Skip to main content

Advertisement

SpringerLink
Log in

Host and habitat filtering in seedling root-associated fungal communities: taxonomic and functional diversity are altered in ‘novel’ soils

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

Abstract

Climatic and land use changes have significant consequences for the distribution of tree species, both through natural dispersal processes and following management prescriptions. Responses to these changes will be expressed most strongly in seedlings near current species range boundaries. In northern temperate forest ecosystems, where changes are already being observed, ectomycorrhizal fungi contribute significantly to successful tree establishment. We hypothesised that communities of fungal symbionts might therefore play a role in facilitating, or limiting, host seedling range expansion. To test this hypothesis, ectomycorrhizal communities of interior Douglas-fir and interior lodgepole pine seedlings were analysed in a common greenhouse environment following growth in five soils collected along an ecosystem gradient. Currently, Douglas-fir’s natural distribution encompasses three of the five soils, whereas lodgepole pine’s extends much further north. Host filtering was evident amongst the 29 fungal species encountered: 7 were shared, 9 exclusive to Douglas-fir and 13 exclusive to lodgepole pine. Seedlings of both host species formed symbioses with each soil fungal community, thus Douglas-fir did so even where those soils came from outside its current distribution. However, these latter communities displayed significant taxonomic and functional differences to those found within the host distribution, indicative of habitat filtering. In contrast, lodgepole pine fungal communities displayed high functional similarity across the soil gradient. Taxonomic and/or functional shifts in Douglas-fir fungal communities may prove ecologically significant during the predicted northward migration of this species; especially in combination with changes in climate and management operations, such as seed transfer across geographical regions for forestry purposes.

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

  • Addy HD, Piercey MM, Currah RS (2005) Microfungal endophytes in roots. Can J Bot 83:1–13

    Article  Google Scholar 

  • Agerer R (2001) Exploration types of ectomycorrhizae. Mycorrhiza 11:107–114

    Article  Google Scholar 

  • Aitken SN, Yeaman S, Holliday JA, Wang T, Curtis-McLane S (2008) Adaptation, migration or extirpation: climate change outcomes for tree populations. Evol Appl 1:95–111

    Article  PubMed Central  PubMed  Google Scholar 

  • Alexander I, Ahmad N, Su See L (1992) The role of mycorrhizas in the regeneration of some Malaysian forest trees. Philos T Roy Soc B 335:379–388

    Article  Google Scholar 

  • Bingham MA, Simard SW (2011) Do mycorrhizal network benefits to survival and growth of interior Douglas-fir seedlings increase with soil moisture stress? Ecol Evol 1:306–316

    Article  PubMed Central  PubMed  Google Scholar 

  • Bogar LM, Kennedy PG (2013) New wrinkles in an old paradigm: neighborhood effects can modify the structure and specificity of Alnus-associated ectomycorrhizal fungal communities. FEMS Microbiol Ecol 83:767–777

    Article  CAS  PubMed  Google Scholar 

  • Bruns TD, Bidartondo MI, Taylor DL (2002) Host specificity in ectomycorrhizal communities: what do the exceptions tell us? Integr Comp Biol 42:352–359

    Article  PubMed  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 

  • Coops NC, Waring RH (2011) A process-based approach to estimate lodgepole pine (Pinus contorta Dougl.) distribution in the Pacific Northwest under climate change. Clim Change 105:313–328

    Article  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. URL http://www.R-project.org/

  • Diamond JM (1975) Assembly of species communities. In: Cody ML, Diamond JM (eds) Ecology and evolution of communities. Harvard University Press, Cambridge, pp 342–444

    Google Scholar 

  • Dormann CF (2007) Promising the future? Global change projections of species distributions. Basic Appl Ecol 8:387–397

    Article  Google Scholar 

  • Elias SA (2013) The problem of conifer species migration lag in the Pacific Northwest region since the last glaciation. Quat Sci Rev 77:55–69

    Article  Google Scholar 

  • Elmqvist T, Folke C, Nyström M, Peterson G, Bengtsson J, Walker B, Norberg J (2003) Response diversity, ecosystem change, and resilience. Front Ecol Environ 1:488–494

    Article  Google Scholar 

  • Fernando AA, Currah RS (1996) A comparative study of the effects of the root endophytes Leptodontidium orchidicola and Phialocephala fortinii (Fungi Imperfecti) on the growth of some subalpine plants in culture. Can J Bot 74:1071–1078

    Article  Google Scholar 

  • Gotelli NJ, Entsminger GL (2009) EcoSim: Null models software for ecology. Version 7. Acquired Intelligence Inc. & Kesey-Bear. Jericho, VT 05465. URL: http://garyentsminger.com/ecosim.htm

