Plant Ecology

, Volume 217, Issue 7, pp 843–856 | Cite as

Temporal and small-scale spatial variation in grassland productivity, biomass quality, and nutrient limitation

  • Valentin H. KlausEmail author
  • Steffen Boch
  • Runa S. Boeddinghaus
  • Norbert Hölzel
  • Ellen Kandeler
  • Sven Marhan
  • Yvonne Oelmann
  • Daniel Prati
  • Kathleen M. Regan
  • Barbara Schmitt
  • Elisabeth Sorkau
  • Till Kleinebecker


Characterization of spatial and temporal variation in grassland productivity and nutrition is crucial for a comprehensive understanding of ecosystem function. Although within-site heterogeneity in soil and plant properties has been shown to be relevant for plant community stability, spatiotemporal variability in these factors is still understudied in temperate grasslands. Our study aimed to detect if soil characteristics and plant diversity could explain observed small-scale spatial and temporal variability in grassland productivity, biomass nutrient concentrations, and nutrient limitation. Therefore, we sampled 360 plots of 20 cm × 20 cm each at six consecutive dates in an unfertilized grassland in Southern Germany. Nutrient limitation was estimated using nutrient ratios in plant biomass. Absolute values of, and spatial variability in, productivity, biomass nutrient concentrations, and nutrient limitation were strongly associated with sampling date. In April, spatial heterogeneity was high and most plots showed phosphorous deficiency, while later in the season nitrogen was the major limiting nutrient. Additionally, a small significant positive association between plant diversity and biomass phosphorus concentrations was observed, but should be tested in more detail. We discuss how low biological activity e.g., of soil microbial organisms might have influenced observed heterogeneity of plant nutrition in early spring in combination with reduced active acquisition of soil resources by plants. These early-season conditions are particularly relevant for future studies as they differ substantially from more thoroughly studied later season conditions. Our study underlines the importance of considering small spatial scales and temporal variability to better elucidate mechanisms of ecosystem functioning and plant community assembly.


Nitrogen Phosphorus Biodiversity Exploratories Project Nutrient concentrations Biodiversity–ecosystem functioning Growth limitation 



We thank Jörg Lüling for untiring work while conducting biomass analyses in the laboratory, the managers of the Exploratory Schwäbische Alb, Swen Renner and Kirsten Reichel-Jung, for their work in maintaining the plot and project infrastructure, Simone Pfeiffer and Christiane Fischer giving support through the central office, Michael Owonibi for managing the central data base and Markus Fischer, Eduard Linsenmair, Dominik Hessenmöller, Jens Nieschulze, Ingo Schöning, François Buscot, Ernst-Detlef Schulze, Wolfgang W. Weisser, and the late Elisabeth Kalko for their role in setting up the Biodiversity Exploratories project.


The work has been funded by the DFG Priority Program 1374 “Infrastructure-Biodiversity-Exploratories” (FI 1246/6-1, FI 1246/9-1, HO 3830/2-2, KA 1590/8-2, OE 516/1-2). All funding bodies are listed and no funding body was involved in conducting and publishing the experiment and its results.

Compliance with ethical standards

Conflict of interest

Thus, the authors declare that they have no conflict of interest.

Field work permit

Field work permits were issued by the responsible state environmental offices of Baden-Württemberg.

Research involving human and animal rights

The study did not involve any experiments with humans or animals.


