Skip to main content
Log in

Quercus rubra-associated ectomycorrhizal fungal communities of disturbed urban sites and mature forests

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

Abstract

The presence and quality of the belowground mycorrhizal fungal community could greatly influence plant community structure and host species response. This study tests whether mycorrhizal fungal communities in areas highly impacted by anthropogenic disturbance and urbanization are less species rich or exhibit lower host root colonization rates when compared to those of less disturbed systems. Using a soil bioassay, we sampled the ectomycorrhizal fungal (EMF) communities associating with Quercus rubra (northern red oak) seedlings in soil collected from seven sites: two mature forest reference sites and five urban sites of varying levels of disturbance. Morphological and polymerase chain reaction–restriction fragment length polymorphism analyses of fungi colonizing root tips revealed that colonization rates and fungal species richness were significantly lower on root systems of seedlings grown in disturbed site soils. Analysis of similarity showed that EMF community composition was not significantly different among several urban site soils but did differ significantly between mature forest sites and all but one urban site. We identified a suite of fungal species that occurred across several urban sites. Lack of a diverse community of belowground mutualists could be a constraint on urban plant community development, especially of late-successional woodlands. Analysis of urban EMF communities can add to our understanding of urban plant community structure and should be addressed during ecological assessment before pragmatic decisions to restore habitats are framed.

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
Fig. 4

Similar content being viewed by others

References

  • Agerer R (1987–1996) Colour atlas of Ectomycorrhizae. Eichhorn-Verlag Eduard Dietenberger, Schwäbisch Gmünd

    Google Scholar 

  • Allen EB, Allen MF, Egerton-Warburton L, Corkidi L, Gomez-Pompa A (2003) Impacts of early- and late-seral mycorrhizae during restoration in seasonal tropical forest, Mexico. Ecol Appl 13:1701–1717

    Article  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Ashkannejhad S, Horton TR (2006) Ectomycorrhizal ecology under primary succession on coastal sand dunes: interactions involving Pinus contorta, suilloid fungi and deer. New Phytol 169:345–354

    Article  PubMed  Google Scholar 

  • Avis PG, Charvat I (2005) The response of ectomycorrhizal fungal inoculum to long-term increases in nitrogen supply. Mycologia 97:329–337

    Article  PubMed  Google Scholar 

  • Bainard LD, Klironomos JN, Gordon AM (2011) The mycorrhizal status and colonization of 26 tree species growing in urban and rural environments. Mycorrhiza 21:91–96

    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 152:139–159

    Article  Google Scholar 

  • Baxter JW, Dighton J (2005) Diversity–functioning relationships in ectomycorrhizal fungal communities. In: Dighton J, White JF, Oudemans P (eds) The fungal community. Its role and organization in the ecosystem. Taylor and Francis Group, Boca Raton, pp 383–398

    Google Scholar 

  • Baxter J, Pickett STA, Carreiro MM, Dighton J (1999) Ectomycorrhizal diversity and community structure in oak forest stands exposed to contrasting anthropogenic impacts. Can J Bot 77:771–782

    Google Scholar 

  • Boerner RE, DeMars JBG, Leicht PN (1996) Spatial patterns of mycorrhizal infectiveness of soils long a successional chronosequence. Mycorrhiza 6:79–90

    Article  Google Scholar 

  • Byrd KB, Parker VT, Vogler DR, Cullings KW (2000) The influence of clear-cutting on ectomycorrhizal fungus diversity in a lodgepole pine (Pinus contorta) stand, Yellowstone National Park, Wyoming, and Gallatin National Forest, Montana. Can J Bot 78:149–156

    Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth

    Google Scholar 

  • Collins BR, Anderson KH (1994) Plant communities of New Jersey: a study in landscape diversity. Rutgers University Press, New Brunswick

    Google Scholar 

  • Cousins JR, Hope D, Gries C, Stutz JC (2003) Preliminary assessment of arbuscular mycorrhizal fungal diversity and community structure in an urban ecosystem. Mycorrhiza 13:319–326

    Article  PubMed  Google Scholar 

  • Cripps CL (2003) Native mycorrhizal fungi with aspen on smelter-impacted sites in the northern Rocky Mountains: occurrence and potential use in reclamation. National Meeting of the American Society of Mining and Reclamation and the 9th Billing Land Reclamation Symposium, Billings, Montana. ASMR, Lexington

  • Danielson RM (1984) Ectomycorrhizal association in jack pine stands in northeastern Alberta. Can J Bot 62:932–939

    Article  Google Scholar 

  • Del Tredici P (2010) Wild urban plants of the northeast: a field guide. Cornell University Press, Ithaca

