, Volume 177, Issue 1, pp 39–51 | Cite as

Spatial gradient in nitrogen deposition affects plant species frequency in acidic grasslands

  • A. PannekEmail author
  • C. Duprè
  • D. J. G. Gowing
  • C. J. Stevens
  • M. Diekmann
Special Topic: Nitrogen Deposition Reassessed


Anthropogenic eutrophication impacts ecosystems worldwide. Here, we use a vegetation dataset from semi-natural grasslands on acidic soils sampled along a gradient in north-western Europe to examine the response of species frequency to nitrogen (N) deposition, controlling for the effects of other environmental variables. A second dataset of acidic grasslands from Germany and the Netherlands containing plots from different time periods was analysed to examine whether the results of the spatial gradient approach coincided with temporal changes in the abundance of species. Out of 44 studied species, 16 were affected by N deposition, 12 of them negatively. Soil pH and phosphorus (P) influenced 24 and 14 species, respectively, predominantly positively. Fewer species were related to the soil contents of NO3 or NH4 +, with no significant differences between the number of positive and negative effects. Whereas the temporal change of species was unrelated to their responses to pH, species responding negatively to N deposition, soil P and NO3 showed a significant decline over time in both countries. Species that were negatively affected by high N deposition and/or high soil P also showed a negative temporal trend and could be characterised by short stature and slow growth. The results confirm the negative role of N deposition for many plant species in semi-natural acidic grasslands. The negative temporal trends of species sensitive to high N deposition and soil P values clearly show a need for maintaining low soil nutrient status and for restoring the formerly infertile conditions in nutrient-enriched grasslands.


Eutrophication Life-history traits Nitrate Semi-natural grasslands Soil pH 



We would like to thank all people who were involved in collecting the original data and making it available to us. Comments of two anonymous referees and the editors improved earlier versions of the manuscript.

Supplementary material

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Supplementary material 1 (PDF 15 kb)
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Supplementary material 2 (PDF 13 kb)
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Supplementary material 4 (PDF 12 kb)


