Oecologia

, Volume 142, Issue 4, pp 636–642

Arbuscular mycorrhiza and Collembola interact in affecting community composition of saprotrophic microfungi

Community Ecology

Abstract

The functioning of the plant-mycorrhiza system depends on interactions with other organisms, including saprotrophic (ST) soil fungi. The interactions between mycorrhizal and ST fungi are likely affected by fungivorous soil animals, such as Collembola. In a two-factorial laboratory experiment lasting for 30 weeks we assessed the effects of an arbuscular mycorrhizal fungus (Glomus mosseae) and Collembola (Protaphorura fimata, Heteromurus nitidus and Folsomia candida) on the community composition of ST microfungi in soil planted with the invasive grass Cynodon dactylon. The presence of mycorrhiza substantially reduced total plant biomass and reduced N and P availability to the soil microflora, though these effects were less pronounced in the presence of Collembola. The density of Collembola was high (corresponding to about 2×105 individuals m−2) and was not affected by the presence of G. mosseae. In spite of the large amount of mycorrhizal mycelium in soil, it contributed little to Collembola nutrition. The presence of mycorrhiza strongly affected the community structure of ST soil fungi. In particular, mycorrhiza reduced the relative abundance of Trichoderma harzianum and Exophiala sp., but increased the abundance of Ramichloridium schulzeri and several sterile forms. However, the difference between fungal communities in mycorrhizal and non-mycorrhizal treatments was much more pronounced in the presence of Collembola. Presumably, the intense grazing by Collembola destabilized the ST fungal community, thereby making it more susceptible to the influence of G. mosseae. These results document for the first time that fungal feeding soil invertebrates can significantly affect the interactions between mycorrhizal fungi and ST soil microorganisms.

Keywords

Soil microflora Microbial competition Species interactions Similarity indexes Mycorrhiza functioning 

