Plant and Soil

, Volume 373, Issue 1–2, pp 183–199 | Cite as

Can soil acidity and light help to explain tree species effects on forest herb layer performance in post-agricultural forests?

  • Arno Thomaes
  • Luc De Keersmaeker
  • An De Schrijver
  • Lander Baeten
  • Kris Vandekerkhove
  • Gorik Verstraeten
  • Kris Verheyen
Regular Article



Tree species affect herb layer species through their effects on soil quality and light regime but their relative importance and interactions are insufficiently known.


Pot experiment with soil taken from stands planted with tree species with contrasting effects on soil acidification, two light regimes and six forest perennials.


The survival or growth of Mercurialis perennis, Lamium galeobdolon, Anemone nemorosa and Primula elatior was lower in the acid Alnus soils than in the less acid Fraxinus soils. By contrast, the acid tolerant Convallaria majalis and Dryopteris dilatata were barely affected by tree species. Light conditions had less impact than soil chemistry and did not compensate for unfavourable soil conditions. Ca and P concentrations increased in plants grown in Fraxinus soils. The Mg and Al shoot/root ratios of respectively one and two of the acid tolerant species was elevated in the most acid soil.


Tree species effects on forest perennials are mainly explained by increased Al concentrations under acidifying species. Changed plant concentrations and allocation are likely associated to Al antagonism. We found no light compensation for the soil effect on the studied species. However, light alters the plant nutrient concentrations and allocation which may suggest an indirect effect.


Overstory-understory interactions Plant nutrient concentrations Al toxicity Soil acidification Ecological compensation Post-agricultural forest 



Thanks to the Agency of Nature and Forests for the permission to collect the soil. Thanks to Stefaan Goessens, Marc Esprit, Stefaan Moreels and Kristine Vander Mijnsbrugge for the practical help with the experiment, Pieter Verschelde for evaluating the possibility of using path analyses. A.D.S. and L.B. were funded by the Research Foundation Flanders (FWO) and G.V. by the Institute for the Promotion of Innovation by Science and Technology in Flanders (IWT). We like to acknowledge Jan Plue and two reviewers for reviewing an earlier version of the ms.