  1. Ashton IW, Miller AE, Bowman WD, Suding KN (2010) Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91:3252–3260. doi: 10.1890/09-1849.1 PubMedCrossRefGoogle Scholar
  2. Bates D, Maechler M, Bolker B (2011) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-42Google Scholar
  3. Bennett EM, Carpenter SR, Caraco NF (2001) Human impact on erodable phosphorus and eutrophication: a global perspective. Bioscience 51:227–234. doi: 10.1641/0006-3568(2001)051 CrossRefGoogle Scholar
  4. Bennie J, Hill MO, Baxter R, Huntley B (2006) Influence of slope and aspect on long-term vegetation change in British chalk grasslands. J Ecol 94:355–368. doi: 10.1111/j.1365-2745.2006.01104.x CrossRefGoogle Scholar
  5. Berge E, Bartnicki J, Olendrzynski K, Tsyro SG (1999) Long-term trends in emissions and transboundary transport of acidifying air pollution in Europe. J Environ Manag 57:31–50. doi: 10.1006/jema.1999.0275 CrossRefGoogle Scholar
  6. Blake L, Goulding KWT, Mott CJB, Johnston AE (1999) Changes in soil chemistry accompanying acidification over more than 100 years under woodland and grass at Rothamsted Experimental Station, UK. Eur J Sol Sci 50:401–412. doi: 10.1046/j.1365-2389.1999.00253.x CrossRefGoogle Scholar
  7. Bobbink R, Hornung M, Roelofs JGM (1998) The effects of air-borne nitrogen pollutants on species diversity in natural and semi-natural European vegetation. J Ecol 86:717–738. doi: 10.1046/j.1365-2745.1998.8650717.x CrossRefGoogle Scholar
  8. Bobbink R, Ashmore M, Braun S, Fluckiger W, van den Wyngaert IJJ (2003) Empirical nitrogen critical loads for natural and semi-natural ecosystems: 2002 update. Swiss Agency for Environment, Forest and Landscape, BernGoogle Scholar
  9. Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman JW, Fenn M, Gilliam F, Nordin A, Pardo L, De Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59PubMedCrossRefGoogle Scholar
  10. Ceulemans T, Merckx R, Hens M, Honnay O (2011) A trait-based analysis of the role of phosphorus vs. nitrogen enrichment in plant species loss across North-west European grasslands. J Appl Ecol 48:1155–1163. doi: 10.1111/j.1365-2664.2011.02023.x CrossRefGoogle Scholar
  11. Ceulemans T, Merckx R, Hens M, Honnay O (2013) Plant species loss from European semi-natural grasslands following nutrient enrichment–is it nitrogen or is it phosphorus? Glob Ecol Biogeogr 22:73–82. doi: 10.1111/j.1466-8238.2012.00771.x CrossRefGoogle Scholar
  12. Ceulemans T, Stevens CJ, Duchateau L, Jacquemyn H, Gowing DJG, Merckx R, Wallace H, van Rooijen N, Goethem T, Bobbink R, Dorland E, Gaudnik C, Alard D, Corcket E, Muller S, Dise NB, Dupré C, Diekmann M, Honnay O (2014) Soil phosphorus constrains biodiversity across European grasslands. Glob Change Biol:n/a-n/a. doi: 10.1111/gcb.12650 Google Scholar
  13. Developmental Core Team R (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  14. Diekmann M, Jandt U, Alard D, Bleeker A, Corcket E, Gowing DJG, Stevens CJ, Duprè C (2014) Long-term changes in calcareous grassland vegetation in North-western Germany–no decline in species richness, but a shift in species composition. Biol Conserv 172:170–179. doi: 10.1016/j.biocon.2014.02.038 CrossRefGoogle Scholar
  15. Dupré C, Ehrlén J (2002) Habitat configuration, species traits and plant distributions. J Ecol 90:796–805. doi: 10.1046/j.1365-2745.2002.00717.x CrossRefGoogle Scholar
  16. Dupré C, Stevens CJ, Ranke T, Bleeker A, Peppler-Lisbach C, Gowing DJG, Dise NB, Dorland EDU, Bobbink R, Diekmann M (2010) Changes in species richness and composition in European acidic grasslands over the past 70 years: the contribution of cumulative atmospheric nitrogen deposition. Glob Change Biol 16:344–357. doi: 10.1111/j.1365-2486.2009.01982.x CrossRefGoogle Scholar
  17. Ellenberg H (1952) Wiesen und Weiden und ihre standörtliche Bewertung. Ulmer, StuttgartGoogle Scholar
  18. Ellenberg H, Leuschner C (2010) Vegetation Mitteleuropas mit den Alpen. In Okologischer, Dynamischer und Historischer Sicht, 6. Ulmer Eugen, StuttgartGoogle Scholar
  19. Falkengren-Grerup U (1995) Long-term changes in flora and vegetation in deciduous forests of southern Sweden. Ecol Bull:215–226Google Scholar
