Plant and Soil

, Volume 379, Issue 1–2, pp 121–133

Impact of understory mosses and dwarf shrubs on soil micro-arthropods in a boreal forest chronosequence

  • Stef Bokhorst
  • David A. Wardle
  • Marie-Charlotte Nilsson
  • Michael J. Gundale
Regular Article

Abstract

Aims

Plant species and functional groups are known to drive the community of belowground invertebrates but whether their effects are consistent across environmental gradients is less well understood. We aimed to determine if plant effects on belowground communities are consistent across a successional gradient in boreal forests of northern Sweden.

Methods

We performed two plant removal experiments across ten stands that form a 364-year post-fire boreal forest chronosequence. Through the removal of plant functional groups (mosses or dwarf shrubs) and of individual species of dwarf shrubs, we aimed to determine if the effects of functional groups and species on the soil micro-arthropod community composition varied across this chronosequence.

Results

Removal of mosses had a strong negative impact on the abundance and diversity of Collembola and Acari and this effect was consistent across the chronosequence. Only specific Oribatid families declined following dwarf-shrub species removals, with some of these responses being limited to old forest stands.

Conclusions

Our results show that the impacts of plants on micro-arthropods is consistent across sites that vary considerably in their stage of post-fire ecosystem development, despite these stages differing greatly in plant productivity, fertility, humus accumulation and moss development. In addition, mosses are a much stronger driver of the micro-arthropod community than vascular plants.

Keywords

Acari Collembola Empetrum hermaphroditum Feather moss Vaccinium myrtillus Vaccinium vitis-idaea 

Supplementary material

11104_2014_2055_MOESM1_ESM.docx (16 kb)
ESM 1(DOCX 16 kb)
11104_2014_2055_MOESM2_ESM.docx (1 mb)
ESM 2(DOCX 1073 kb)

