Skip to main content
Log in

Ericaceous dwarf shrubs affect ectomycorrhizal fungal community of the invasive Pinus strobus and native Pinus sylvestris in a pot experiment

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

This study aimed to elucidate the relationship between ericaceous understorey shrubs and the diversity and abundance of ectomycorrhizal fungi (EcMF) associated with the invasive Pinus strobus and native Pinus sylvestris. Seedlings of both pines were grown in mesocosms and subjected to three treatments simulating different forest microhabitats: (a) grown in isolation and grown with (b) Vaccinium myrtillus or (c) Vaccinium vitis-idaea. Ericaceous plants did not act as a species pool of pine mycobionts and inhibited the ability of the potentially shared species Meliniomyces bicolor to form ectomycorrhizae. Similarly, Ericaceae significantly reduced the formation of Thelephora terrestris ectomycorrhizae in P. sylvestris. EcMF species composition in the mesocosms was strongly affected by both the host species and the presence of an ericaceous neighbour. When grown in isolation, P. strobus root tips were predominantly colonised by Wilcoxina mikolae, whereas those of P. sylvestris were more commonly colonised by Suillus and Rhizopogon spp. Interestingly, these differences were less evident (Suillus + Rhizopogon spp.) or absent (W. mikolae) when the pines were grown with Ericaceae. P. strobus exclusively associated with Rhizopogon salebrosus s.l., suggesting the presence of host specificity at the intrageneric level. Ericaceous plants had a positive effect on colonisation of P. strobus root tips by R. salebrosus s.l. This study demonstrates that the interaction of selective factors such as host species and presence of ericaceous plants may affect the realised niche of the ectomycorrhizal fungi.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abarenkov K, Nilsson RH, Larsson KH, Alexander IJ, Eberhardt U, Erland S, Hoiland K, Kjøller R, Larsson E, Pennanen T, Sen R, Taylor AFS, Tedersoo L, Ursing BM, Vrålstad T, Liimatainen K, Peintner U, Koljalg U (2010) The UNITE database for molecular identification of fungi—recent updates and future perspectives. New Phytol 186:281–285

    Article  PubMed  Google Scholar 

  • Baxter JW, Dighton J (2001) Ectomycorrhizal diversity alters growth and nutrient acquisition of grey birch (Betula populifolia) seedlings in host–symbiont culture conditions. New Phytol 152:139–149

    Article  Google Scholar 

  • Bruns TD, Peay KG, Boynton PJ, Grubisha LC, Hynson NA, Nguyen NH, Rosenstock NP (2009) Inoculum potential of Rhizopogon spores increases with time over the first 4 yr of a 99-yr spore burial experiment. New Phytol 181:463–470

    Article  PubMed  Google Scholar 

  • Carrillo-Gavilan MA, Vila M (2010) Little evidence of invasion by alien conifers in Europe. Divers Distrib 16:203–213

    Article  Google Scholar 

  • Collier FA, Bidartondo MI (2009) Waiting for fungi: the ectomycorrhizal invasion of lowland heathlands. J Ecol 97:950–963

    Article  Google Scholar 

  • Courty PE, Pritsch K, Schloter M, Hartmann A, Garbaye J (2005) Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytol 167:309–319

    Article  CAS  PubMed  Google Scholar 

  • Curlevski NJA, Chambers SM, Anderson IC, Cairney JWG (2009) Identical genotypes of an ericoid mycorrhiza-forming fungus occur in roots of Epacris pulchella (Ericaceae) and Leptospermum polygalifolium (Myrtaceae) in an Australian sclerophyll forest. FEMS Microbiol Ecol 67:411–420

    Article  CAS  PubMed  Google Scholar 

  • Dickie IA, Bolstridge N, Cooper JA, Peltzer DA (2010) Co-invasion by Pinus and its mycorrhizal fungi. New Phytol 187:475–484

    Article  PubMed  Google Scholar 

  • Gardes M, Bruns TD (1993) Its primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Genney DR, Alexander IJ, Hartley SE (2000) Exclusion of grass roots from soil organic layers by Calluna: the role of ericoid mycorrhizas. J Exp Bot 51:1117–1125

