Abstract
Shrub willows (Salix spp.) form associations with arbuscular mycorrhizal (AM), ectomycorrhizal (EM) and dark septate endophytic (DSE) fungi. Willow root colonization by these three types of fungi was studied on a deglaciated forefront of Lyman Glacier, Washington, USA. Root colonization was low; less than 1% of the root length was colonized by AM and 25.6% by DSE. EM colonized 25% of the root tips and 19.4% of the root length. AM and DSE colonization were not related to distance from the present glacier terminus or to canopy cover. EM colonization increased with distance from the glacier terminus based on gridline intercept data but not on root tip frequency data. Availability of propagules in the substrate was low, but numbers of propagules increased with distance from the glacier terminus. The EM communities were dominated by three ascomycetes showing affinity to Sordariaceae in BLAST analyses. Other frequent taxa on the glacier forefront included species of Cortinariaceae, Pezizaceae, Russulaceae, Thelephoraceae and Tricholomataceae. When occurrence of individual taxa was used as a response variable to canopy cover, distance from the glacier terminus, and their interaction, four different fungal guilds were identified: 1) fungi that did not respond to these environmental variables; 2) fungi that occurred mainly in intercanopy areas and decreased with distance from the glacier terminus; 3) fungi that were insensitive to canopy cover but increased with distance from the glacier terminus; 4) fungi that occurred mainly under willow canopies and increased with distance from the glacier terminus. We suggest that fungal colonization is mainly limited by fungal propagule availability. Environmental conditions may also limit successful establishment of plant-fungus associations. We propose that the four EM guilds partly explain successional dynamics. The initial EM community comprises fungi that tolerate low organic matter and nitrogen environment (first and second guilds above). During later community development, these fungi are replaced by those that benefit from an increased organic matter and nitrogen environment (third and fourth guilds above).
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References
Alexander M (1965) Most probable number method for microbial populations. In: Black CA (eds) Methods of soil analysis, part 2. Chemical and microbiological properties. American Society of Agronomy, Madison, Wis, pp 1467–1472
Alfredsen G, Høiland K (2001) Succession of terrestrial macrofungi along a deglaciation gradient at Glacier Blåisen, South Norway. Nord J Bot 21:19–37
Allen E, Chambers JE, Connor KF, Allen MF, Brown RW (1987) Natural re-establishment of mycorrhizae in disturbed alpine ecosystems. Arct Alp Res 19:11–20
Allen MF (1988) Re-establishment of VA mycorrhizas following severe disturbance: comparative patch dynamics of a shrub desert and a subalpine volcano. Proc R Soc Edinburgh 94B: 63–71
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
Baar J (1996) The ectomycorrhizal flora of primary and secondary stands of Pinus sylvestris in relation to soil conditions and ectomycorrhizal succession. J Veg Sci 7:497–504
Baar J, Horton TR, Kretzer AM, Bruns TD (1999) Mycorrhizal colonization of Pinus muricata from resistant propagules after a stand-replacing fire. New Phytol 143:409–418
Bruns T, Tan J, Bidartondo M, Szaro T, Redecker D (2002) Survival of Suillus pungens and Amanita francheti ectomycorrhizal genets was rare or absent after a stand-replacing wildfire. New Phytol 155:517–523
Cázares E (1992) Mycorrhizal fungi and their relationship to plant succession in subalpine habitats. PhD thesis, Oregon State University
Daniels BA, Skipper HD (1982) Methods for recovery and quantitative estimation of propagules from soil. In: Schenk NC (eds) Methods and principles of mycorrhizal research. American Phytopathological Society, St. Paul, Minn, pp 29–35
Danielson RM (1991) Temporal changes and effects of amendments on the occurrence of sheathing mycorrhizas of conifers growing in oil sand tailings and coal spoil. Agric Ecosyst Environ 35:261–281
Deacon JW, Fleming LV (1992) Interactions of ectomycorrhizal fungi. In: Allen MF (eds) Mycorrhizal functioning: an integrative plant-fungal process. Chapman and Hall, New York, pp 249–300
Dighton J, Poskitt JM, Howard DM (1986) Changes in occurrence of basidiomycete fruit bodies during forest stand development with specific reference to mycorrhizal species. Trans Br Mycol Soc 87:163–171
Gardes M, Bruns TD (1996) Community structure of ectomycorrhizal fungi in a Pinus muricata forest: above- and below-ground views. Can J Bot 74:1572–1583
Gibson F, Deacon JW (1988) Experimental study of establishment of ectomycorrhizas in different regions of birch root systems. Trans Br Mycol Soc 91:239–251
Gibson F, Deacon JW (1990) Establishment of ectomycorrhizas in aseptic culture: effects of glucose, nitrogen and phosphorus in relation to successions. Mycol Res 94:166–172
Glen M, Tommerup IC, Bougher NL, O’Brien PA (2002) Are Sebacinaceae common and widespread ectomycorrhizal associates of Eucalyptus species in Australian forests? Mycorrhiza 12:243–247
Gryta H, Debaud J-C, Effose A, Gay G, Marmeisse R (1997) Fine-scale structure of populations of the ectomycorrhizal fungus Hebeloma cylindrosporum in coastal sand dune forest ecosystems. Mol Ecol 6:353–364