References

  1. Bardgett RD (2002) Causes and consequences of biological diversity in soil. Zoology 105:367–374PubMedCrossRefGoogle Scholar
  2. Blok D, Heijmans M, Schaepman-Strub G, van Ruijven J, Parmentier FJW, Maximov TC, Berendse F (2011) The cooling capacity of mosses: controls on water and energy fluxes in a Siberian Tundra site. Ecosystems 14:1055–1065CrossRefGoogle Scholar
  3. Bokhorst S, Huiskes A, Convey P, Aerts R (2007) Climate change effects on organic matter decomposition rates in ecosystems from the Maritime Antarctic and Falkland Islands. Global Change Biol 13:2642–2653CrossRefGoogle Scholar
  4. Bokhorst S, Huiskes AHL, Convey P, Bodegom PMV, Aerts R (2008) Climate change effects on soil arthropod communities from the Falkland Islands and the Maritime Antarctic. Soil Biol Biochem 40:1547–1556CrossRefGoogle Scholar
  5. Bonkowski M, Villenave C, Griffiths B (2009) Rhizosphere fauna: the functional and structural diversity of intimate interactions of soil fauna with plant roots. Plant Soil 321:213–233CrossRefGoogle Scholar
  6. Chauvat M, Trap J, Perez G, Delporte P, Aubert M (2011) Assemblages of Collembola across a 130-year chronosequence of beech forest. Soil Organisms 83:405–418Google Scholar
  7. Cornelissen JHC, Perez-Harguindeguy N, Diaz S, Grime JP, Marzano B, Cabido M, Vendramini F, Cerabolini B (1999) Leaf structure and defence control litter decomposition rate across species and life forms in regional floras on two continents. New Phyt 143:191–200CrossRefGoogle Scholar
  8. Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Pérez-Harguindeguy H, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, van Bodegom P, Brovkin V, Alex Chatain A, Callaghan TV, Díaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti V, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–1071PubMedCrossRefGoogle Scholar
  9. De Deyn GB, Raaijmakers CE, Zoomer HR, Berg MP, de Ruiter PC, Verhoef HA, Bezemer TM, van der Putten WH (2003) Soil invertebrate fauna enhances grassland succession and diversity. Nature 422:711–713PubMedCrossRefGoogle Scholar
  10. DeLuca TH, Nilsson MC, Zackrisson O (2002) Nitrogen mineralization and phenol accumulation along a fire chronosequence in northern Sweden. Oecol 133:206–214CrossRefGoogle Scholar
  11. DeLuca TH, Zackrisson O, Gentili F, Sellstedt A, Nilsson MC (2007) Ecosystem controls on nitrogen fixation in boreal feather moss communities. Oecol 152:121–130CrossRefGoogle Scholar
  12. Diaz S, Symstad AJ, Chapin FS, Wardle DA, Huenneke LF (2003) Functional diversity revealed by removal experiments. Trends Ecol Evolut 18:140–146CrossRefGoogle Scholar
  13. Eisenhauer N, Reich PB (2012) Above- and below-ground plant inputs both fuel soil food webs. Soil Biol Biochem 45:156–160CrossRefGoogle Scholar
  14. Eisenhauer N, Schadler M (2011) Inconsistent impacts of decomposer diversity on the stability of aboveground and belowground ecosystem functions. Oecol 165:403–415CrossRefGoogle Scholar
  15. Eisenhauer N, Sabais ACW, Scheu S (2011) Collembola species composition and diversity effects on ecosystem functioning vary with plant functional group identity. Soil Biol Biochem 43:1697–1704CrossRefGoogle Scholar
  16. Endlweber K, Scheu S (2007) Interactions between mycorrhizal fungi and Collembola: effects on root structure of competing plant species. Biol Fertil Soils 43:741–749CrossRefGoogle Scholar
  17. Filser J (2002) The role of Collembola in carbon and nitrogen cycling in soil. Pedobiologia 46:234–245Google Scholar
  18. Fjellberg A (1998) The Collembola of Fennoscandia and Denmark Part 1: Poduromorpha, vol 35. Fauna Entomologica Scandinavica. Brill, LeidenGoogle Scholar
  19. Fjellberg A (2007) The Collembola of Fennoscandia and Denmark Part 2: Entomobryomorpha and Symphypleona. Fauna Entomologica Scandinavica, vol 42. Brill, LeidenGoogle Scholar
  20. Gisin H (1943) Ökologie und Lebensgmeinschaften der Collembolen im Schweizer Exkursiongebiet Basels. Rev Suisse Zool 50:131–224Google Scholar
  21. Gundale MJ, Wardle DA, Nilsson MC (2010) Vascular plant removal effects on biological N fixation vary across a boreal forest island gradient. Ecol 91:1704–1714CrossRefGoogle Scholar
  22. Gundale MJ, Wardle DA, Nilsson MC (2012) The effect of altered macroclimate on N-fixation by boreal feather mosses. Biol Lett 8:805–808PubMedCentralPubMedCrossRefGoogle Scholar
  23. Hågvar S (1982) Collembola in Norwegian coniferous forest soils 1. Relations to plant communities and soil fertility. Pedobiologia 24:255–296Google Scholar
  24. Hågvar S (1984) Six common mite species (Acari) in Norwegian coniferous forest soils: relations to vegetaion types and soil characteristics. Pedobiologia 27:355–364Google Scholar