    Article  CAS  PubMed  Google Scholar 

  • Genney DR, Anderson IC, Alexander IJ (2006) Fine-scale distribution of pine ectomycorrhizas and their extramatrical mycelium. New Phytol 170:381–390

    Article  PubMed  Google Scholar 

  • Grelet GA, Johnson D, Paterson E, Anderson IC, Alexander IJ (2009) Reciprocal carbon and nitrogen transfer between an ericaceous dwarf shrub and fungi isolated from Piceirhiza bicolorata ectomycorrhizas. New Phytol 182:359–366

    Article  CAS  PubMed  Google Scholar 

  • Hadincová V, Köhnleinová I, Marešová J (2007) Invasive behaviour of white pine (Pinus strobus L.) in sandstone areas in the Czech Republic. In: Härtel H, Cílek V, Herben T, Jackson A, Williams R (eds) Sandstones Landscapes. Academia, Prague, pp 219–224

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hambleton S, Sigler L (2005) Meliniomyces, anew anamorph genus for root-associated fungi with phylogenetic affinities to Rhizoscyphus ericae (Hymenoscyphus ericae), Leotiomycetes. Stud Mycol 53:1–27

    Article  Google Scholar 

  • Horton TR, Bruns TD, Parker VT (1999) Ectomycorrhizal fungi associated with Arctostaphylos contribute to Pseudotsuga menziesii establishment. Can J Bot 77:93–102

    Google Scholar 

  • Ishida TA, Nara K, Hogetsu T (2007) Host effects on ectomycorrhizal fungal communities: insight from eight host species in mixed conifer–broadleaf forests. New Phytol 174:430–440

    Article  CAS  PubMed  Google Scholar 

  • Iwanski M, Rudawska M, Leski T (2006) Mycorrhizal associations of nursery grown Scots pine (Pinus sylvestris L.) seedlings in Poland. Ann For Sci 63:715–723

    Article  Google Scholar 

  • Jacobson KM, Miller OK (1992) Physiological variation between tree associated populations of Suillus granulatus as determined by in vitro mycorrhizal synthesis experiments. Can J Bot 70:26–31

    Article  Google Scholar 

  • Jonsson LM, Nilsson MC, Wardle DA, Zackrisson O (2001) Context dependent effects of ectomycorrhizal species richness on tree seedling productivity. Oikos 93:353–364

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Kennedy PG, Peay KG, Bruns TD (2009) Root tip competition among ectomycorrhizal fungi: are priority effects a rule or an exception? Ecology 90:2098–2107

    Article  PubMed  Google Scholar 

  • Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301

    Article  Google Scholar 

  • Korkama T, Fritze H, Pakkanen A, Pennanen T (2007) Interactions between extraradical ectomycorrhizal mycelia, microbes associated with the mycelia and growth rate of Norway spruce (Picea abies) clones. New Phytol 173:798–807

    Article  CAS  PubMed  Google Scholar 

  • Krpata D, Muhlmann O, Kuhnert R, Ladurner H, Göbl F, Peintner U (2007) High diversity of ectomycorrhizal fungi associated with Arctostaphylos uva-ursi in subalpine and alpine zones: potential inoculum for afforestation. For Ecol Manag 250:167–175

    Article  Google Scholar 

  • Kubartová A (2007) Decomposition of needle litter in Pinus sylvestris and Pinus strobus forests in the Bohemian Switzerland National Park (Czech Republic). In: Härtel H, Cílek V, Herben T, Jackson A, Williams R (eds) Sandstones landscapes. Academia, Prague, pp 234–237

    Google Scholar 

  • Leski T, Aučina A, Skridaila A, Pietras M, Riepšas E, Rudawska M (2010) Ectomycorrhizal community structure of different genotypes of Scots pine under forest nursery conditions. Mycorrhiza 20:473–481