Supplementary material


  1. Abedi M, Bartelheimer M, Poschlod P (2012) Aluminiumtoxic effects on seedling root survival affect plant composition along soil reaction gradients – a case study in dry sandy grasslands. J Veg Sci. doi: 10.1111/jvs.12016 Google Scholar
  2. Aerts R, Honnay O (2011) Forest restoration, biodiversity and ecosystem functioning. BMC Ecol 11:29PubMedCrossRefGoogle Scholar
  3. Aubert M, Bureau F, Alard D, Bardat J (2004) Effect of tree mixture on the humic epipedon and vegetation diversity in managed beech forests (Normandy, France). Can J Res 34(1):233–248CrossRefGoogle Scholar
  4. Baeten L, Bauwens B, De Schrijver A, De Keersmaeker L, Van Calster H, Vandekerkhove K, Roelandt B, Beeckman H, Verheyen K (2009a) Herb layer changes (1954–2000) related to the conversion of coppice-with-standards forest and soil acidification. Appl Veg Sci 12:187–197CrossRefGoogle Scholar
  5. Baeten L, Hermy M, Verheyen K (2009b) Environmental limitation contributes to the differential colonization capacity of two forest herbs. J Veg Sci 20(2):209–223CrossRefGoogle Scholar
  6. Baeten L, Vanhellemont M, De Frenne P, De Schrijver A, Hermy M, Verheyen K (2010) Plasticity in response to phosphorus and light availability in four forest herbs. Oecologia 163(4):1021–1032PubMedCrossRefGoogle Scholar
  7. Barbier S, Gosselin F, Balandier P (2008) Influence of tree species on understory vegetation diversity and mechanisms involved - a critical review for temperate and boreal forests. For Ecol Manag 254(1):1–15CrossRefGoogle Scholar
  8. Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using Eigen and S4. R package version 0.999902344-0.
  9. Bigelow SW, Canham CD (2002) Community organization of tree species along soil gradients in a north-eastern USA forest. J Ecol 90(1):188–200CrossRefGoogle Scholar
  10. Bolan NS (1991) A critical-review on the role of mycorrhizal fungi in the uptake of phosphorus by plants. Plant Soil 134(2):189–207CrossRefGoogle Scholar
  11. Bray R, Kurtz L (1945) Determination of total, organic, and available forms of phosphorus in soils. Soil Sci 59:39–45CrossRefGoogle Scholar
  12. Cornelis J, Hermy M, Roelandt B, De Keersmaeker L, Vandekerkhove K (2009) Bosplantengemeenschappen in Vlaanderen, een typologie van bossen gebaseerd op de kruidlaag. Agentschap voor Natuur en Bos & Instituut voor Natuur- en Bosonderzoek, BrusselGoogle Scholar
  13. Cote B, Fyles JW (1994) Leaf litter disappearance of hardwood species of southern Quebec: interaction between litter quality and stand type. Ecosci 1(4):322–328Google Scholar
  14. Cronan CS, Grigal DF (1995) Use of calcium aluminium ratios as indicators of stress in forest ecosystems. J Environ Qual 24(2):209–226CrossRefGoogle Scholar
  15. De Keersmaeker L, Martens L, Verheyen K, Hermy M, De Schrijver A, Lust N (2004) Impact of soil fertility and isolation on diversity of herbaceous woodland species colonizing afforestations in Muizen Forest, Belgium. For Ecol Manag 188:291–304CrossRefGoogle Scholar
  16. De Schrijver A, De Frenne P, Staelens J, Verstraeten G, Muys B, Vesterdal L, Wuyts K, Van Nevel L, Schelfhout S, De Neve S, Verheyen K (2012a) Tree species traits cause divergence in soil acidification during four decades of postagricultural forest development. Glob Chang Biol 18:1127–1140CrossRefGoogle Scholar
  17. De Schrijver A, Vesterdal L, Hansen K, De Frenne P, Augusto L, Achat DL, Staelens J, Baeten L, De Keersmaeker L, De Neve S, Verheyen K (2012b) Four decades of post-agricultural forest development have caused major redistributions of soil phosphorus fractions. Oecologia 169(1):221–234PubMedCrossRefGoogle Scholar
  18. Devries W, Breeuwsma A (1986) Relative importance of natural and anthropogenic proton sources in soil in the Netherlands. Water Air Soil Pollut 28(1–2):173–184Google Scholar
  19. Dzwonko Z, Loster S (1997) Effects of dominant trees and antropogenic disturbances on species richness and floristic composition of secondary communities in Southern Poland. J Appl Ecol 34:861–870CrossRefGoogle Scholar
  20. Edwards CA, Arancon NQ, Vasko-Bennett M, Little B, Askar A (2009) The relative toxicity of metaldehyde and iron phosphate-based molluscicides to earthworms. Crop Prot 28(4):289–294CrossRefGoogle Scholar
  21. Ellenberg H, Weber HE, Düll R, Wirth V, Werner W, Paulissen D (1992) Zeigerwerte von Pflanzen in Mitteleuropa. Scr Geobot 18:1–248Google Scholar
  22. Falkengren-Grerup U (1998) Nitrogen response of herbs and graminoids in experiments with simulated acid soil solution. Environ Pollut 102:93–99CrossRefGoogle Scholar