  25. Hågvar S, Abrahamsen G (1984) Collembola in Norwegian coniferous forest soils III. Relations to soil chemistry. Pedobiologia 27:331–339Google Scholar
  26. Heemsbergen DA, Berg MP, Loreau M, van Hal JR, Faber JH, Verhoef HA (2004) Biodiversity effects on soil processes explained by interspecific functional dissimilarity. Science 306:1019–1020PubMedCrossRefGoogle Scholar
  27. Hyodo F, Kusaka S, Wardle DA, Nilsson MC (2013) Changes in stable nitrogen and carbon isotope ratios of plants and soil across a boreal forest fire chronosequence. Plant Soil 364:111–119CrossRefGoogle Scholar
  28. Jackson BG, Nilsson MC, Wardle DA (2013) The effects of the moss layer on the decomposition of intercepted vascular plant litter across a post-fire boreal forest chronosequence. Plant SoilGoogle Scholar
  29. Krab EJ, Berg MP, Aerts R, van Logtestijn RSP, Cornelissen JHC (2013) Vascular plant litter input in subarctic peat bogs changes Collembola diets and decomposition patterns. Soil Biol Biochem 63:106–115CrossRefGoogle Scholar
  30. Krantz GW, Walter DE (2009) A manual of Acarology. Texas Tech University Press, LubbockGoogle Scholar
  31. Lang SI, Cornelissen JHC, Klahn T, Van Logtestijn RSP, Broekman R, Schweikert W, Aerts R (2009) An experimental comparison of chemical traits and litter decomposition rates in a diverse range of subarctic bryophyte, lichen and vascular plant species. J Ecol 97:886–900CrossRefGoogle Scholar
  32. Liefting M, Ellers J (2008) Habitat-specific differences in thermal plasticity in natural populations of a soil arthropod. Biol J Linnean Soc 94:265–271CrossRefGoogle Scholar
  33. Lindo Z, Nilsson M-C, Gundale MJ (2013) Bryophyte-cyanobacteria associations as regulators of the northern latitude carbon balance in response to global change. Global Change Biol 19:2022–2035CrossRefGoogle Scholar
  34. Marshall CB, McLaren JR, Turkington R (2011) Soil microbial communities resistant to changes in plant functional group composition. Soil Biol Biochem 43:78–85CrossRefGoogle Scholar
  35. McLaren JR, Turkington R (2010) Ecosystem properties determined by plant functional group identity. J Ecol 98:459–469CrossRefGoogle Scholar
  36. Milcu A, Partsch S, Langel R, Scheu S (2006) The response of decomposers (earthworms, springtails and microorganisms) to variations in species and functional group diversity of plants. OIKOS 112:513–524CrossRefGoogle Scholar
  37. Nielsen UN, Osler GHR, Campbell CD, Burslem D, van der Wal R (2010a) The influence of vegetation type, soil properties and precipitation on the composition of soil mite and microbial communities at the landscape scale. J Biogeography 37:1317–1328CrossRefGoogle Scholar
  38. Nielsen UN, Osler GHR, Campbell CD, Neilson R, Burslem D, van der Wal R (2010b) The enigma of soil animal species diversity revisited: the role of small-scale heterogeneity. Plos One 5:6CrossRefGoogle Scholar
  39. Nielsen UN, Osler GHR, Campbell CD, Burslem D, van der Wal R (2012) Predictors of fine-scale spatial variation in soil mite and microbe community composition differ between biotic groups and habitats. Pedobiologia 55:83–91CrossRefGoogle Scholar
  40. Pande YD, Berthet P (1973) Studies on the food and feeding habits of soil oribatei in a black pine plantation. Oecol 12:413–426CrossRefGoogle Scholar
  41. Parkinson D, Visser S, Whittaker JB (1979) Effects of Collembolan grazing on fungal colonization of leaf litter. Soil Biol Biochem 11:529–535CrossRefGoogle Scholar
  42. Perez G, Decaëns T, Dujardin G, Akpa-Vinceslas M, Langlois E, Chauvat M (2013) Response of collembolan assemblages to plant species successional gradient. PedobiologiaGoogle Scholar
  43. Proctor MCF (2000) Physiological ecology. In: Shaw AJ, Goffinet B (eds) Bryophyte biology. Cambridge University Press, Cambridge, pp 225–247CrossRefGoogle Scholar
  44. Sabais ACW, Scheu S, Eisenhauer N (2011) Plant species richness drives the density and diversity of Collembola in temperate grassland. Acta Oecol 37:195–202CrossRefGoogle Scholar
  45. Salmane I, Brumelis G (2008) The importance of the moss layer in sustaining biological diversity of Gamasina mites in coniferous forest soil. Pedobiologia 52:69–76CrossRefGoogle Scholar
  46. Salmon S, Mantel J, Frizzera L, Zanella A (2006) Changes in humus forms and soil animal communities in two developmental phases of Norway spruce on an acidic substrate. Forest Ecol Manag 237:47–56CrossRefGoogle Scholar
  47. Scheu S, Schulz E (1996) Secondary succession, soil formation and development of a diverse community of oribatids and saprophagous soil macro-invertebrates. Biodivers Conserv 5:235–250CrossRefGoogle Scholar