References

  1. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Aust Ecol 26:32–46CrossRefGoogle Scholar
  2. Anderson MJ (2004) PERMANOVA_2factor: a FORTRAN computer program for permutational multivariate analysis of variance using permutation tests. Department of Statistics, University of AucklandGoogle Scholar
  3. Andrade G, Linderman RG, Bethlenfalvay GJ (1998) Bacterial associations with the mycorrhizosphere and hyphosphere of the arbuscular mycorrhizal fungus Glomus mosseae. Plant Soil 202:79–87CrossRefGoogle Scholar
  4. Bakonyi G, Posta K, Kiss I, Fabian M, Nagy P, Nosek JN (2002) Density-dependent regulation of arbuscular mycorrhiza by Collembola. Soil Biol Biochem 34:661–664CrossRefGoogle Scholar
  5. Barea JM, Azcón R, Azcón-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie van Leeuwenhoek J Microbiol Serol 81:343–351CrossRefGoogle Scholar
  6. Curry JP (1994) Grassland invertebrates. Chapman and Hall, LondonGoogle Scholar
  7. Filion M, St-Arnaud M, Fortin JA (1999) Direct interaction between the arbuscular mycorrhizal fungus Glomus intraradices and different rhizosphere microorganisms. New Phytol 141:525–533CrossRefGoogle Scholar
  8. Fitter AH, Garbaye J (1994) Interactions between mycorrhizal fungi and other soil organisms. Plant Soil 159:123–132Google Scholar
  9. Gams W, Domsch KH (1967) Beiträge zur Anwendung der Bodenwaschtechnik für die Isolierung von Bodenpilzen. Arch Mikrobiol 58:134–144CrossRefGoogle Scholar
  10. Gange AC (2000) Arbuscular mycorrhizal fungi, Collembola and plant growth. Trends Ecol Evol 15:369–372CrossRefPubMedGoogle Scholar
  11. Gange AC, Ayres RL (1999) On the relation between arbuscular mycorrhizal colonization and plant “benefit”. Oikos 87:615–621Google Scholar
  12. Green H, Larsen J, Olsson PA, Jensen DF, Jakobsen I (1999) Suppression of the biocontrol agent Trichoderma harzianum by mycelium of the arbuscular mycorrhizal fungus Glomus intraradices in root-free soil. Appl Environ Microbiol 65:1428–1434PubMedGoogle Scholar
  13. Hodge A (2000) Microbial ecology of the arbuscular mycorrhiza. FEMS Microbiol Ecol 32:91–96Google Scholar
  14. Hodge A, Stewart J, Robinson D, Griffiths BS, Fitter AH (2000) Competition between roots and soil micro-organisms for nutrients from nitrogen-rich patches of varying complexity. J Ecol 88:150–164CrossRefGoogle Scholar
  15. Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299CrossRefPubMedGoogle Scholar
  16. Horn HS (1966) Measurements of “overlap” in comparative ecological studies. Am Nat 100:419–424CrossRefGoogle Scholar
  17. Jakobsen I, Rosendahl L (1990) Carbon flow into soil and external hyphae from roots of mycorrhizal cucumber plants. New Phytol 115:77–83Google Scholar
  18. Johnson NC, Graham JH, Smith FA (1997) Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol 135:575–586CrossRefGoogle Scholar
  19. Johnson D, Leake JR, Ostle N, Ineson P, Read DJ (2002) In situ 13CO2 pulse-labelling of upland grassland demonstrates a rapid pathway of carbon flux from arbuscular mycorrhizal mycelia to the soil. New Phytol 153:327–334CrossRefGoogle Scholar
  20. Kaye JP, Hart SC (1997) Competition for nitrogen between plants and soil microorganisms. Trends Ecol Evol 12:139–143CrossRefGoogle Scholar
  21. Klironomos JN, Kendrick WB (1995) Stimulative effects of arthropods on endomycorrhizas of sugar maple in the presence of decaying litter. Funct Ecol 9:528–536Google Scholar
  22. Klironomos JN, Kendrick WB (1996) Palatability of microfungi to soil arthropods in relation to the functioning of arbuscular mycorrhizae. Biol Fertil Soils 21:43–52CrossRefGoogle Scholar
  23. Klironomos JN, Ursic M (1998) Density-dependent grazing on the extraradical hyphal network of the arbuscular mycorrhizal fungus, Glomus intraradices, by the collembolan, Folsomia candida. Biol Fertil Soils 26:250–253CrossRefGoogle Scholar
  24. 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 24:685–692CrossRefGoogle Scholar
  25. Klironomos JN, Rillig MC, Allen MF, Zak DR, Kubiske M, Pregitzer KS (1997) Soil fungal-arthropod responses to Populus tremuloides grown under enriched atmospheric CO2 under field conditions. Global Change Biol 3:473–478CrossRefGoogle Scholar
  26. Klironomos JN, Bednarczuk EM, Neville J (1999) Reproductive significance of feeding on saprobic and arbuscular mycorrhizal fungi by the collembolan, Folsomia candida. Funct Ecol 13:756–761CrossRefGoogle Scholar
  27. Krebs CJ (1989) Ecological methodology. Harper Collins, New YorkGoogle Scholar