  • Griesbauer HP, Green DS (2010) Assessing the climatic sensitivity of Douglas-fir at its northern range margins in British Columbia, Canada. Trees 24:375–389

    Article  Google Scholar 

  • Gundale MJ, Kardol P, Nilsson M-C, Nilsson U, Lucas RW, Wardle DA (2014) Interactions with soil biota shift from negative to positive when a tree species is moved outside of its native range. New Phytol. doi:10.1111/nph.12699

    PubMed  Google Scholar 

  • Hamann A, Wang TL (2005) Models of climatic normals for genecology and climate change studies in British Columbia. Agr Forest Meteorol 128:211–221

    Article  Google Scholar 

  • Hamann A, Wang TL (2006) Potential effects of climate change on ecosystem and tree species distribution in British Columbia. Ecology 87:2773–2786

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Hoeksema JD, Hernandez JV, Rogers DL, Mendoza LL, Thompson JN (2012) Geographic divergence in a species-rich symbiosis: interactions between Monterey pines and ectomycorrhizal fungi. Ecology 93:2274–2285

    Article  PubMed  Google Scholar 

  • IPCC (2013) Climate change 2013: the physical science basis. In: Stocker TF, Qin D, Plattner G-K et al (eds) Contribution of working group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

    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 

  • Iverson LR, Schwartz MW, Prasad AM (2004) How fast and how far might tree species migrate in the eastern United States due to climate change? Glob Ecol Biogeogr 13:209–219

    Article  Google Scholar 

  • Ji B, Gehring CA, Wilson GW, Miller RM, Flores-Rentería JNC (2013) Patterns of diversity and adaptation in Glomeromycota from three prairie grasslands. Mol Ecol 22:2573–2587

    Article  CAS  PubMed  Google Scholar 

  • Johnson MT, Stinchcombe JR (2007) An emerging synthesis between community ecology and evolutionary biology. Trends Ecol Evol 22(5):250–257

  • Johnson NC, Wilson GWT, Bowker MA, Wilson JA, Miller RM (2010) Resource limitation is a driver of local adaptation in mycorrhizal symbioses. Proc Natl Acad Sci U S A 107:2093–2098

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karst J, Jones MD, Turkington R (2009) Ectomycorrhizal colonization and intraspecific variation in growth responses of lodgepole pine. Plant Ecol 200:161–165

    Article  Google Scholar 

  • Kennedy PG, Peay K, 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 

  • Kõljalg U, Nilsson RH, Abarenkov K et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277

    Article  PubMed  Google Scholar 

  • Kolotelo D, van Steenis E, Peterson M, Bennett R, Trotter D, Dennis J (2001) Seed handling guidebook. British Columbia Ministry of Forests. Tree Improvement Branch, Victoria

    Google Scholar 

  • Kranabetter JM, Stoehr MU, O’Neill GA (2012) Divergence in ectomycorrhizal communities with foreign Douglas-fir populations and implications for assisted migration. Ecol Appl 22:550–560

    Article  CAS  PubMed  Google Scholar 

  • Liimatainen K, Niskanen T, Dima B, Kytövuori I, Ammirati JF, Frøslev TG (2014) The largest type study of Agaricales species to date: bringing identification and nomenclature of Phlegmacium (Cortinarius) into the DNA era. Persoonia - Mol Phylogeny Evol Fungi 33:98–140

    Article  CAS  Google Scholar 

  • Lim S, Berbee ML (2013) Phylogenetic structure of ectomycorrhizal fungal communities of western hemlock changes with forest age and stand type. Mycorrhiza 23:473–486

    Article  PubMed  Google Scholar 

  • Little EL (1978) Atlas of United States trees, volume 5, U.S. Department of Agriculture Miscellaneous Publication 1361, Florida

    Google Scholar 

  • Jull MJ (1999) Douglas-fir silviculture “on the edge”: silvicultural systems at the northern range of the species. In: Lousier JD, Kessler WB (eds) Ecology and management of interior Douglas-fir (Pseudotsuga menziesii var. glauca) at the northern extreme of its range. Proceedings of a workshop held 7–9 October 1996 in Fort St. James, British Columbia. University of Northern British Columbia, Prince George, pp 34-44

  • Mandyam K, Jumpponen A (2005) Seeking the elusive function of the root-colonising dark septate endophytic fungi. Stud Mycol 53:173–189

    Article  Google Scholar 

  • Martin KJ, Rygiewicz PT (2005) Fungal specific PCR primers developed for analysis of the ITS region of environmental DNA extracts. BMC Microbiol 5:28

    Article  PubMed Central  PubMed  Google Scholar 

  • Marx DH, Ruehle JL, Kenney DS, Cordell CE, Riffle JW, Molina RJ, Pawuk WH, Navratil S, Tinus RW, Goodwin OC (1982) Commercial vegetative inoculum of Pisolithus tinctorius and inoculation techniques for development of ectomycorrhizae on container-grown tree seedlings. For Sci 28:373–400