  48. Schneider K, Migge S, Norton RA, Scheu S, Langel R, Reineking A, Maraun M (2004) Trophic niche differentiation in soil microarthropods (Oribatida, acari): evidence from stable isotope ratios (15N/14N). Soil Biol Biochem 36:1769–1774CrossRefGoogle Scholar
  49. Seastedt TR, Crossley DA (1980) Effects of microarthropods on the seasonal dynamics of nutrients in forest litter. Soil Biol Biochem 12:337–342CrossRefGoogle Scholar
  50. Siepel H, De Ruiter-Dijkman EM (1993) Feeding guilds of Oribatid mites based on their carbohydrase activities. Soil Biol Biochem 25:1491–1497CrossRefGoogle Scholar
  51. Spehn E, Joshi J, Schmid B, Alphei J, Körner C (2000) Plant diversity effects on soil heterotrophic activity in experimental grassland ecosystems. Plant Soil 224:217–230CrossRefGoogle Scholar
  52. St John MG, Wall DH, Behan-Pelletier VM (2006) Does plant species co-occurrence influence soil mite diversity? Ecol 87:625–633CrossRefGoogle Scholar
  53. St John MG, Bellingham PJ, Walker LR, Orwin KH, Bonner KI, Dickie IA, Morse CW, Yeates GW, Wardle DA (2012) Loss of a dominant nitrogen-fixing shrub in primary succession: consequences for plant and below-ground communities. J Ecol 100:1074–1084CrossRefGoogle Scholar
  54. Suding KN, Miller AE, Bechtold H, Bowman WD (2006) The consequence of species loss on ecosystem nitrogen cycling depends on community compensation. Oecol 149:141–149CrossRefGoogle Scholar
  55. Tybirk K, Nilsson MC, Michelson A, Kristensen HL, Shevtsova A, Strandberg MT, Johansson M, Nielsen KE, Rils-Nielsen T, Strandberg B, Johnsen I (2000) Nordic Empetrum dominated ecosystems: Function and susceptibility to environmental changes. Ambio 29:90–97Google Scholar
  56. Urcelay C, Diaz S, Gurvich DE, Chapin FS, Cuevas E, Dominguez LS (2009) Mycorrhizal community resilience in response to experimental plant functional type removals in a woody ecosystem. J Ecol 97:1291–1301CrossRefGoogle Scholar
  57. Van der Putten WH, Vet LEM, Harvey JA, Wackers FL (2001) Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol Evolut 16:547–554CrossRefGoogle Scholar
  58. Van Dooremalen C, Berg MP, Ellers J (2013) Acclimation responses to temperature vary with vertical stratification: implications for vulnerability of soil-dwelling species to extreme temperature events. Global Change Biol 19:975–984CrossRefGoogle Scholar
  59. Van Straalen NM, Rijninks PC (1982) The efficiency of Tullgren apparatus with respect to interpreting seasonal changes in age structure of soil arthropod populations. Pedobiologia 24:197–209Google Scholar
  60. Walker LR, Moral. Rd (2003) Primary succession and ecosystem rehabilitation. Cambridge University PressGoogle Scholar
  61. Ward SE, Bardgett RD, McNamara NP, Ostle NJ (2009) Plant functional group identity influences short-term peatland ecosystem carbon flux: evidence from a plant removal experiment. Funct Ecol 23:454–462CrossRefGoogle Scholar
  62. Wardle DA, Zackrisson O (2005) Effects of species and functional group loss on island ecosystem properties. Nature 435:806–810PubMedCrossRefGoogle Scholar
  63. Wardle DA, Bonner KI, Barker GM, Yeates GW, Nicholson KS, Bardgett RD, Watson RN, Ghani A (1999) Plant removals in perennial grassland: vegetation dynamics, decomposers, soil biodiversity, and ecosystem properties. Ecol Monograph 69:535–568CrossRefGoogle Scholar
  64. Wardle DA, Jonsson M, Bansal S, Bardgett RD, Gundale MJ, Metcalfe DB (2012) Linking vegetation change, carbon sequestration and biodiversity: insights from island ecosystems in a long-term natural experiment. J Ecol 100:16–30CrossRefGoogle Scholar
  65. Weigmann G (2006) Hornmilben (Oribatida). Tierwelt Deutschlands 76. Goecke and Evers, KelternGoogle Scholar
  66. Zackrisson O (1980) Forest fire history: ecological significance and dating problems in the North Swedish Boreal Forest. In: The fire history workshop, Laboratory of Tree-Ring Research, University of Arizona, Tucson, October 20–24, 1980Google Scholar
  67. Zackrisson O, Nilsson MC, Wardle DA (1996) Key ecological function of charcoal from wildfire in the Boreal forest. Oikos 77:10–19CrossRefGoogle Scholar
  68. Zackrisson O, DeLuca TH, Nilsson MC, Sellstedt A, Berglund LM (2004) Nitrogen fixation increases with successional age in boreal forests. Ecol 85:3327–3334CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Stef Bokhorst
    • 1
  • David A. Wardle
    • 1
  • Marie-Charlotte Nilsson
    • 1
  • Michael J. Gundale
    • 1
  1. 1.Department of Forest Ecology and ManagementSwedish University of Agricultural SciencesUmeåSweden

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