    Google Scholar 

  • Dickie IA, Reich PB (2005) Ectomycorrhizal fungal communities at forest edges. J Ecol 93:244–255

    Article  Google Scholar 

  • Dickie IA, Koide RT, Fayish AC (2001) Vesicular–arbuscular mycorrhizal infection of Quercus rubra seedlings. New Phytol 151:257–264

    Article  Google Scholar 

  • Dickie IA, Schnitzer SA, Reich PB, Hobbie CE (2005) Spatially disjunct effects of co-occurring competition and facilitation. Ecol Lett 8:1191–1200

    Article  PubMed  Google Scholar 

  • Dighton J, Mason PA (1985) Mycorrhizal dynamics during forest tree Development. In: Moore D, Casselton LA, Wood DA, Frankland JC (eds) Developmental biology of higher fungi. Cambridge University Press, Cambridge, pp 117–139

    Google Scholar 

  • Ditchkoff SS, Saalfeld ST, Gibson CJ (2006) Animal behavior in urban ecosystems: modifications due to human-induced stress. Urban Ecosyst 9:5–12

    Article  Google Scholar 

  • Eviner VT, Hawkes CV (2008) Embracing variability in the application of plant–soil interactions to the restoration of communities and ecosystems. Restor Ecol 16:713–729

    Article  Google Scholar 

  • Fleming LV (1983) Succession of mycorrhizal fungi on birch: infection of seedlings planted around mature trees. Plant Soil 71:263–267

    Article  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  PubMed  CAS  Google Scholar 

  • Horton TR, Bruns TD (1998) Multiple-host fungi are the most frequent and abundant ectomycorrhizal types in a mixed stand of Douglas fir (Pseudotsuga menziesii) and bishop pine (Pinus muricata). New Phytol 139:331–339

    Article  Google Scholar 

  • Horton TR, Bruns TD (2001) The molecular revolution in ectomycorrhizal ecology: peeking into the molecular black-box. Mol Ecol 10:1855–1871

    Article  PubMed  CAS  Google Scholar 

  • Horton TR, van der Heijden M (2008) The role of symbioses in seedling establishment and survival. In: Leck MA, Parker VT, Simpson RL (eds) Seedling ecology and evolution. Cambridge University Press, Cambridge, pp 189–213

    Google Scholar 

  • Jones MD, Durall DM, Cairney JWG (2003) Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging. New Phytol 157:399–422

    Article  Google Scholar 

  • Jumpponen A, Egerton-Warburton LM (2005) Mycorrhizal fungi in successional environments: a community assembly model incorporating host plant, environmental, and biotic filters. In: Dighton J, White FJ, Oudemans P (eds) The fungal community. Its role and organization in the ecosystem. Taylor and Francis Group, Boca Raton, pp 139–168

    Google Scholar 

  • Keizer PJ, Arnolds E (1994) Succession of ectomycorrhizal fungi in roadside verges planted with common oak (Quercus robur L.) in Drenthe, The Netherlands. Mycorrhiza 4:147–159

    Article  Google Scholar 

  • Kranabetter JM, Frieson J (2002) Ectomycorrhizal community structure on western hemlock (Tsuga heterophylla) seedlings transplanted from forests into openings. Can J Bot 80:861–868

    Article  Google Scholar 

  • Lilleskov EA, Bruns TD (2001) Nitrogen and ectomycorrhizal fungal communities: what we know, what we need to know. New Phytol 149:156–158

    Article  Google Scholar 

  • Lilleskov EA, Bruns TD (2005) Spore dispersal of a resupinate ectomycorrhizal fungus, Tomentella sublilacina, via soil food webs. Mycologia 97:762–769

    Article  PubMed  Google Scholar 

  • Lilleskov EA, Fahey TJ, Lovett GM (2001) Ectomycorrhizal fungal aboveground community change over an atmospheric nitrogen deposition gradient. Ecol Appl 11:397–410

    Article  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 

  • LoBuglio KF (1999) Cenococcum. In: Cairney JWG, Chambers SM (eds) Ectomycorrhizal fungi: key genera in profile. Springer, Berlin, pp 287–309

    Google Scholar 

  • Lundholm JT, Marlin A (2006) Habitat origins and microhabitat preferences of urban plant species. Urban Ecosyst 9:139–159

    Article  Google Scholar 

  • McDonnell MJ, Pickett STA, Groffman P, Bohlen P, Parmelee RW, Carreiro MM, Medley K (1997) Ecosystem processes along an urban-to-rural gradient. Urban Ecosyst 1:21–36

    Article  Google Scholar 

  • Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbiosis: community-ecological consequences and practical implications. In: Allen MF (ed) Mycorrhizal functioning. An integrative plant–fungal process. Chapman and Hall, New York, pp 357–423

