Plant and Soil

, Volume 424, Issue 1–2, pp 491–501 | Cite as

Assessing soil ecosystem processes – biodiversity relationships in a nature reserve in Central Europe

  • Tancredi Caruso
  • Edith C. Hammer
  • Stefan Hempel
  • Josef Kohler
  • E. Kathryn Morris
  • Stavros D. Veresoglou
  • Nora Opitz
  • Jeannine Wehner
  • Matthias C. Rillig
Regular Article


Background and aims

Plant diversity – ecosystem processes relationships are essential to our understanding of ecosystem functioning. We aimed at disentangling the nature of such relationships in a mesotrophic grassland that was highly heterogeneous with regards to nutrient availability.


Rather than targeting primary productivity, like most existing reports do, we focused our study on belowground ecosystem processes. We tested three, largely mutually exclusive, hypotheses of ecosystem processes relationships: the redundancy hypothesis, the insurance hypothesis and the centrifugal model hypothesis. We sampled the grassland twice within a single plant growing season in a spatially explicit way and assayed the soil for nitrification, urease activity, relative bacterial activity and a microbial community profile based on respiration while we simultaneously assessed plant diversity.


Results supported the centrifugal model. We justify the lack of support for the other two hypotheses on the basis of having conducted an observational study in an environmentally heterogeneous site.


The centrifugal model hypothesis appears to be a very good predictive model for explaining diversity in observational, heterogeneous studies. The specific study represents one of the few observational studies that consider measures of ecosystem functioning other than primary productivity.


The centrifugal model hypothesis Diversity-productivity relationships Ecosystem functioning The insurance hypothesis The redundancy hypothesis 



The project was funded by the Dahlem Center of Plant Sciences. We would like to thank Erik Verbruggen, Stefanie Maaß and Daniel Daphi for technical assistance.

Author contributions

Coordinated the project: SH; Acquired funding for the project: TC, ECH, SH, JK, EKM, SDV; conducted the harvests: TC, ECH, SH, JK, EKM, SDV, NO, JW; conceived the analysis, analyzed the data and wrote the paper: SDV; everybody contributed comments to the manuscript; ECH assayed relative bacterial to fungal activity, JK measured community-level physiological profiles and SDV analyzed urease activity and nitrification rates.

Supplementary material

11104_2017_3557_MOESM1_ESM.doc (69 kb)
ESM 1 (DOC 69 kb)
11104_2017_3557_MOESM2_ESM.xls (133 kb)
ESM 2 (XLS 133 kb)