    Article  PubMed  Google Scholar 

  • Lilleskov EA, Fahey TJ, Horton TR, Lovett GM (2002) Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology 83:104–115

    Article  Google Scholar 

  • Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Mikola P (1969) Afforestation of treeless areas. Unasylva 23:S1–S20

    Google Scholar 

  • Molina R, Trappe JM (1994) Biology of the ectomycorrhizal genus, Rhizopogon. 1. Host associations, host-specificity and pure culture syntheses. New Phytol 126:653–675

    Article  Google Scholar 

  • Morris MH, Smith ME, Rizzo DM, Rejmánek M, Bledsoe CS (2008) Contrasting ectomycorrhizal fungal communities on the roots of co-occurring oaks (Quercus spp.) in a California woodland. New Phytol 178:167–176

    Article  PubMed  Google Scholar 

  • Morris MH, Perez-Perez MA, Smith ME, Bledsoe CS (2009) Influence of host species on ectomycorrhizal communities associated with two co-occurring oaks (Quercus spp.) in a tropical cloud forest. FEMS Microbiol Ecol 69:274–287

    Article  CAS  PubMed  Google Scholar 

  • Nilsson MC, Hogberg P, Zackrisson O, Wang FY (1993) Allelopathic effects by Empetrum hermaphroditum on development and nitrogen uptake by roots and mycorrhizae of Pinus silvestris. Can J Bot 71:620–628

    Article  Google Scholar 

  • Nožička J (1965) Zavádění vejmutovky v čEeských zemích do r. 1938 (White pine introduction into the Czech countries up to year 1938). Práce výzkumného ústavu lesnického čESSR 31:41–67

    Google Scholar 

  • Nuñez MA, Horton TR, Simberloff D (2009) Lack of belowground mutualisms hinders Pinaceae invasions. Ecology 90:2352–2359

    Article  PubMed  Google Scholar 

  • Pickles BJ, Genney DR, Potts JM, Lennon JJ, Anderson IC, Alexander IJ (2010) Spatial and temporal ecology of Scots pine ectomycorrhizas. New Phytol 186:755–768

    Article  CAS  PubMed  Google Scholar 

  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  • Pringle A, Bever JD, Gardes M, Parrent JL, Rillig MC, Klironomos JN (2009) Mycorrhizal symbioses and plant invasions. Annu Rev Ecol Evol S 40:699–715

    Article  Google Scholar 

  • R Core Development Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391

    Article  Google Scholar 

  • Read DJ (1998) The mycorrhizal status of pines. In: Richardson DM (ed) Ecology and biogeography of Pinus. Cambridge University Press, Cambridge, pp 324–340

    Google Scholar 

  • Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457

    Article  PubMed  Google Scholar 

  • Rejmánek M (1989) Invasibility of plant communities. In: Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmánek M, Williamson M (eds) Biological invasions. A global perspective. SCOPE 37. Wiley, Chichester, pp 369–388

    Google Scholar 

  • Richard F, Selosse MA, Gardes M (2009) Facilitated establishment of Quercus ilex in shrub-dominated communities within a Mediterranean ecosystem: do mycorrhizal partners matter? FEMS Microbiol Ecol 68:14–24

    Article  CAS  PubMed  Google Scholar 

  • Richardson DM, Allsopp N, D’Antonio CM, Milton SJ, Rejmánek M (2000) Plant invasions—the role of mutualisms. Biol Rev 75:65–93

    Article  CAS  PubMed  Google Scholar 

  • Rusca TA, Kennedy PG, Bruns TD (2006) The effect of different pine hosts on the sampling of Rhizopogon spore banks in five Eastern Sierra Nevada forests. New Phytol 170:551–560

    Article  CAS  PubMed  Google Scholar 

  • Selosse MA, Richard F, He XH, Simard SW (2006) Mycorrhizal networks: des liaisons dangereuses? Trends Ecol Evol 21:621–628

    Article  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Elsevier, Amsterdam

