, Knops J (1996) Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379:718–720

    Article  CAS  Google Scholar 

  • Vojtech E, Turnball LA, Hector A (2007) Differences in light interception in grass monocultures predict short-term competitive outcomes under productive conditions. PLoS ONE 2, e499. doi:10.1371/journal.pone.0000499

  • von Wettberg EJ, Weiner J (2003) Larger Triticum aestivum plants do not preempt nutrient-rich patches in a glasshouse experiment. Plant Ecol 169:85–92

    Article  Google Scholar 

  • Wassen MJ, Olde Venterink H, Lapshina ED, Tanneberger F (2005) Endangered plants persist under phosphorus limitation. Nature 437:547–550

    Article  PubMed  CAS  Google Scholar 

  • Weigelt A, Röttgermann M, Steinlein T, Beyschlag W (2000) Influence of water availability on competitive interactions between plant species on sandy soils. Folia Geobot 35:169–178

    Article  Google Scholar 

  • Weigelt A, Steinlein T, Beyschlag W (2005) Competition in inland dunes: the impact of water availability on below-ground processes. Plant Ecol 176:57–68

    Article  Google Scholar 

  • Weigelt A, Schumacher J, Walther T, Bartelheimer M, Steinlein T, Beyschlag W (2007) Identifying mechanisms of competition in multi-species communities. J Ecol 95:53–64

    Article  Google Scholar 

  • Weiner J (1986) How competition for light and nutrients affects size variability in Ipomoea tricolor populations. Ecology 67:1425–1427

    Article  Google Scholar 

  • Weiner J, Wright DB, Castro S (1997) Symmetry of belowground competition between Kochia scoparia individuals. OIKOS 79:85–91

    Article  Google Scholar 

  • Wijesinghe DK, John AJ, Beurskens S, Hutchings MJ (2001) Root system size and precision in nutrient foraging: responses to spatial pattern of nutrient supply in six herbaceous species. J Ecol 89:972–983

    Article  Google Scholar 

  • Wilson SD, Keddy PA (1986) Measuring diffuse competition along an environmental gradient: results from a shoreline plant community. Am Nat 127:862–869

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. Christiane Werner for valuable scientific advice. Further we thank Barbara Teichner for carrying out the mass-spectrometry measurements and Elke Furlkröger for skilful technical assistance. The help of Holger Abel, Marcel Austenfeld, Jürgen Birtsch, Sven Luhmann, Birgit Peperkorn, Simone Sommer and Melanie Wittland during plant harvest and sample preparation is gratefully acknowledged.

Author information

Authors and Affiliations

  1. Chair of Experimental and Systems Ecology, University of Bielefeld, Universitätsstr. 25, 33615, Bielefeld, Germany

    Maik Bartelheimer, Thomas Steinlein & Wolfram Beyschlag

  2. Institute of Botany, Faculty of Biology and Preclinical Medicine, University of Regensburg, 93040, Regensburg, Germany

    Maik Bartelheimer

Authors
  1. Maik Bartelheimer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas Steinlein
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wolfram Beyschlag
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maik Bartelheimer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bartelheimer, M., Steinlein, T. & Beyschlag, W. 15N-nitrate-labelling demonstrates a size symmetric competitive effect on belowground resource uptake. Plant Ecol 199, 243–253 (2008). https://doi.org/10.1007/s11258-008-9429-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11258-008-9429-7

Keywords

Search

Navigation