  23. Falkengren-Grerup U, Tyler G (1993) Experimental evidence for the relative sensitivity of deciduous forest plants to high soil acidity. For Ecol Manag 60(3):11–326Google Scholar
  24. Falkengren-Grerup U, Quist ME, Tyler G (1995) Relative importance of exchangeable and soil solution cation concentrations to the distribution of vascular plants. Environ Exp Bot 35(1):9–15CrossRefGoogle Scholar
  25. FAO (2012) State of the world’s forests: 2012. Food and Agriculture Organization of the United Nations, RomeGoogle Scholar
  26. Grubb PJ, Lee WG, Kollmann J, Wilson JB (1996) Interaction of irradiance and soil nutrient supply on growth of seedlings of ten European tall-shrub species and Fagus sylvatica. J Ecol 84(6):827–840CrossRefGoogle Scholar
  27. Gusewell S (2004) N : P ratios in terrestrial plants: variation and functional significance. New Phytol 164(2):243–266CrossRefGoogle Scholar
  28. Gyaneshwar P, Kumar GN, Parekh LJ, Poole PS (2002) Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245(1):83–93CrossRefGoogle Scholar
  29. Hermy M, Verheyen K (2007) Legacies of the past in the present-day forest biodiversity: a review of past land-use effects on forest plant species composition and diversity. Ecol Res 22(3):361–371CrossRefGoogle Scholar
  30. Hermy M, Honnay O, Firbank L, Grashof-Bokdam CJ, Lawesson JE (1999) An ecological comparison between ancient and other forest plant species of Europe, and the implications for forest conservation. Biol Conserv 91(1):9–22CrossRefGoogle Scholar
  31. Hill MO, Roy DB, Mountford JO, Bunce RGH (2000) Extending Ellenberg’s indicator values to a new area: an algorithmic approach. J Appl Ecol 37(1):3–15CrossRefGoogle Scholar
  32. Hipps NA, Davies MJ, Dodds P, Buckley GP (2005) The effects of phosphorus nutrition and soil pH on the growth of some ancient woodland indicator plants and their interaction with competitor species. Plant Soil 271(1–2):131–141CrossRefGoogle Scholar
  33. Huang JWW, Shaff JE, Grunes DL, Kochian LV (1992) Aluminum effects on calcium fluxes at the root apex of aluminum-tolerant and aluminum-sensitive wheat cultivars. Plant Physiol 98(1):230–237PubMedCrossRefGoogle Scholar
  34. Jarrell WM, Beverly RB (1981) The dilution effect in plant nutrition studies. In: Brady NC (ed) Advance in agronomy, vol 34. Academic, New York, pp 197–224Google Scholar
  35. Jones DL, Kochian LV (1995) Aluminum inhibition of the inositol 1,4,5-triphosphate signal-transduction pathway in wheat roots - a role in aluminum toxicity. Plant Cell 7(11):1913–1922PubMedGoogle Scholar
  36. Kooijman AM, Cammeraat E (2010) Biological control of beech and hornbeam affects species richness via changes in the organic layer, pH and soil moisture characteristics. Funct Ecol 24(2):469–477CrossRefGoogle Scholar
  37. Lindh B (2008) Flowering of understory herbs following thinning in the Western Cascades, Oregon. For Ecol Manag 256(5):929–936CrossRefGoogle Scholar
  38. Lucash MS, Yanai RD, Blum JD, Park BB (2012) Foliar nutrient concentrations related to soil sources across a range of sites in the Northeastern United States. Soil Sci Soc Am J 76(2):674–683CrossRefGoogle Scholar
  39. MacDonald GK, Bennett EM, Taranu ZE (2012) The influence of time, soil characteristics, and land-use history on soil phosphorus legacies: a global meta-analysis. Glob Chang Biol 18(6):1904–1917CrossRefGoogle Scholar
  40. Metali F, Salim K, Burslem D (2012) Evidence of foliar aluminium accumulation in local, regional and global datasets of wild plant. New Phytol 193(3):637–649PubMedCrossRefGoogle Scholar
  41. Moir WH (1966) Influence of ponderosa pine on herbaceous vegetation. Ecol 47(6):1045–1048CrossRefGoogle Scholar
  42. Muys B, Granval P (1997) Earthworms as bio-indicaters of forest site quality. Soil Biol Biochem 29(3–4):323–328CrossRefGoogle Scholar
  43. Nilsson SI, Miller HG, Miller JD (1982) Forest growth as a possible cause of soil and water acidification - an examination of the concepts. Oikos 39(1):40–49CrossRefGoogle Scholar
  44. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GV, Solymos P, Stevens MHH, Wagner H (2013) vegan: community ecology package. R package version 2.1-24/r2394.
  45. Palow DT, Oberbauer SF (2009) Soil type affects seedling shade response at low light for two Inga species from Costa Rica. Plant Soil 319(1–2):25–35CrossRefGoogle Scholar
  46. 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
  47. Poorter H, Niinemets U, Poorter L, Wright IJ, Villar R (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182(3):565–588PubMedCrossRefGoogle Scholar