  1. Adler PB, Seabloom EW, Borer ET, Hillebrand H, Hautier Y, Hector A, Harpole WS, O’Halloran LR, Grace JB, Anderson TM, Bakker JD, Biederman LA, Brown CS, Buckley YM, Calabrese LB, Chu CJ, Cleland EE, Collins SL, Cottingham KL, Crawley MJ, Damschen EI, Davies KF, DeCrappeo NM, Fay PA, Firn J, Frater P, Gasarch EI, Gruner DS, Hagenah N, Lambers JHR, Humphries H, Jin VL, Kay AD, Kirkman KP, Klein JA, Knops JMH, La Pierre KJ, Lambrinos JG, Li W, MacDougall AS, McCulley RL, Melbourne BA, Mitchell CE, Moore JL, Morgan JW, Mortensen B, Orrock JL, Prober SM, Pyke DA, Risch AC, Schuetz M, Smith MD, Stevens CJ, Sullivan LL, Wang G, Wragg PD, Wright JP, Yang LH (2011) Productivity is a poor predictor of plant species richness. Science 333:1750–1753CrossRefPubMedGoogle Scholar
  2. Beck TH (1979) Die Nitrifikation in Böden (Sammelreferat). J Plant Nutr Soil Sci 142:299–309Google Scholar
  3. Byrnes JEK, Gampfeldt L, Isbell F, Lefcheck JS, Griffin JN, Hector A, Cardinale BJ, Hooper DU, Dee LE, Duffy JE (2014) Investigating the relationship between biodiversity and ecosystem multifunctionality: challenges and solutions. Methods Ecol Evol 5:111–124CrossRefGoogle Scholar
  4. Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM (2003) A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microbiol 69:3593–3599CrossRefPubMedPubMedCentralGoogle Scholar
  5. Chapin FS III, Walker BH, Hobbs RJ, Hooper DU, Lawton JH, Sala OE, Tilman D (1997) Biotic control over the functioning of ecosystems. Science 277:500–504CrossRefGoogle Scholar
  6. de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795e811CrossRefGoogle Scholar
  7. Doak DF, Bigger D, Harding EK, Marvier MA, O'Malley RE, Thomson D (1998) The statistical inevitability of stability-diversity relationships in community ecology. Am Nat 151:264–276PubMedGoogle Scholar
  8. Fagotti DSL, Miyauchi MYH, Oliveira AG, Santinoni IA, Eberhardt DN, Nimtz A, Ribeiro RA, Paula AM, Queiroz CAS, Andrade G, Zangaro W, Nogueira MA (2012) Gradients in N-cycling attributes along forestry and agricultural land-use systems are indicative of soil capacity for N supply. Soil Use Manag 28:292–298CrossRefGoogle Scholar
  9. Fornara DA, Tilman D (2009) Ecological mechanisms associated with the positive diversity–productivity relationship in an N-limited grassland. Ecology 90:408–418CrossRefPubMedGoogle Scholar
  10. Fridley JD (2001) The influence of species diversity on ecosystem productivity: how, where and why? Oikos 93:514–526CrossRefGoogle Scholar
  11. Hector A, Schmid B, Beierkuhnlein C, Caldeira MC, Diemer M, Dimitrakopoulos PG, Finn JA, Freitas H, Giller PS, Good J, Harris R, Hogberg P, Huss-Danell K, Joshi J, Jumpponen A, Korner 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
  12. Hector A, Joshi J, Scherer-Lorenzen M, Schmid B, Spehn EM, Wacker L, Weilenmann M, Bazeley-White E, Beierkuhnlein C, Caldeira MC, Dimitrakopoulos PG, Finn JA, Huss-Danell K, Jumpponen A, Leadley PW, Loreau M, Mulder CPH, Neßhöver C, Palmborg C, Read DJ, Siamantziouras SD, Terry AC, Troumbis AY (2007) Biodiversity and ecosystem functioning: reconciling the results of experimental and observational studies. Funct Ecol 21:998–1002CrossRefGoogle Scholar
  13. Hooper DU, Chapin FS III, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vendermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35CrossRefGoogle Scholar
  14. Horn S, Hempel S, Ristow M, Rillig MC, Kowarik I, Caruso T (2015) Plant community assembly at small scales: spatial versus environmental factors in a central European grassland. Acta Oecol 63:56–62CrossRefGoogle Scholar
  15. Isbell F, Calcagno V, Hector A, Connolly J, Stanley Harpole W, Reich PB, Scherer-Lorenzen M, Schmid B, Tilman D, van Ruijven J, Weigelt A, Wilsey BJ, Zavaleta ES, Loreau M (2011) High plant diversity is needed to maintain ecosystem services. Nature 477:199–196CrossRefPubMedGoogle Scholar
  16. Ives AR, Hughes JB (2002) General relationships between species diversity and stability in competitive systems. Am Nat 159:388–395CrossRefPubMedGoogle Scholar
  17. Jiang L, Wan SQ, Li LH (2009) Species diversity and productivity: why do results of diversity-manipulation experiments differ from natural patterns? J Ecol 97:603–608CrossRefGoogle Scholar
  18. Kahmen A, Perner J, Andorff V, Weisser W, Buchmann N (2005) Effects of plant diversity, community composition and environmental parameters in montane European grasslands. Oecologia 142:605–615CrossRefGoogle Scholar
  19. Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68–72CrossRefGoogle Scholar
  20. Kang SH, Mills AL (2004) Soil bacterial community structure changes following disturbance of the overlying plant community. Soil Sci 169:55–65CrossRefGoogle Scholar
  21. Keddy PA (1990) Competitive hierarchies and centrifugal organization in plant communities. In: Grace J, Tilman D (eds) Perspectives on plant competition. Academic Press, San Diego, pp 266–290Google Scholar
  22. Keddy PA, MacLellan P (1990) Centrifugal organization in forests. Oikos 59:75–84CrossRefGoogle Scholar