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Tedersoo L, Suvi T, Beaver K, Koljalg U (2007) Ectomycorrhizal fungi of the Seychelles: diversity patterns and host shifts from the native Vateriopsis seychellarum (Dipterocarpaceae) and Intsia bijuga (Caesalpiniaceae) to the introduced Eucalyptus robusta (Myrtaceae), but not Pinus caribea (Pinaceae). New Phytol 175:321–333

    Article  CAS  PubMed  Google Scholar 

  • Tedersoo L, Jairus T, Horton BM, Abarenkov K, Suvi T, Saar I, Koljalg U (2008a) Strong host preference of ectomycorrhizal fungi in a Tasmanian wet sclerophyll forest as revealed by DNA barcoding and taxon-specific primers. New Phytol 180:479–490

    Article  CAS  PubMed  Google Scholar 

  • Tedersoo L, Suvi T, Jairus T, Koljalg U (2008b) Forest microsite effects on community composition of ectomycorrhizal fungi on seedlings of Picea abies and Betula pendula. Environ Microbiol 10:1189–1201

    Article  CAS  PubMed  Google Scholar 

  • Tedersoo L, Partel K, Jairus T, Gates G, Poldmaa K, Tamm H (2009) Ascomycetes associated with ectomycorrhizas: molecular diversity and ecology with particular reference to the Helotiales. Environ Microbiol 11:3166–3178

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) Clustal-W—improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toljander JF, Eberhardt U, Toljander YK, Paul LR, Taylor AFS (2006) Species composition of an ectomycorrhizal fungal community along a local nutrient gradient in a boreal forest. New Phytol 170:873–883

    Article  CAS  PubMed  Google Scholar 

  • van der Heijden EW, Kuyper TW (2003) Ecological strategies of ectomycorrhizal fungi of Salix repens: root manipulation versus root replacement. Oikos 103:668–680

    Article  Google Scholar 

  • van der Putten WH, Klironomos JN, Wardle DA (2007) Microbial ecology of biological invasions. ISME J 1:28–37

    Article  PubMed  Google Scholar 

  • Villarreal-Ruiz L, Anderson IC, Alexander IJ (2004) Interaction between an isolate from the Hymenoscyphus ericae aggregate and roots of Pinus and Vaccinium. New Phytol 164:183–192

    Article  CAS  Google Scholar 

  • Vohník M, Fendrych M, Albrechtová J, Vosátka M (2007a) Intracellular colonisation of Rhododendron and Vaccinium roots by Cenococcum geophilum, Geomyces pannorum and Meliniomyces variabilis. Folia Microbiol 52:407–414

    Article  Google Scholar 

  • Vohník M, Fendrych M, Kolařík M, Gryndler M, Hršelová H, Albrechtová J, Vosátka M (2007b) The ascomycete Meliniomyces variabilis isolated from a sporocarp of Hydnotrya tulasnei (Pezizales) intracellularly colonises roots of ecto- and ericoid mycorrhizal host plants. Czech Mycol 59:215–226

    Google Scholar 

  • Vrålstad T (2004) Are ericoid and ectomycorrhizal fungi part of a common guild? New Phytol 164:7–10

    Article  Google Scholar 

  • Vrålstad T, Fossheim T, Schumacher T (2000) Piceirhiza bicolorata—the ectomycorrhizal expression of the Hymenoscyphus ericae aggregate? New Phytol 145:549–563

    Article  Google Scholar 

  • Vrålstad T, Schumacher T, Taylor AFS (2002) Mycorrhizal synthesis between fungal strains of the Hymenoscyphus ericae aggregate and potential ectomycorrhizal and ericoid hosts. New Phytol 153:143–152

    Article  Google Scholar 

  • Walbert K, Ramsfield TD, Ridgway HJ, Jones EE (2010) Ectomycorrhizal species associated with Pinus radiata in New Zealand including novel associations determined by molecular analysis. Mycorrhiza 20:209–215

    Article  CAS  PubMed  Google Scholar 

  • Walker JF, Miller OK, Lei T, Semones S, Nilsen E, Clinton BD (1999) Suppression of ectomycorrhizae on canopy tree seedlings in Rhododendron maximum L.-(Ericaceae) thickets in the southern Appalachians. Mycorrhiza 9:49–56