  48. Portsmuth A, Niinemets U (2007) Structural and physiological plasticity in response to light and nutrients in five temperate deciduous woody species of contrasting shade tolerance. Funct Ecol 21(1):61–77CrossRefGoogle Scholar
  49. R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  50. Reich PB, Oleksyn J, Modrzynski J, Mrozinski P, Hobbie SE, Eissenstat DM, Chorover J, Chadwick OA, Hale CM, Tjoelker MG (2005) Linking litter calcium, earthworms and soil properties: a common garden test with 14 tree species. Ecol Lett 8:811–818CrossRefGoogle Scholar
  51. Rothstein DE, Zak DR (2001) Photosynthetic adaptation and acclimation to exploit seasonal periods of direct irradiance in three temperate, deciduous-forest herbs. Funct Ecol 15(6):722–731CrossRefGoogle Scholar
  52. Sauer TJ, James DE, Cambardella CA, Hernandez-Ramirez G (2012) Soil properties following reforestation or afforestation of marginal cropland. Plant Soil 360(1–2):375–390CrossRefGoogle Scholar
  53. Stevenson FJ, Cole MA (1999) Cycles of soil, 2nd edn. Wiley, LondonGoogle Scholar
  54. Sydes C, Grime JP (1981) Effects of tree leaf litter on herbaceous vegetation in deciduous woodland I: field investigations. J Ecol 69(1):237–248CrossRefGoogle Scholar
  55. Taverna K, Peet RK, Phillips LC (2005) Long-term change in ground-layer vegetation of deciduous forests of the North Carolina Piedmont, USA. J Ecol 93:202–213CrossRefGoogle Scholar
  56. Thomaes A, De Keersmaeker L, De Schrijver A, Vandekerkhove K, Verschelde P, Verheyen K (2011) Can tree species choice influence recruitment of ancient forest species in post-agricultural forest? Plant Ecol 212(4):573–584CrossRefGoogle Scholar
  57. Thomaes A, De Keersmaeker L, Van Calster H, De Schrijver A, Vandekerkhove K, Verstraeten G, Verheyen K (2012) Diverging effects of two contrasting tree species on soil and herb layer development in a chronosequence of post-agricultural forest. For Ecol Manag 278:90–100CrossRefGoogle Scholar
  58. Thomas SC, Halpern CB, Falk DA, Liguori DA, Austin KA (1999) Plant diversity in managed forests: understory responses to thinning and fertilization. Ecol Appl 9:864–879CrossRefGoogle Scholar
  59. Van Calster H, Baeten L, Verheyen K, De Keersmaeker L, Dekeyser S, Rogister JE, Hermy M (2008) Diverging effects of overstorey conversion scenarios on the understorey vegetation in a former coppice-with-standards forest. For Ecol Manag 256(4):519–528CrossRefGoogle Scholar
  60. Van Miegroet H, Cole DW (1984) The impact of nitrification on soil acidification and cation leaching in a Red alder ecosystem. J Environ Qual 13(4):586–590CrossRefGoogle Scholar
  61. van Oijen D, Feijen M, Hommel P, den Ouden J, de Waal R (2005) Effects of tree species composition on within-forest distribution of understorey species. Appl Veg Sci 8(2):155–166CrossRefGoogle Scholar
  62. Vandecasteele B, De Vos B, Tack FMG (2002) Identification of dredged sediment-derived soils in the alluvial plains of the Leie and the Upper and Sea Scheldt rivers (Belgium) based on physico-chemical soil properties. J Environ Monit 4(2):306–312PubMedCrossRefGoogle Scholar
  63. Verheyen K, Guntenspergen G, Biesbrouck B, Hermy M (2003) An integrated analysis of the effects of past land-use on forest plant species colonization at the landscape scale. J Ecol 91:731–742CrossRefGoogle Scholar
  64. Verstraeten G, Baeten L, De Frenne P, Thomaes A, Demey A, Muys B, Verheyen K (submitted) Forest herbs show species-specific responses to the variation in light regime and soil acidification: an experiment mimicking forest conversion scenarios. Basic Appl EcolGoogle Scholar
  65. Weber-Blaschke G, Claus M, Rehfuess KE (2002) Growth and nutrition of ash (Fraxinus excelsior L.) and sycamore (Acer pseudoplatanus L.) on soils of different base saturation in pot experiments. For Ecol Manag 167(1–3):43–56CrossRefGoogle Scholar
  66. Wulf M, Naaf T (2009) Herb layer response to broadleaf tree species with different leaf litter quality and canopy structure in temperate forests. J Veg Sci 20(3):517–526CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Arno Thomaes
    • 1
  • Luc De Keersmaeker
    • 1
  • An De Schrijver
    • 2
  • Lander Baeten
    • 2
    • 3
  • Kris Vandekerkhove
    • 1
  • Gorik Verstraeten
    • 2
  • Kris Verheyen
    • 2
  1. 1.Research Institute for Nature and Forest (INBO)GeraardsbergenBelgium
  2. 2.Forest & Nature LabGhent UniversityGontrode (Melle)Belgium
  3. 3.Department of BiologyGhent UniversityGhentBelgium

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