  23. Kreyling J, Beierkuhnlein C, Ellis L, Jentsch A (2008) Invasibility of grassland and heath communities exposed to extreme weather events - additive effects of diversity resistance and fluctuating physical environment. Oikos 117:1542–4554CrossRefGoogle Scholar
  24. Loreau M, de Mazancourt C (2013) Biodiversity and ecosystem stability: a synthesis of underlying mechanisms. Ecol Lett 16:106–115CrossRefPubMedGoogle Scholar
  25. Loreau M, Mouquet N (1999) Immigration and maintainance of local species diversity. Am Nat 154:427–440CrossRefPubMedGoogle Scholar
  26. MacArthur RH (1955) Fluctuations of animal populations and a measure of community stability. Ecology 36:533–535CrossRefGoogle Scholar
  27. Mace GM, Norris K, Fitter AH (2012) Biodiversity and ecosystem services: a multilayered relationship. Trends Ecol Evol 27:19–26CrossRefPubMedGoogle Scholar
  28. May RM (1972) Will a large complex system be stable? Nature 238:413–414CrossRefPubMedGoogle Scholar
  29. McNaughton SJ (1977) Diversity and stability of ecological communities - comment on role of empirism in ecology. Am Nat 111:515–525CrossRefGoogle Scholar
  30. Mokany K, Asj J, Roxburgh S (2008) Functional identity is more important than diversity in influencing ecosystem processes in a temperate native grassland. J Ecol 96:884–893CrossRefGoogle Scholar
  31. Oberdorfer EP (2001) Pflanzensoziologische Exkursionsflora für Deutschland und angrenzende Gebiete, 8th edn. Ulmer, StuttgartGoogle Scholar
  32. Odum EP (1953) Fundamentals of ecology. W. B. Saunders, PhiladelphiaGoogle Scholar
  33. Penny KI (1996) Appropriate critical values when testing for a single multivariate outlier by using the Mahalanobis distance. Appl Stat 45:73–81CrossRefGoogle Scholar
  34. Pimm SL (1982) Food webs. Chapman & Hall, LondonCrossRefGoogle Scholar
  35. Pinheiro J, Bates D, DebRoy S, Sarkar D, R Development Core Team (2013) nlme: linear and nonlinear mixed effects models. R package version 3.1-108Google Scholar
  36. R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  37. Reiss J, Bridle JR, Montoya JM, Woodward G (2009) Emerging horizons in biodiversity and ecosystem functioning research. Trends Ecol Evol 24:505–514CrossRefPubMedGoogle Scholar
  38. Romanuk TN, Kolasa J (2002) Environmental variability alters the relationship between richness and variability of community abundances in aquatic rock pool microcosms. Ecoscience 9:55–62CrossRefGoogle Scholar
  39. Rosenzweig ML, Abramsky Z (1986) Centrifugal community organization. Oikos 46:339–348CrossRefGoogle Scholar
  40. Rousk J, Brookes PC, Baath E (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol 75:1589–1596CrossRefPubMedPubMedCentralGoogle Scholar
  41. Schulze ED, Mooney HA (1993) Biodiversity and ecosystem function. Springer-Verlag, BerlinCrossRefGoogle Scholar
  42. Tetard-Jones C, Kertesz MA, Gallois P, Preziosi RF (2007) Genotype-by-genotype interactions modified by a third species in a plant-insect system. Am Nat 170:492–499CrossRefPubMedGoogle Scholar
  43. Thompson K, Askew AP, Grime JP, Dunnett NP, Willis AJ (2005) Biodiversity, ecosystem function and plant traits in mature and immature plant communities. Funct Ecol 19:355–358CrossRefGoogle Scholar
  44. Tilman D, Downing JA (1994) Biodiversity and stability in grasslands. Nature 367:363–365.Google Scholar
  45. Tilman D, Lehman CL, Bristow CE (1998) Diversity-stability relationships: statistical inevitability or ecological consequence? Am Nat 151:277–282PubMedGoogle Scholar
  46. Tilman D, Reich PB, Knops JMH (2006) Biodiversity and ecosystem stability in a decade-long grassland experiment. Nature 441:629–632CrossRefPubMedGoogle Scholar
  47. Tilman D, van Ruijven J, Weigelt A, Wilsey BJ, Zavaleta ES, Loreau M (2011) High plant diversity is needed to maintain ecosystem services. Nature 477:199–202CrossRefPubMedGoogle Scholar
  48. Valone TJ, Hoffman CD (2003) Population stability is higher in more diverse annual plant communities. Ecol Lett 6:90–95CrossRefGoogle Scholar
  49. Vogel A, Eisenhauer N, Weigelt A, Scherer-Lorenzen M (2013) Plant diversity does not buffer drought effects on early-stage litter mass loss rates and microbial properties. Glob Chang Biol 19:2795–2803CrossRefPubMedGoogle Scholar
  50. Yachi S, Loreau M (1999) Biodiversity and ecosystem productivity in a fluctuating environment: the insurance hypothesis. Proc Natl Acad Sci U S A 96:1463–1468CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Tancredi Caruso
    • 1
    • 2
    • 3
  • Edith C. Hammer
    • 1
    • 2
    • 4
  • Stefan Hempel
    • 1
    • 2
  • Josef Kohler
    • 1
    • 2
  • E. Kathryn Morris
    • 1
    • 5
  • Stavros D. Veresoglou
    • 1
    • 2
  • Nora Opitz
    • 1
    • 2
  • Jeannine Wehner
    • 1
    • 2
  • Matthias C. Rillig
    • 1
    • 2
  1. 1.Institut für Biologie, Plant EcologyFreie Universität BerlinBerlinGermany
  2. 2.Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB)BerlinGermany
  3. 3.School of Biological SciencesQueen’s University BelfastBelfastUK
  4. 4.Department of Biology, Microbial Ecology/BiodiversityLund UniversityLundSweden
  5. 5.Department of BiologyXavier UniversityCincinnatiUSA

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