Skip to main content

Advertisement

SpringerLink
Log in

Species-specific effects of soil fauna on fungal foraging and decomposition

  • Ecosystem ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Decomposer fungi are primary decomposing agents in terrestrial soils. Their mycelial networks play an important role in nutrient mineralisation and distribution, but are also nutritious resources for various soil invertebrates. Global climate change is predicted to alter the diversity and community composition of these soil fauna. To understand whether changes in invertebrate species diversity are likely to affect fungal-mediated decomposition, this study compared the grazing potentials of different invertebrate taxa and functional groups. Specifically, the grazing impacts of seven invertebrate taxa on the growth and spatial distribution of six basidiomycete fungi growing from beech wood blocks in soil microcosms were explored. Wood decay rates by fungi were also compared. The consequences of grazing were both taxon- and species-specific. Generally, macro-invertebrates caused the greatest damage, while meso- and micro-invertebrates often stimulated mycelial growth. Invertebrate size, preferences and population dynamics are likely to influence grazing potentials. Effects of grazing varied between fungi, with mycelial morphology and biochemistry possibly influencing susceptibility. Heavy grazing indirectly increased fungal-mediated wood decomposition. Changes in invertebrate community composition are predicted to have consequences for fungal growth, activity and community structure in woodland soils. Abiotic climate change factors including CO2 and temperature affect mycelial productivity directly, but the indirect effects, mediated through changes in the soil invertebrate community, may be equally important in controlling ecosystem functioning.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • A’Bear AD, Boddy L, Raspotnig G, Jones TH (2010) Non-trophic effects of oribatid mites on cord-forming basidiomycetes in soil microcosms. Ecol Entomol 35:477–484

    Google Scholar 

  • Baldrian P, Valásková V (2008) Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 32:501–521

    Article  PubMed  CAS  Google Scholar 

  • Bardgett RD (2005) The biology of soil. Oxford University Press, Oxford

    Book  Google Scholar 

  • Bardgett RD, Chan KF (1999) Experimental evidence that soil fauna enhance nutrient mineralization and plant nutrient in montane grassland ecosystems. Soil Biol Biochem 31:23–33

    Google Scholar 

  • Berg MP, Stoffer M, van der Heuvel HH (2004) Feeding guilds in Collembola based on digestive enzymes. Pedobiologia 48:589–601

    Article  Google Scholar 

  • Boddy L, Donnelly DP (2008) Fractal geometry and microorganisms in the environment. In: Senesi N, Wilkinson KJ (eds) Biophysical chemistry of fractal structures and processes in environmental systems. Wiley, Chichester, pp 239–272

    Chapter  Google Scholar 

  • Boddy L, Jones TH (2008) Interactions between Basidiomycota and invertebrates. In: Boddy L, Frankland JC, van West P (eds) Ecology of saprotrophic basidiomycete. Academic, San Diego, pp 155–179

    Chapter  Google Scholar 

  • Boddy L, Watkinson SC (1995) Wood decomposition, higher fungi, and their role in nutrient redistribution. Can J Bot 73:1377–1383

    Article  Google Scholar 

  • Bokhorst S, Huiskes A, Convey P, van Bodegomc PM, Aerts R (2008) Climate change effects on soil arthropod communities from the Falkland Islands and the Maritime Antarctic. Soil Biol Biochem 40:1547–1556

    Article  CAS  Google Scholar 

  • Bradford MA, Jones TH, Bardgett RD, Black HIJ, Boag B, Bonkowski M, Cook R, Eggers T, Gange AC, Grayston SJ, Kandeler E, McCaig AE, Newington JE, Prosser JI, Setala H, Staddon PL, Tordoff GM, Tscherko D, Lawton JH (2002) Impacts of soil faunal community composition on model grassland ecosystems. Science 298:615–617

    Article  PubMed  CAS  Google Scholar 

  • Bretherton S, Tordoff GM, Jones TH, Boddy L (2006) Compensatory growth of Phanerochaete velutina mycelial systems grazed by Folsomia candida (Collembola). Microbial Ecol 58:33–40

    Article  CAS  Google Scholar 

  • Butterfield J (1999) Changes in decomposition rates and Collembola densities during the forestry cycle in conifer plantations. J Appl Ecol 36:92–100