  28. Larsen J, Olsson PA, Jakobsen I (1998) The use of fatty acid signatures to study mycelial interactions between the arbuscular mycorrhizal fungus Glomus intraradices and the saprotrophic fungus Fusarium culmorum in root-free soil. Mycol Res 102:1491–1496CrossRefGoogle Scholar
  29. Linderman RG (1988) Mycorrhizal interactions with the rhizosphere mycoflora: the mycorrhizosphere effect. Phytopathology 78:366–370Google Scholar
  30. Magurran AE (1988) Ecological diversity and its measurement. Princeton University Press, Princeton, N.J.Google Scholar
  31. Marschner P, Baumann K (2003) Changes in bacterial community structure induced by mycorrhizal colonisation in split-root maize. Plant Soil 251:279–289CrossRefGoogle Scholar
  32. Marschner P, Crowley DE, Lieberei R (2001) Arbuscular mycorrhizal infection changes the bacterial 16 S rDNA community composition in the rhizosphere of maize. Mycorrhiza 11:297–302CrossRefGoogle Scholar
  33. McAllister CB, Garcia-Romera I, Godeas A, Ocampo JA (1994) Interactions between Trichoderma koningii, Fusarium solani and Glomus mosseae—effects on plant growth, arbuscular mycorrhizas and the saprophyte inoculants. Soil Biol Biochem 26:1363–1367CrossRefGoogle Scholar
  34. McAllister CB, Garcia-Garrido JM, Garcia-Romera I, Godeas A, Ocampo JA (1996) Interactions between Alternaria alternata, Fusarium equiseti and Glomus mosseae. I. Endophyte-saprophyte interactions in vitro. Symbiosis 20:163–174Google Scholar
  35. McArdle BH, Anderson MJ (2001). Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–297Google Scholar
  36. Medina A, Probanza A, Gutierrez Mañero FJ, Azcón R (2003) Interactions of arbuscular-mycorrhizal fungi and Bacillus strains and their effects on plant growth, microbial rhizosphere activity (thymidine and leucine incorporation) and fungal biomass (ergosterol and chitin). Appl Soil Ecol 22:15–28CrossRefGoogle Scholar
  37. Newell K (1984) Interactions between two decomposer basidiomycetes and a collembolan under Sitka spruce: distribution, abundance and selective grazing. Soil Biol Biochem 16:227–233CrossRefGoogle Scholar
  38. Olsson PA, Francis R, Read DJ, Soderstrom B (1998) Growth of arbuscular mycorrhizal mycelium in calcareous dune sand and its interaction with other soil microorganisms as estimated by measurement of specific fatty acids. Plant Soil 201:9–16CrossRefGoogle Scholar
  39. Parkinson D, Visser S, Whittaker JB (1979) Effects of collembolan grazing on fungal colonization of leaf litter. Soil Biol Biochem 11:529–535CrossRefGoogle Scholar
  40. Puzachenko YG, Kuznetsov GV (1998) Ecological differentiation of rodents in tropical semi-evergreen broad-leaved forests of North Vietnam (in Russian). Zool Z 77:117–132Google Scholar
  41. Scheu S (1992) Automated measurement of the respiratory response of soil microcompartments—active microbial biomass in earthworm faeces. Soil Biol Biochem 24:1113–1118CrossRefGoogle Scholar
  42. Schreiner RP, Bethlenfalvay GJ (2003) Crop residue and Collembola interact to determine the growth of mycorrhizal pea plants. Biol Fertil Soils 39:1–8Google Scholar
  43. Schreiner RP, Mihara KL, McDaniel H, Bethlenfalvay GJ (1997) Mycorrhizal fungi influence plant and soil functions and interactions. Plant Soil 188:199–209CrossRefGoogle Scholar
  44. Smith SE, Read DJ (1997) Mycorrhizal Symbiosis. Academic Press, LondonGoogle Scholar
  45. Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New YorkGoogle Scholar
  46. Sylvia DM (1994) Vesicular-arbuscular mycorrhizal fungi. In: Weaver RW et al (eds) Methods of soil analysis, part 2. Microbiological and biochemical properties. American Society of Agronomy, Madison, Wis., pp 351–378Google Scholar
  47. Tiunov AV, Scheu S (2000) Microfungal communities in soil, litter and casts of Lumbricus terrestris L. (Lumbricidae): a laboratory experiment. Appl Soil Ecol 14:17–26CrossRefGoogle Scholar
  48. Tiunov AV, Scheu S (2004) Carbon availability controls the growth of detritivores (Lumbricidae) and their effect on nitrogen mineralization. Oecologia 138:83–90CrossRefPubMedGoogle Scholar
  49. Vazquez MM, Cesar S, Azcón R, Barea JM (2000) Interactions between arbuscular mycorrhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl Soil Ecol 15:261–272CrossRefGoogle Scholar
  50. Wolda H (1981) Similarity indices, sample size and diversity. Oecologia 50:296–302CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  1. 1.Laboratory of Soil ZoologyInstitute of Ecology and EvolutionMoscowRussia
  2. 2.Institute of ZoologyDarmstadt University of TechnologyDarmstadtGermany

Personalised recommendations