  20. Falkengren-Grerup U, Lakkenborg-Kristensen H (1994) Importance of ammonium and nitrate to the performance of herb-layer species from deciduous forests in Southern Sweden. Environ Exp Bot 34:31–38. doi: 10.1016/0098-8472(94)90006-x CrossRefGoogle Scholar
  21. Falkowski P, Scholes RJ, Boyle E, Canadell J, Canfield D, Elser J, Gruber N, Hibbard K, Hogberg P, Linder S, Mackenzie FT, Moore B, Pedersen T, Rosenthal Y, Seitzinger S, Smetacek V, Steffen W (2000) The global carbon cycle: a test of our knowledge of earth as a system. Science 290:291–296. doi: 10.1126/science.290.5490.291 PubMedCrossRefGoogle Scholar
  22. Fangmeier A, Hadwiger-Fangmeier A, Van der Eerden L, Jager HJ (1994) Effects of atmospheric ammonia on vegetation- A review. Environ Pollut 86:43–82. doi: 10.1016/0269-7491(94)90008-6 PubMedCrossRefGoogle Scholar
  23. Fitter AH, Peat HJ (1994) The ecological flora database ( J Ecol 82:415. doi:  10.2307/2261309
  24. Galloway JN, Cowling EB (2002) Reactive nitrogen and the world: 200 years of change. Ambio 31:64–71. doi: 10.1579/0044-7447-31.2.64 PubMedGoogle Scholar
  25. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892. doi: 10.1126/science.1136674 PubMedCrossRefGoogle Scholar
  26. Gauger T, Anshelm F, Schuster H, Erisman JW, Vermeulen AT, Draaijers GPJ, Bleeker A, Nagel H-D (2002) Mapping of ecosystem specific long term trends in deposition loads and concentrations of air pollutants in Germany and their comparison with critical loads and critical levels. Umweltbundesamt, BerlinGoogle Scholar
  27. Gilliam FS (2006) Response of the herbaceous layer of forest ecosystems to excess nitrogen deposition. J Ecol 94:1176–1191. doi: 10.1111/j.1365-2745.2006.01155.x CrossRefGoogle Scholar
  28. Güsewell S (2004) N : p ratios in terrestrial plants: variation and functional significance. New Phytol 164:243–266. doi: 10.1111/j.1469-8137.2004.01192.x CrossRefGoogle Scholar
  29. Horswill P, O’Sullivan O, Phoenix GK, Lee JA, Leake JR (2008) Base cation depletion, eutrophication and acidification of species-rich grasslands in response to long-term simulated nitrogen deposition. Environ Pollut 155:336–349. doi: 10.1016/j.envpol.2007.11.006 PubMedCrossRefGoogle Scholar
  30. Janssens F, Peeters A, Tallowin JRB, Bakker JP, Bekker RM, Fillat F, Oomes MJM (1998) Relationship between soil chemical factors and grassland diversity. Plant Soil 202:69–78. doi: 10.1023/A:1004389614865 CrossRefGoogle Scholar
  31. Kleijn D, Bekker RM, Bobbink R, De Graaf MCC, Roelofs JGM (2008) In search for key biogeochemical factors affecting plant species persistence in heathland and acidic grasslands: a comparison of common and rare species. J Appl Ecol 45:680–687. doi: 10.1111/j.1365-2664.2007.01444.x CrossRefGoogle Scholar
  32. Kleyer M, Bekker RM, Knevel IC, Bakker JP, Thompson K, Sonnenschein M, Poschlod P, van Groenendael JM, Klimes L, Klimesova J, Klotz S, Rusch GM, Hermy M, Adriaens D, Boedeltje G, Bossuyt B, Dannemann A, Endels P, Gotzenberger L, Hodgson JG, Jackel AK, Kuhn I, Kunzmann D, Ozinga WA, Romermann C, Stadler M, Schlegelmilch J, Steendam HJ, Tackenberg O, Wilmann B, Cornelissen JHC, Eriksson O, Garnier E, Peco B (2008) The LEDA traitbase: a database of life-history traits of the Northwest European flora. J Ecol 96:1266–1274. doi: 10.1111/j.1365-2745.2008.01430.x CrossRefGoogle Scholar
  33. Lucassen ECHET, Bobbink R, Smolders AJP, van der Ven PJM, Lamers LPM, Roelofs JGM (2003) Interactive effects of low pH and high ammonium levels responsible for the decline of Cirsium dissectum (L.) Hill. Plant Ecol 165:45–52. doi: 10.1023/a:1021467320647 CrossRefGoogle Scholar
  34. Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704. doi: 10.1111/j.1469-8137.2011.03967.x PubMedCrossRefGoogle Scholar
  35. Ministry of Agriculture Fisheries and Food (1986) The analysis of agricultural materials. Her Majesty’s Stationery Office, LondonGoogle Scholar
  36. Monitoring Agricultural Resourses (MARS) (2009) European Commission Joint Research Centre.
  37. Morecroft MD, Sellers EK, Lee JA (1994) An experimental investigation into the effects of atmospheric nitrogen deposition on two semi-natural grasslands. J Ecol 82:475. doi: 10.2307/2261256 CrossRefGoogle Scholar