  1. Abbas M, Ebeling A, Oelmann Y, Ptacnik R, Roscher C, Weigelt A, Weisser WW, Wilke W, Hillebrand H (2013) Biodiversity effects on plant stoichiometry. PLoS One 8(3):e58179CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ågren GI (2008) Stoichiometry and nutrition of plant growth in natural communities. Annu Rev Ecol Evol Syst 39:153–170CrossRefGoogle Scholar
  3. Allan E, Manning P, Prati D, Grassein F, Alt F, Binkenstein J, Blaser S, Blüthgen N, Hölzel N, Klaus VH, Kleinebecker T, Morris E-K, Oelmann Y, Renner SC, Rillig MC, Schäfer M, Schloter M, Schmitt B, Schöning I, Schrumpf M, Solly E, Sorkau E, Steckel J, Steffen-Dewenter I, Stempfhuber B, Trumbore S, Weiner CN, Weisser WW, Werner W, Westphal C, Wilcke W, Fischer M (2015) Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition. Ecol Lett 18:834–843CrossRefPubMedPubMedCentralGoogle Scholar
  4. Balvanera P, Pfisterer AB, Buchmann N, He JS, Nakashizuka T, Raffaelli D (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156CrossRefPubMedGoogle Scholar
  5. Bazzaz FA, Catovsky S (2001) Resource partitioning. Encyclopedia of Biodiversity. Academic Press, San DiegoGoogle Scholar
  6. Deppe U (2015) Wetterstation Riethein Lichse website. Accessed 4 Nov 2015
  7. Fischer M, Bossdorf O, Gockel S, Hänsel F, Hemp A, Hessenmöller D, Korte G, Nieschulze J, Pfeiffer S, Prati D, Renner S, Schöning I, Schumacher U, Wells K, Buscot F, Kalko EKV, Linsenmair KE, Schulze E-D, Weisser WW (2010) Implementing large-scale and long-term functional biodiversity research: the biodiversity Exploratories. Basic Appl Ecol 11:473–485CrossRefGoogle Scholar
  8. Fridley JD, Grime JP, Askew AP, Moser B, Stevens CJ (2011) Soil heterogeneity buffers community response to climate change in species-rich grassland. Glob Chang Biol 17:2002–2011CrossRefGoogle Scholar
  9. Fujita Y, Olde Venterink H, van Bodegom PM, Douma JC, Heil GW, Hölzel N, Jabłońska E, Kotowski W, Okruszko T, Pawlikowski P, de Ruiter PC, Wassen MJ (2014) Low investment in sexual reproduction threatens plants adapted to phosphorus limitation. Nature 505:82–86CrossRefPubMedGoogle Scholar
  10. Gavito ME, Schweiger P, Jakobsen I (2003) P uptake by arbuscular mycorrhizal hyphae: effect of soil temperature and atmospheric CO2 enrichment. Glob Chang Biol 9:106–116CrossRefGoogle Scholar
  11. Gilliam FS, Dick DA (2010) Spatial heterogeneity of soil nutrients and plant species in herb-dominated communities of contrasting land use. Plant Ecol 209:83–94CrossRefGoogle Scholar
  12. Gross N, Bloor JMG, Louault F, Maire V, Soussana JF (2009) Effects of land-use change on productivity depend on small scale plant species diversity. Basic Appl Ecol 10:687–696CrossRefGoogle Scholar
  13. Gubsch M, Roscher C, Gleixner G, Habekost M, Lipowsky A, Schmid B, Schulze E-D, Steinbeiss S, Buchmann N (2011) Foliar and soil δ15N values reveal increased nitrogen partitioning among species in diverse grassland communities. Plant Cell Environ 34:895–908CrossRefPubMedGoogle Scholar
  14. Güsewell S (2004) N: P ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266CrossRefGoogle Scholar
  15. Harpole WS, Tilman D (2007) Grassland species loss resulting from reduced niche dimension. Nature 446:791–793CrossRefPubMedGoogle Scholar
  16. Hector A, Schmid B, Beierkuhnlein C, Caldeira MC, Diemer M, Dimitrakopoulos PG, Finn JA, Freitas H, Giller HS, Good J, Harris R, Högberg P, Huss-Danell K, Joshi J, Jumpponen A, Körner C, Leadley PW, Loreau M, Minns A, Mulder CPH, O’Donovan G, Otway SJ, Pereira JS, Prinz A, Read DJ, Scherer-Lorenzen M, Schulze ED, Siamantziouras ASD, Spehn EM, Terry AC, Troumbis AY, Woodward FI, Yachi S, Lawton JH (1999) Plant diversity and productivity experiments in European grasslands. Science 286:1123–1127CrossRefPubMedGoogle Scholar