    Google Scholar 

  • Neil K, Wu J (2006) Effects of urbanization on plant flowering phenology: a review. Urban Ecosyst 9:243–257

    Article  Google Scholar 

  • Newbound M, Mccarthy MA, Lebel T (2010) Fungi and the urban environment: a review. Landsc Urban Plan 96:138–145

    Article  Google Scholar 

  • Newton AC, Pigott CD (1991) Mineral nutrition and mycorrhizal infection of seedling oak and birch. I. Nutrient uptake and the development of mycorrhizal infection during seedling establishment. New Phytol 117:37–44

    Article  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • O’Brien HE, Parrent JL, Jackson JA, Moncalvo J, Vilgalys R (2005) Fungal community analysis by large-scale sequencing of environmental samples. Appl Environ Microbiol 71:5544–5550

    Article  PubMed  Google Scholar 

  • Parsons WJ, Ehrenfeld JG, Handel SN (1998) Vertical growth and mycorrhizal infection of woody plant roots as potential limits to the restoration of woodlands on landfills. Restor Ecol 6:280–289

    Article  Google Scholar 

  • Pavao-Zuckerman MA (2008) The nature of urban soils and their role in ecological restoration in cities. Restor Ecol 16:642–649

    Article  Google Scholar 

  • Peay KG, Kennedy PG, Davies SJ, Tan S, Bruns TD (2010) Potential link between plant and fungal distributions in a dipterocarp rainsforest: community and phylogenetic structure of tropical ectomycorrhizal fungi across a plant and soil ecotone. New Phytol 185:529–542

    Article  PubMed  CAS  Google Scholar 

  • Peter M, Ayor F, Egli S (2001) Nitrogen addition in a Norway spruce stand altered macromycete sporocarp production and below-ground ectomycorrhizal species composition. New Phytol 149:211–325

    Article  Google Scholar 

  • Read DJ, Birch CPD (1987) The effects and implications of disturbance of mycorrhizal mycelial systems. Proc R Soc Edinb 94B:13–24

    Google Scholar 

  • Robinson L, Newell JP, Marzluff JM (2005) Twenty-five years of sprawl in the Seattle region: growth management responses and implications for conservation. Landsc Urban Plan 71:51–72

    Article  Google Scholar 

  • Sadik N (1999) The state of world population 1999–6 billion: a time for choices. United Nations Population Fund, New York

    Google Scholar 

  • Sanderson EW (2009) Mannahatta: a natural history of New York City. Abrams, New York

    Google Scholar 

  • Shaw CG, Sidle RC (1982) Evaluation of planting sites common to a southeast Alaska clear-cut. II. Available inoculum of the ectomycorrhizal fungus Cenococcum geophilum. Can J For Res 13:9–11

    Article  Google Scholar 

  • Taylor AFS (2002) Fungal diversity in ectomycorrhizal communities: sampling effort and species detection. Plant Soil 244:19–28

    Article  CAS  Google Scholar 

  • Taylor DL, Bruns TD (1999) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: minimal overlap between the mature forest and resistant propagule communities. Mol Ecol 8:1837–1850

    Article  PubMed  CAS  Google Scholar 

  • Trappe JM (1964) Mycorrhizal hosts and distribution of Cenococcum graniforme. Lloydia 27:100–106

    Google Scholar 

  • USDA NRCS (2007) The PLANTS Database. National Plant Data Center. http://plants.usda.gov. Accessed 16 Dec 2007

  • van der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97:1139–1150

    Article  Google Scholar 

  • Wallenda T, Kottke I (1998) Nitrogen deposition and ectomycorrhizas. New Phytol 139:169–187

    Article  CAS  Google Scholar 

  • Weiher E (2007) On the status of restoration science: obstacles and opportunities. Restor Ecol 15:340–343

    Article  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

Acknowledgments

This research was made possible by funding from the Doris Duke Charitable Foundation and the New Jersey Mycological Association. Thank you to Lena Struwe, Jean Molina, and Sasha Eisenman for access to lab space and procedural advice. We appreciate Peter Morin’s input on statistical analyses. Thank you to Duke Farms, Helyar Woods, Greenbelt Native Plant Center, and the US EPA Edison facility for site access. Discussions with Blake Mathys, Victor Medore, Carrie Norin, and Elena Tartaglia were very helpful. Comments and suggestions from two anonymous reviewers greatly improved this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Amy S. Karpati.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Karpati, A.S., Handel, S.N., Dighton, J. et al. Quercus rubra-associated ectomycorrhizal fungal communities of disturbed urban sites and mature forests. Mycorrhiza 21, 537–547 (2011). https://doi.org/10.1007/s00572-011-0362-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-011-0362-6

Keywords

Navigation