  38. NEGTAP (2001) Transboundary air pollution: Acidification, eutrophication and ground-level ozone in the UK. CEH, EdinburghGoogle Scholar
  39. Newman EI (1973) Competition and diversity in herbaceous vegetation. Nature 244:310. doi: 10.1038/244310a0 CrossRefGoogle Scholar
  40. Newman EI (1995) Phosphorus inputs to terrestrial ecosystems. J Ecol 83:713–726. doi: 10.2307/2261638 CrossRefGoogle Scholar
  41. Nordin A, Högberg P, Näsholm T (2001) Soil nitrogen form and plant nitrogen uptake along a boreal forest productivity gradient. Oecologia 129:125–132. doi: 10.1007/s004420100698 CrossRefGoogle Scholar
  42. Olde Venterink H, Wassen MJ, Verkroost AWM, De Ruiter PC (2003) Species richness-productivity patterns differ between N-, P-, and K-limited wetlands. Ecology 84:2191–2199. doi: 10.1890/01-0639 CrossRefGoogle Scholar
  43. Pennings SC, Clark CM, Cleland EE, Collins SL, Gough L, Gross KL, Milchunas DG, Suding KN (2005) Do individual plant species show predictable responses to nitrogen addition across multiple experiments? Oikos 110:547–555. doi: 10.1111/j.0030-1299.2005.13792.x CrossRefGoogle Scholar
  44. Peñuelas J, Sardans J, Rivas-ubach A, Janssens IA (2012) The human-induced imbalance between C, N and P in Earth’s life system. Glob Change Biol 18:3–6. doi: 10.1111/j.1365-2486.2011.02568.x CrossRefGoogle Scholar
  45. Phoenix GK, Emmett BA, Britton AJ, Caporn SJM, Dise NB, Helliwell R, Jones L, Leake JR, Leith ID, Sheppard LJ, Sowerby A, Pilkington MG, Rowe EC, Ashmorek MR, Power SA (2012) Impacts of atmospheric nitrogen deposition: responses of multiple plant and soil parameters across contrasting ecosystems in long-term field experiments. Glob Change Biol 18:1197–1215. doi: 10.1111/j.1365-2486.2011.02590.x CrossRefGoogle Scholar
  46. Pieterse G, Bleeker A, Vermeulen AT, Wu Y, Erisman JW (2007) High resolution modelling of atmosphere-canopy exchange of acidifying and eutrophying components and carbon dioxide for European forests. Tellus B 59:412–424. doi: 10.1111/j.1600-0889.2007.00266.x CrossRefGoogle Scholar
  47. Rich T, Redbane M, Fasham M, McMeechan F, Dobson D (2005) Ground and shrub vegetation. In: Hill D, Fasham M, Tucker G, Shewry M, Shaw P (eds) Handbook of biodiversity methods: survey, evaluation and monitoring. Cambridge University Press, Cambridge, pp 202–222Google Scholar
  48. Roelofs JGM, Bobbink R, Brouwer E, DeGraaf MCC (1996) Restoration ecology of aquatic and terrestrial vegetation on non-calcareous sandy soils in The Netherlands. Acta Bot Neerl 45:517–541CrossRefGoogle Scholar
  49. Roem WJ, Berendse F (2000) Soil acidity and nutrient supply ratio as possible factors determining changes in plant species diversity in grassland and heathland communities. Biol Conserv 92:151–161. doi: 10.1016/S0006-3207(99)00049-X CrossRefGoogle Scholar
  50. Sala OE, Chapin FS 3rd, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774. doi: 10.1126/science.287.5459.1770 PubMedCrossRefGoogle Scholar
  51. Schuster B, Diekmann M (2003) Changes in species density along the soil pH gradient-evidence from German plant communities. Folia Geobot 38:367–379. doi: 10.1007/bf02803245 CrossRefGoogle Scholar
  52. Skogen KA, Holsinger KE, Cardon ZG (2011) Nitrogen deposition, competition and the decline of a regionally threatened legume, Desmodium cuspidatum. Oecologia 165:261–269. doi: 10.1007/s00442-010-1818-7 PubMedCrossRefGoogle Scholar
  53. Smith RI, Fowler D, Sutton MA, Flechard C, Coyle M (2000) Regional estimation of pollutant gas dry deposition in the UK: model description, sensitivity analyses and outputs. Atmos Environ 34:3757–3777. doi: 10.1016/S1352-2310(99)00517-8 CrossRefGoogle Scholar
  54. Stevens CJ, Dise NB, Gowing DJ (2009) Regional trends in soil acidification and exchangeable metal concentrations in relation to acid deposition rates. Environ Pollut 157:313–319. doi: 10.1016/j.envpol.2008.06.033 PubMedCrossRefGoogle Scholar
  55. Stevens CJ, Dupré C, Dorland E, Gaudnik C, Gowing DJ, Bleeker A, Diekmann M, Alard D, Bobbink R, Fowler D, Corcket E, Mountford JO, Vandvik V, Aarrestad PA, Muller S, Dise NB (2010a) Nitrogen deposition threatens species richness of grasslands across Europe. Environ Pollut 158:2940–2945. doi: 10.1016/j.envpol.2010.06.006 PubMedCrossRefGoogle Scholar