  17. Hector A, Bazeley-White E, Loreau M, Otway S, Schmid B (2002) Overyielding in grassland communities: testing the sampling effect hypothesis with replicated biodiversity experiments. Ecol Lett 5:502–511CrossRefGoogle Scholar
  18. Hedley MJ, Stewart JWB (1982) Method to measure microbial phosphate in soils. Soil Biol Biochem 14:377–385CrossRefGoogle Scholar
  19. Hejcman M, Szaková J, Schellberg J, Tlustoš P (2010) The Rengen grassland experiment: relationship between soil and biomass chemical properties, amount of elements applied, and their uptake. Plant Soil 333:163–179CrossRefGoogle Scholar
  20. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363CrossRefPubMedGoogle Scholar
  21. Kahmen A, Renker C, Unsicker SB, Buchmann N (2006) Niche complementarity for nitrogen: an explanation for the biodiversity and ecosystem functioning relationship? Ecology 87:1244–1255CrossRefPubMedGoogle Scholar
  22. Klaus VH, Kleinebecker T, Hölzel N, Boch S, Müller J, Socher S, Prati D, Fischer M (2011) Nutrient concentrations and fibre contents of plant community biomass reflect diversity patterns in a broad range of agricultural grasslands. Perspect Plant Ecol 13:287–295CrossRefGoogle Scholar
  23. Klaus VH, Hölzel N, Boch S, Müller J, Socher SA, Prati D, Fischer M, Kleinebecker T (2013) Direct and indirect associations between plant species richness and productivity in grasslands: regional differences preclude simple generalization of productivity-biodiversity relationships. Preslia 85:97–112Google Scholar
  24. Kleinebecker T, Weber H, Hölzel N (2011a) Effects of soil conditions, seasonality and grazing on aboveground biomass quality in calcareous grasslands. Plant Ecol 212:1563–1576CrossRefGoogle Scholar
  25. Kleinebecker T, Klaus VH, Hölzel N (2011b) Reducing sample quantity and maintaining high prediction accuracy of quality parameters in grassland biomass with near-infrared reflectance spectroscopy (NIRS). J Near Infrared Spectrosc 19:495–505CrossRefGoogle Scholar
  26. Kleinebecker T, Hölzel N, Prati D, Schmitt B, Fischer M, Klaus VH (2014) Evidence from the real world: 15N natural abundances reveal enhanced nitrogen use at high plant diversity in Central European grasslands. J Ecol 102:456–465CrossRefGoogle Scholar
  27. Koerselman W, Meuleman AFM (1996) The vegetation N: P ratio: a new tool to detect the nature of nutrient limitation. J Appl Ecol 33:1441–1450CrossRefGoogle Scholar
  28. Koorem K, Gazol A, Öpik M, Moora M, Saks Ü, Uibopuu A, Sõber V, Zobel M (2014) Soil nutrient content influences the abundance of soil microbes but not plant biomass at the small-scale. PLoS One 9(3):e91998CrossRefPubMedPubMedCentralGoogle Scholar
  29. Kuo S (1996) Phosphorus. In: Sparks DL, Page AL, Helmke PA, Loeppert R, Soltanpour PN, Tabatabai MA, Johnston AE, Sumner ME (eds) Methods of soil analysis Part 3—chemical methods. Soil Science Society of America, Madison, pp 869–919Google Scholar
  30. Lemaire G, Hodgson J, Chabbi A (eds) (2011) Grassland productivity and ecosystem services. CABI, WallingfordGoogle Scholar
  31. Maestre FT, Cortina J (2002) Spatial patterns of surface soil properties and vegetation in a Mediterranean semi-arid steppe. Plant Soil 241:279–291CrossRefGoogle Scholar
  32. Maestre FT, Escudero A, Martinez I, Guerrero C, Rubio A (2005) Does spatial patterning matter to ecosystem functioning? Insights from biological soil crusts. Func Ecol 19:566–573CrossRefGoogle Scholar
  33. Marschner P (2011) Marschner’s mineral nutrition of higher plants. Academic Press, AmsterdamGoogle Scholar
  34. McCune B, Grace JB (2002) Analysis of Ecological Communities. MjM Software Design, Gleneden BeachGoogle Scholar