    Google Scholar 

  • Massicotte HB, Trappe JM, Peterson RL, Melville LH (1992) Studies on Cenococcum geophilum. II. Sclerotium morphology, germination, and formation in pure culture and growth pouches. Can J Bot 70:125–132

    Article  Google Scholar 

  • Massicotte HB, Molina R, Tackaberry LE, Smith JE, Amaranthus MP (1999) Diversity and host specificity of ectomycorrhizal fungi retrieved from three adjacent forest sites by five host species. C J Bot 77:1053–1076

    Google Scholar 

  • Mayerhofer MS, Kernaghan G, Harper KA (2013) The effects of fungal root endophytes on plant growth: a meta-analysis. Mycorrhiza 23:119–128

    Article  PubMed  Google Scholar 

  • Mikola P (1970) Mycorrhizal inoculation in afforestation. Int Rev For Res 3:123–196

    Article  Google Scholar 

  • Nara K (2009) Spores of ectomycorrhizal fungi: ecological strategies for germination and dormancy. New Phytol 181:245–248

    Article  PubMed  Google Scholar 

  • Newsham KK (2011) A meta-analysis of plant responses to dark septate root endophytes. New Phytol 190:783–793

    Article  CAS  PubMed  Google Scholar 

  • Newsham KK, Upson R, Read DJ (2009) Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecol 2:10–20

    Article  Google Scholar 

  • Nguyen NH, Hynson NA, Bruns TD (2012) Stayin’ alive: survival of mycorrhizal fungal propagules from a 6-yr-old forest soil. Fungal Ecol 5:741–746

    Article  Google Scholar 

  • Nilsson RH, Hyde KD, Pawlowska J et al (2014) Improving ITS sequence data for identification of plant pathogenic fungi. Fungal Divers 67:11–19

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013). Vegan: community ecology package. R package version 2.0-10. http://CRAN.R-project.org/package=vegan

  • Peay KG, Schubert MG, Nguyen NH, Bruns TD (2012) Measuring ectomycorrhizal fungal dispersal: macroecological patterns driven by microscopic propagules. Mol Ecol 21:4122–4136

    Article  PubMed  Google Scholar 

  • Pedlar JH, McKenney DW, Aubin I, Beardmore T, Beaulieu J, Iverson L, O'Neill GA, Winder RS, Ste-Marie C (2012) Placing forestry in the assisted migration debate. Biosci 62:835–842

    Article  Google Scholar 

  • Peterson RL, Bradbury SM (1999) Use of plant mutants, intraspecific variants, and non-hosts in studying mycorrhiza formation and function. In: Varma A, Hock B (eds) Mycorrhiza, 2nd edn. Springer, Berlin, pp 153–176

    Chapter  Google Scholar 

  • Pickles BJ, Egger KN, Massicotte HB, Green DS (2012) Ectomycorrhizas and climate change. Fungal Ecol 5:73–84

    Article  Google Scholar 

  • Pojar J, Klinka K, Meidinger DV (1987) Biogeoclimatic ecosystem classification in British Columbia. For Ecol Manag 22:119–154

    Article  Google Scholar 

  • Rehfeldt GE, Jaquish BC, Lopez-Upton J, Saenz-Romero C, St Clair JB, Leites LP, Joyce DG (2014) Comparative genetic responses to climate for the varieties of Pinus ponderosa and Pseudotsuga menziesii: Realized climate niches. For Ecol Manag 324:126–137

    Article  Google Scholar 

  • Reithmeier L, Kernaghan G (2013) Availability of ectomycorrhizal fungi to black spruce above the present treeline in Eastern Labrador. PLoS One 8:e77527

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rineau F, Courty P-E (2011) Secreted enzymatic activities of ectomycorrhizal fungi as a case study of functional diversity and functional redundancy. Ann For Sci 68:69–80

    Article  Google Scholar 

  • Rosado SCS, Kropp BR, Piché Y (1994) Genetics of ectomycorrhizal symbiosis. I. Host plant variability and heritability of ectomycorrhizal and root traits. New Phytol 126:105–110

    Article  Google Scholar 

  • Roy M, Rochet J, Manzi S, Jargeat P, Gryta H, Moreau P-M, Gardes M (2013) What determines Alnus-associated ectomycorrhizal community diversity and specificity? A comparison of host and habitat effects at a regional scale. New Phytol 198:1228–1238

    Article  CAS  PubMed  Google Scholar 

  • Ruotsalainen AL, Kytöviita M-M (2004) Mycorrhiza does not alter low temperature impact of Gnaphalium norvegicum. Oecologia 140:226–233