    Article  Google Scholar 

  • Walker JF, Miller OK, Horton JL (2005) Hyperdiversity of ectomycorrhizal fungus assemblages on oak seedlings in mixed forests in the southern Appalachian Mountains. Mol Ecol 14:829–838

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis N, Gelfand D, Sninsky J, White T (eds) PCR—protocols and applications—a laboratory manual. Academic, New York, pp 315–322

    Google Scholar 

Download references

Acknowledgements

We acknowledge Petra Wildová for excellent lab assistance, Kateřina Štajerová for suggestions that improved the manuscript and Tony Dixon for language correction. We would like to thank two anonymous reviewers for their highly valuable comments on our manuscript. Grant Agency of Charles University (9714/2009), COST OC 10058 (Ministry of Education, Youth and Sports of the Czech Republic) and Charles University SVV 261209/2010 provided financial support. This study is a part of the Academy of Sciences of the Czech Republic research programme AV0Z60050516.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Petr Kohout.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material S1

Numbers of EcM root tips colonised by different morphotypes in each pot. Each row represents a single pot. Sy Pinus sylvestris grown in isolation, SyVm P. sylvestris gown with Vaccinium myrtillus, SyVv P. sylvestris grown with V. vitis-idaea, St P. strobus grown in isolation, StVm P. strobus grown with V. myrtillus, StVv P. strobus grown with V. vitis-idaea, nm non-mycorrhizal. (PDF 36 kb)

Supplementary material S2

Numbers of sequences obtained from all suilloid EcM fungi in each pot. Each row represents a single pot. Sy Pinus sylvestris grown in isolation, SyVm P. sylvestris grown with Vaccinium myrtillus, SyVv P. sylvestris grown with V. vitis-idaea, St P. strobus grown in isolation, StVm P. strobus grown with V. myrtillus, StVv P. strobus grown with V. vitis-idaea. EcM fungi: SBO Suillus bovinus, SVA S. variegatus, SGR1 S. granulatus 1, SGR2 S. granulatus 2, SLU S. luteus, RRO Rhizopogon roseolus s.l., RLU R. luteolus, RSA R. salebrosus s.l. (PDF 37 kb)

Supplementary material S3

Phylogenetic tree of part of Rhizoscyphus ericae aggregate based on a neighbour-joining analysis of 470 characters of ITS1, 5,8S rDNA and part of the ITS2 sequences. Numbers above branches denote neighbour-joining bootstrap values from 1,000 replications. The tree was rooted using sequences of Hymenoscyphus fructigenus and Anguillospora crassa. Sequences obtained in the present study are shown in bold. They are labelled with the database accession number, the host plant species from which they were obtained and the cultivation treatment (Sy Pinus sylvestris grown in isolation, SyVm P. sylvestris gown with Vaccinium myrtillus, St P. strobus grown in isolation). The parentheses show the delimitation of the fungal taxa. (PDF 223 kb)

Supplementary material S4

Phylogenetic tree of part of Rhizopogon salebrosus s.l. based on a neighbour-joining analysis of 503 characters of ITS1, 5,8S rDNA and part of the ITS2 sequences. Numbers denote neighbour-joining bootstrap values from 1,000 replications. The tree was rooted using sequence of Rhizopogon roseolus. Sequences obtained in the present study are shown in bold. R. salebrosus fruit bodies’ sequences obtained from the EMBL database are labelled with the database accession number and country of origin; EMBL database sequences originating from root tips are labelled in addition with the host plant species. (PDF 256 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kohout, P., Sýkorová, Z., Bahram, M. et al. Ericaceous dwarf shrubs affect ectomycorrhizal fungal community of the invasive Pinus strobus and native Pinus sylvestris in a pot experiment. Mycorrhiza 21, 403–412 (2011). https://doi.org/10.1007/s00572-010-0350-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-010-0350-2

Keywords

Navigation