    Article  Google Scholar 

  • Croll NA (1970) The behavior of nematodes. Edward Arnold, London

    Google Scholar 

  • Deacon J (2006) Fungal biology. Blackwell, Oxford

    Google Scholar 

  • Dowson CG, Rayner ADM, Boddy L (1988) Inoculation of mycelial cord-forming Basidiomycetes in woodland soil and litter. II. Resource capture and persistence. New Phytol 109:343–349

    Article  Google Scholar 

  • Dutton MV, Evans CS, Atkey PT, Wood DA (1993) Oxalate production by basidiomycetes, including the white-rot species Coriolus versicolor and Phanerochaete chrysoporium. Appl Microbiol Biot 39:5–10

    CAS  Google Scholar 

  • Dyer HC, Boddy L, Preston-Meek CM (1992) Effect of the nematode Panagrellus redivivus on growth and enzyme production by Phanerochaete velutina and Stereum hirsutum. Mycol Res 96:1019–1028

    Article  CAS  Google Scholar 

  • Gange AC, Gange EG, Sparks TH, Boddy L (2007) Rapid and recent changes in fungal fruiting patterns. Science 306:71

    Article  Google Scholar 

  • Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall DH, Hättenschwiler S (2010) Diversity meets decomposition. Trends Ecol Evol 25:372–380

    Article  PubMed  Google Scholar 

  • Hättenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218

    Article  Google Scholar 

  • Hedlund K, Boddy L, Preston CM (1991) Mycelial responses of the soil fungus Mortierella isabellina to grazing by Onychiurus armatus (Collembola). Soil Biol Biochem 36:591–599

    Google Scholar 

  • Hiol Hiol FH, Dixon RK, Curl EA (1994) The feeding preference of mycophagous collembola varies with the ectomycorrhizal symbiont. Mycorrhiza 5:99–103

    Article  Google Scholar 

  • Hopkin SP (1990) Species-specific differences in the net assimilation of zinc, cadmium, lead, copper and iron by the terrestrial isopods Oniscus asellus and Porcellio scaber. J Appl Ecol 27:460–474

    Article  Google Scholar 

  • Hynes J, Muller CT, Jones TH, Boddy L (2007) Changes in volatile production during the course of fungal mycelial interactions between Hypholoma fasciculare and Resinicium bicolor. J Chem Ecol 33:43–57

    Article  PubMed  CAS  Google Scholar 

  • Jones TH, Thompson LJ, Lawton JH, Bezemer TM, Bardgett RD, Blackburn TM, Bruce KD, Cannon PF, Hall GS, Hartley SE, Howson G, Jones CG, Kampichler C, Kandeler E, Ritchie DA (1998) Impacts of rising atmospheric carbon dioxide on model terrestrial ecosystems. Science 280:441–443

    Article  PubMed  CAS  Google Scholar 

  • Kaneko N, McLean MA, Parkinson D (1998) Do mites and Collembola affect pine litter fungal biomass and microbial respiration? Appl Soil Ecol 9:209–213

    Article  Google Scholar 

  • Kempken F, Rohlfs M (2010) Fungal secondary metabolite biosysthesis—a chemical defence strategy againsy antagonistic animals? Fungal Ecol 3:1–8

    Article  Google Scholar 

  • Klironomos JN, Widden P, Deslandes I (1992) Feeding preferences of the collembolan Folsomia candida in relation to microfungal succession on decaying litter. Soil Biol Biochem 24:685–692

    Article  Google Scholar 

  • Ladygina N, Dedyukhina EG, Vainshtein MB (2006) A review on microbial synthesis of hydrocarbons. Process Biochem 41:1001–1014

    Article  CAS  Google Scholar 

  • Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808

    Article  PubMed  CAS  Google Scholar 

  • Maraun M, Martens H, Migge S, Theenhaus A, Scheu S (2003) Adding to ‘the enigma of soil animal diversity’: Fungal feeders and saprotrophic soil invertebrates prefer similar food substrates. Eur J Soil Biol 39:85–95

    Article  Google Scholar 

  • McNaughton SJ (1983) Compensatory plant growth as a response to herbivory. Oikos 40:329–336

    Article  Google Scholar 

  • Mitschunas N, Wagner M, Filser J (2006) Evidence for a positive influence of fungivorous soil invertebrates on the seed bank persistence of grassland species. J Ecol 94:791–800

    Article  Google Scholar 

  • Molano-Flores B (2001) Herbivory and calcium concentrations affect calcium oxalate crystal formation in leaves of Sida (Malvaceae). Ann Bot (London) 88:387–391