    Article  PubMed  Google Scholar 

  • Simard SW (2009) The foundational role of mycorrhizal networks in self-organisation of interior Douglas-fir forests. For Ecol Manag 258S:S95eS107

    Google Scholar 

  • Simard SW, Beiler KJ, Bingham MA, Deslippe JR, Philip LJ, Teste FP (2012) Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol Rev 26:39–60

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, San Diego

    Google Scholar 

  • Smith ME, Douhan GW, Fremier AK, Rizzo DM (2009) Are true multihost fungi the exception or the rule? Dominant ectomycorrhizal fungi on Pinus sabiniana differ from those on co-occurring Quercus species. New Phytol 182:295–299

    Article  PubMed  Google Scholar 

  • Stone L, Roberts A (1990) The checkerboard score and species distributions. Oecologia 85:74–79

    Article  Google Scholar 

  • Tedersoo L, Pärtel K, Jairus T, Gates G, Põldmaa 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 K (2000) The functional ecology of soil seed banks. In: Fenner M (ed) Seeds the ecology of regeneration in plant communities. CABI Publishing, Wallingford, pp 215–235

    Chapter  Google Scholar 

  • Timling I, Dahlberg A, Walker DA, Gardes M, Charcosset JY, Welker JM, Taylor DL (2012) Distribution and drivers of ectomycorrhizal fungal communities across the North American Arctic. Ecosphere 3:111

    Article  Google Scholar 

  • Twieg BD, Durall DM, Simard SW (2007) Ectomycorrhizal fungal succession in mixed temperate forests. New Phytol 176:437–447

    Article  PubMed  Google Scholar 

  • Upson R, Read DJ, Newsham KK (2009) Nitrogen form influences the response of Deschampsia antarctica to dark septate root endophytes. Mycorrhiza 20:1–11

    Article  PubMed  Google Scholar 

  • Verhoeven KJF, Simonsen KL, McIntyre LM (2005) Implementing false discovery rate control: increasing your power. Oikos 108:643–647

    Article  Google Scholar 

  • Wang T, Hamann A, Spittlehouse D, Aitken SN (2006) Development of scale-free climate data for western Canada for use in resource management. Int J Climatol 26:383–397

    Article  Google Scholar 

  • Wang T, Campbell EM, O’Neill GA, Aitken SN (2012) Projecting future distributions of ecosystem climate niches: uncertainties and management applications. For Ecol Manag 279:128–140

    Article  Google Scholar 

  • Weiher E, Keddy PA (1999) Ecological assembly rules: perspectives, advances, retreats. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor J (1990) Analysis of phylogenetic relationships by amplification and direct sequencing of ribosomal RNA genes. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, New York, pp 315–322

    Google Scholar 

  • Zobel M (1997) The relative role of species pools in determining plant species richness: an alternative explanation of species coexistence? Tree 12:266–269

    CAS  PubMed  Google Scholar 

  • Zobel M, van der Maarek E, Dupré C (1998) Species pool: the concept, its determination and significance for community restoration. Appl Veg Sci 1:55–66

    Article  Google Scholar 

  • Zobel M, Otto R, Laanisto L, Naranjo-Cigala A, Pärtel M, Fernández-Palacios JM (2011) The formation of species pools: historical habitat abundance affects current local diversity. Glob Ecol Biogeogr 20:251–259

    Article  Google Scholar 

Download references

Acknowledgments

We thank A. Harris, J. Lawyer, J. Lee, C. Lim, J. Orlowsky, S. Robertson, N.-A. Rose and J. Salokannel for the field or lab assistance. Seeds were kindly provided by G. O’Neill and S. Reitenbach at the BC Ministry of Forests, Lands and Natural Resources. Two anonymous reviewers gave extremely helpful feedback on the manuscript. Funding was provided by the Forest Genetics Council of BC.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Author notes

  1. Brian J. Pickles

    Present address: Department of Forest and Conservation Sciences, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

Authors and Affiliations

  1. Ecosystem Science and Management Program, University of Northern British Columbia, 3333 University Way, Prince George, BC, V2N 4Z9, Canada

    Brian J. Pickles, Monika A. Gorzelak, D. Scott Green, Keith N. Egger & Hugues B. Massicotte

Authors
  1. Brian J. Pickles
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Monika A. Gorzelak
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. D. Scott Green
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Keith N. Egger
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hugues B. Massicotte
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Brian J. Pickles.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 255 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pickles, B.J., Gorzelak, M.A., Green, D.S. et al. Host and habitat filtering in seedling root-associated fungal communities: taxonomic and functional diversity are altered in ‘novel’ soils. Mycorrhiza 25, 517–531 (2015). https://doi.org/10.1007/s00572-015-0630-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-015-0630-y

Keywords

Search

Navigation