  56. Stevens CJ, Thompson K, Grime JP, Long CJ, Gowing DJG (2010b) Contribution of acidification and eutrophication to declines in species richness of calcifuge grasslands along a gradient of atmospheric nitrogen deposition. Funct Ecol 24:478–484. doi: 10.1111/j.1365-2435.2009.01663.x CrossRefGoogle Scholar
  57. Stevens C, Dupré C, Gaudnik C, Dorland E, Dise N, Gowing D, Bleeker A, Alard D, Bobbink R, Fowler D, Vandvik V, Corcket E, Mountford JO, Aarrestad PA, Muller S, Diekmann M (2011a) Changes in species composition of European acid grasslands observed along a gradient of nitrogen deposition. J Veg Sci 22:207–215. doi: 10.1111/j.1654-1103.2010.01254.x CrossRefGoogle Scholar
  58. Stevens CJ, Dupré C, Dorland E, Gaudnik C, Gowing DJ, Bleeker A, Diekmann M, Alard D, Bobbink R, Fowler D, Corcket E, Mountford JO, Vandvik V, Aarrestad PA, Muller S, Dise NB (2011b) The impact of nitrogen deposition on acid grasslands in the Atlantic region of Europe. Environ Pollut 159:2243–2250. doi: 10.1016/j.envpol.2010.11.026 PubMedCrossRefGoogle Scholar
  59. Stevens CJ, Dupré C, Dorland E, Gaudnik C, Gowing DJG, Diekmann M, Alard D, Bobbink R, Corcket E, Mountford JO, Vandvik V, Aarrestad PA, Muller S, Dise NB (2011c) Grassland species composition and biogeochemistry in 153 sites along environmental gradients in Europe. Ecology 92:1544. doi: 10.1890/11-0115.1 CrossRefGoogle Scholar
  60. Suding KN, Collins SL, Gough L, Clark C, Cleland EE, Gross KL, Milchunas DG, Pennings S (2005) Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proc Natl Acad Sci USA 102:4387–4392. doi: 10.1073/pnas.0408648102 PubMedCentralPubMedCrossRefGoogle Scholar
  61. Tamm CO (1991) Nitrogen in terrestrial ecosystems: questions of productivity, vegetational changes, and ecosystem stability. Springer, BerlinCrossRefGoogle Scholar
  62. Tilman D, Fargione J, Wolff B, D’Antonio C, Dobson A, Howarth R, Schindler D, Schlesinger WH, Simberloff D, Swackhamer D (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284. doi: 10.1126/science.1057544 PubMedCrossRefGoogle Scholar
  63. Treseder KK (2004) A meta-analysis of mycorrhizal responses to nitrogen, phosphorus, and atmospheric CO2 in field studies. New Phytol 164:347–355. doi: 10.1111/j.1469-8137.2004.01159.x CrossRefGoogle Scholar
  64. Vallano DM, Sparks JP (2013) Foliar δ15 N is affected by foliar nitrogen uptake, soil nitrogen, and mycorrhizae along a nitrogen deposition gradient. Oecologia 172:47–58. doi: 10.1007/s00442-012-2489-3 PubMedCrossRefGoogle Scholar
  65. van den Berg LJ, Dorland E, Vergeer P, Hart MA, Bobbink R, Roelofs JG (2005) Decline of acid-sensitive plant species in heathland can be attributed to ammonium toxicity in combination with low pH. New Phytol 166:551–564. doi: 10.1111/j.1469-8137.2005.01338.x PubMedCrossRefGoogle Scholar
  66. van Jaarsveld JA (2004) The operational priority substances model. Report No. 500045001/2004, National Institute for Public Health and the Environment, Bilthoven, The NetherlandsGoogle Scholar
  67. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750. doi: 10.1890/1051-0761(1997)007 Google Scholar
  68. Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15. doi: 10.1890/08-0127.1 PubMedCrossRefGoogle Scholar
  69. Wassen MJ, Venterink HO, Lapshina ED, Tanneberger F (2005) Endangered plants persist under phosphorus limitation. Nature 437:547–550. doi: 10.1038/nature03950 PubMedCrossRefGoogle Scholar
  70. Weigelt A, Bol R, Bardgett RD (2005) Preferential uptake of soil nitrogen forms by grassland plant species. Oecologia 142:627–635. doi: 10.1007/s00442-004-1765-2 PubMedCrossRefGoogle Scholar
  71. Wisskirchen R, Haeupler H (1998) Standardliste der Farn- und Blütenpflanzen Deutschlands. Eugen Ulmer, StuttgartGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • A. Pannek
    • 1
    Email author
  • C. Duprè
    • 1
  • D. J. G. Gowing
    • 2
  • C. J. Stevens
    • 3
  • M. Diekmann
    • 1
  1. 1.Department of Ecology, FB 2, Vegetation Ecology and Conservation BiologyUniversity of BremenBremenGermany
  2. 2.Department of Environment, Earth and EcosystemsOpen UniversityMilton KeynesUK
  3. 3.Lancaster Environment CentreLancaster UniversityLancasterUK

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