    Article  CAS  Google Scholar 

  • Newell K (1984) Interaction between two decomposer Basidiomycetes and a collembolan under Sitka spruce: grazing and its potential effects on fungal distribution and litter decomposition. Soil Biol Biochem 16:235–239

    Article  Google Scholar 

  • Petersen H, Luxton M (1982) A comparative analysis of soil fauna populations and their role in the decomposition process. Oikos 39:287–388

    Google Scholar 

  • Seastedt TR (1984) The role of microarthropods in decomposition and mineralisation processes. Annu Rev Entomol 29:25–46

    Article  Google Scholar 

  • Setälä H, Berg PM, Jones TH (2005) Trophic structure and functional redundancy in soil communities. In: Bardgett RD, Usher MB, Hopkins DW (eds) Biological diversity and function in soils. Cambridge University Press, Cambridge, pp 236–249

    Chapter  Google Scholar 

  • Shimada M, Akamtsu Y, Tokimatsu T, Mii K, Hattori T (1997) Possible biochemical roles of oxalic acid as a low molecular weight compound involved in brown-rot and white-rot wood decays. J Biotechnol 59:103–113

    Article  Google Scholar 

  • Southwood TRE, Henderson PA (2000) Ecological methods, 3rd edn. Blackwell, Oxford

    Google Scholar 

  • Staddon P, Lindo Z, Crittenden PD, Gilbert F, Gonzales A (2010) Connectivity, non-random extinction and ecosystem function in experimental metacommunities. Ecol Lett 13:543–552

    Article  PubMed  Google Scholar 

  • Topp W, Kappes H, Kulfan J, Zach P (2006) Distribution pattern of woodlice (Isopoda) and millipedes (Diplopoda) in four primeval forests of the Western Carpathians (Central Slovakia). Soil Biol Biochem 38:43–50

    Article  CAS  Google Scholar 

  • Tordoff GM, Boddy L, Jones TH (2006) Grazing by Folsomia candida (Collembola) differently affects mycelial morphology of the cord-forming bacidiomycetes Hypholoma fasciculare, Phanerochaete velutina, and Resinicium bicolour. Mycol Res 110:335–345

    Article  PubMed  Google Scholar 

  • Tordoff GM, Boddy L, Jones TH (2008) Species-specific impacts of collembola grazing on fungal foraging ecology. Soil Biol Biochem 40:434–442

    Article  CAS  Google Scholar 

  • van der Putten I, van der Putten WH (2010) Impacts of soil microbial communities on exotic plant invasions. Trends Ecol Evol 25:512–519

    Article  PubMed  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633

    Article  PubMed  CAS  Google Scholar 

  • Wiggins EA, Curl EA, Harper JD (1979) Effects of soil fertility and cotton rhizosphere on populations of collembola. Pedobiologia 19:77–82

    Google Scholar 

  • Wolters V, Silver WL, Bignell DE, Coleman DC, Lavelle P, van der Putten WH, de Ruiter P, Rusek J, Wall DH, Wardle DA, Brussard L, Dangerfield JM, Brown VK, Giller KE, Hooper DU, Tiedje J, Sala O, van Veen JA (2000) Effects of global changes on above- and belowground biodiversity in terrestrial ecosystems: implications for ecosystem functioning. Bioscience 50:1089–1098

    Article  Google Scholar 

  • Yeates GW, Bongers T, de Goede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in soil nematode families and genera–an outline for soil ecologists. J Nematol 25:315–331

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Don A’Bear, Matthew Dray, Eleanor Kean and Eleanor Sherrard Smith provided comments during manuscript preparation. The work was funded by the Natural Environment Research Council (NE/G523420/1).

Author information

Authors and Affiliations

  1. Cardiff School of Biosciences, Cardiff University, Museum Avenue, Cardiff, CF10 3AX, UK

    Thomas W. Crowther, Lynne Boddy & T. Hefin Jones

Authors
  1. Thomas W. Crowther
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lynne Boddy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. T. Hefin Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lynne Boddy.

Additional information

Communicated by Hakan Wallander.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Crowther, T.W., Boddy, L. & Jones, T.H. Species-specific effects of soil fauna on fungal foraging and decomposition. Oecologia 167, 535–545 (2011). https://doi.org/10.1007/s00442-011-2005-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-011-2005-1

Keywords

Search

Navigation