  35. Mullen RB, Schmidt SK (1993) Mycorrhizal infection, phosphorus uptake, and phenology in Ranunculus adoneus: implications for the functioning of mycorrhizae in alpine systems. Oecologia 94:229–234CrossRefGoogle Scholar
  36. Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36CrossRefGoogle Scholar
  37. Oelmann Y, Temperton VM, Buchmann N, Roscher C, Schumacher J, Schulze E-D, Weisser WW, Wilcke W (2007) Soil and plant nitrogen pools as related to plant diversity in an experimental grassland. Soil Sci Soc Am J 71:720–729CrossRefGoogle Scholar
  38. Olde Venterink H, van der Vliet RE, Wassen MJ (2001) Nutrient limitation along a productivity gradient in wet meadows. Plant Soil 234:171–179CrossRefGoogle Scholar
  39. Olde Venterink H, Wassen MJ, Verkroost AWM, de Ruiter PC (2003) Diversity–productivity patterns differ between NP-, and K-limited wetlands. Ecology 84:2191–2199CrossRefGoogle Scholar
  40. Osem Y, Perevolotsky A, Kigel J (2002) Grazing effect on diversity of annual plant communities in a semi-arid rangeland: interactions with small-scale spatial and temporal variation in primary productivity. J Ecol 90:936–946CrossRefGoogle Scholar
  41. Parker SS, Seabloom EW, Schimel JP (2012) Grassland community composition drives small-scale spatial patterns in soil properties and processes. Geoderma 170:269–279CrossRefGoogle Scholar
  42. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2015) nlme: Linear and nonlinear mixed effects models. R package version 31–118. http://www.CRANR-projectorg/package=nlme
  43. R Development Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  44. Regan K, Nunan N, Boeddinghaus R, Baumgartner V, Berner D, Boch S, Oelmann Y, Overmann J, Prati D, Schloter M, Schmitt B, Sorkau E, Steffens M, Kandeler E, Marhan S (2014) Seasonal controls on grassland microbial biogeography: Are they governed by plants, abiotic properties or both? Soil Biol Biochem 71:21–30CrossRefGoogle Scholar
  45. Reynolds HL, Mittelbach GG, Darcy-Hall TL, Houseman GR, Gross KL (2007) No effect of varying soil resource heterogeneity on plant species richness in a low fertility grassland. J Ecol 95:723–733CrossRefGoogle Scholar
  46. Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423CrossRefGoogle Scholar
  47. Socher S, Prati D, Müller J, Klaus V, Hölzel N, Fischer M (2012) Direct and productivity-mediated indirect effects of fertilization, mowing and grazing intensities on grassland plant species richness. J Ecol 100:1391–1399CrossRefGoogle Scholar
  48. Vitousek PM, Howarth RW (1991) Nitrogen limitation on land and in the sea: how can it occur? Biogeochemistry 13:87–115CrossRefGoogle Scholar
  49. Wassen MJ, OldeVenterink H, Lapshina ED, Tanneberger F (2005) Endangered plants persist under phosphorus limitation. Nature 437:547–550CrossRefPubMedGoogle Scholar
  50. Whitford WG (2002) Ecology of desert systems. Academic Press, LondonGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Valentin H. Klaus
    • 1
    Email author
  • Steffen Boch
    • 2
    • 3
  • Runa S. Boeddinghaus
    • 4
  • Norbert Hölzel
    • 1
  • Ellen Kandeler
    • 4
  • Sven Marhan
    • 4
  • Yvonne Oelmann
    • 5
  • Daniel Prati
    • 2
  • Kathleen M. Regan
    • 4
  • Barbara Schmitt
    • 2
  • Elisabeth Sorkau
    • 5
  • Till Kleinebecker
    • 1
  1. 1.Institute of Landscape EcologyUniversität MünsterMünsterGermany
  2. 2.Institute of Plant SciencesUniversität BernBernSwitzerland
  3. 3.Botanical GardenUniversität BernBernSwitzerland
  4. 4.Institute of Soil Science and Land EvaluationUniversität HohenheimStuttgartGermany
  5. 5.Universität Tübingen, GeoecologyTübingenGermany

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