Harley JL, Harley EL (1987) A checklist of mycorrhiza in the British flora. New Phytol 105(Suppl):1–102
Helm DJ, Allen EB, Trappe JM (1996) Mycorrhizal chronosequence near Exit Glacier, Alaska. Can J Bot 74:1496–1506
Horton TR, Cázares E, Bruns TD (1998) Ectomycorrhizal, vesicular-arbuscular and dark septate fungal colonization of bishop pine (Pinus muricata) seedlings in the first 5 months of growth after wildfire. Mycorrhiza 8:11–18
Jumpponen A (1999) Spatial distribution of discrete RAPD phenotypes of a root endophytic fungus, Phialocephala fortinii, at a primary successional site on a glacier forefront. New Phytol 141:333–344
Jumpponen A (2001) Dark septate endophytes — are they mycorrhizal. Mycorrhiza 11:207–211
Jumpponen A (2003) Soil fungal community assembly in a primary successional glacier forefront ecosystem as inferred from rDNA sequence analyses. New Phytol 158:569–578
Jumpponen A, Trappe JM (1998) Dark-septate root endophytes: a review with special reference to facultative biotrophic symbiosis. New Phytol 140:295–310
Jumpponen A, Mattson K, Trappe JM, Ohtonen R (1998) Effects of established willows on primary succession on Lyman Glacier forefront: evidence for simultaneous canopy inhibition and soil facilitation. Arct Alp Res 30:31–39
Jumpponen A, Trappe JM, Cázares E (1999a) Ectomycorrhizal fungi in Lyman Lake Basin: a comparison between primary and secondary successional sites. Mycologia 91:575–582
Jumpponen A, Väre H, Mattson KG, Ohtonen R, Trappe JM (1999b) Characterization of ‘safe sites’ for pioneers in primary succession on recently deglaciated terrain. J Ecol 87:98–105
Jumpponen A, Trappe JM, Cázares E (2002) Occurrence of ectomycorrhizal fungi on a receding glacier forefront. Mycorrhiza 12:43–49
Last FT, Dighton J, Mason PA (1987) Successions of sheathing mycorrhizal fungi. Trends in Ecology and Evolution 2:157–161
Lilleskov EA, Fahey TJ, Horton TR, Lovett GM (2002a) Belowground ectomycorrhizal community change over a nitrogen deposition gradient in Alaska. Ecology 83:104–115
Lilleskov EA, Hobbie EA, Fahey TJ (2002b) Ectomycorrhizal fungal taxa differing in response to nitrogen deposition also differ in pure culture organic nitrogen use and natural abundance of nitrogen isotopes. New Phytol 154:219–231
Lodge DJ, Wentworth TR (1990) Negative association among VA mycorrhizal fungi and some ectomycorrhizal fungi inhabiting the same root system. Oikos 57:347–356
Matthews JA (1992) The ecology of recently-deglaciated terrain — a geoecological approach to glacier forelands and primary succession. Cambridge University Press, New York
Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbioses: community-ecological consequences and practical implication. In: Allen MF (eds) Mycorrhizal functioning: an integrative plant-fungal process. Chapman and Hall, New York, pp 357–423
Neville J, Tessier JL, Morrison I, Scaratt J, Canning B, Klironomos JN (2002) Soil depth distribution of ecto- and arbuscular mycorrhizal fungi associated with Populus tremuloides within a 3-year-old boreal forest clear-cut. Appl Soil Ecol 19:209–216
Ohtonen R, Fritze H, Pennanen T, Jumpponen A, Trappe JM (1999) Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia 119:239–246
Peter M, Ayer F, Egli S (2001) Nitrogen addition in a Norway spruce stand altered macromycete sporocarp production and below-ground ectomycorrhizal species composition. New Phytol 149:311–325
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:158–161
Pickett STA, Collins SL, Armesto JJ (1987) A hierarchical consideration of causes and mechanisms of succession. Vegetatio 69:109–114
Read DJ (1989) Mycorrhizas and nutrient cycling in sand dune ecosystems. Proc R Soc Edinburgh 96B:89–110
Read DJ (1992) The mycorrhizal fungal community with special reference to nutrient mobilization. In: Carroll GC, Wicklow DT (eds) The fungal community — its organization and role in the ecosystem. Dekker, New York, pp 631–654
SAS (1989) SAS/STAT user’s guide, version 6, 4th edn, vol 1. SAS, Cary, N.C.
SAS (1997) SAS/STAT software: changes and enhancements through release 6.12. SAS, Cary, N.C.
Selosse M-A, Bauer R, Moyersoen B (2002) Basal hymenomycetes belonging to the Sebacinaceae are ectomycorrhizal on temperate deciduous trees. New Phytol 155:183–195
Sigler WV, Zeyer J (2002) Microbial diversity and activity along the forefields of two receding glaciers. Microb Ecol 43:397–407
Termorshuizen AJ, Schaffers AP (1989) Succession of mycorrhizal fungi in stands of Pinus sylvestris in the Netherlands. Agric Ecosyst Environ 28:503–507
Trappe JM, Luoma DL (1992) The ties that bind: fungi in ecosystems. In: Carroll GC, Wicklow DT (eds) The fungal community — its organization and role in the ecosystem. Dekker, New York, pp 17–27
Trappe JM, Strand RF (1969) Mycorrhizal deficiency in a Douglas-fir region nursery. For Sci 15:381–389
Tyler G (1989) Edaphical distribution patterns of macrofungal species in deciduous forest in South Sweden. Acta Ecol 10:309–326
van der Heijden EW, Vosatka M (1999) Mycorrhizal associations of Salix repens L. communities in succession of dune ecosystems. II. Mycorrhizal dynamics and interactions of ectomycorrhizal and arbuscular mycorrhizal fungi. Can J Bot 77:1833–1841
van der Heijden EW, de Vries FW, Kuyper TW (1999) Mycorrhizal associations of Salix repens L. communities in succession of dune ecosystems. I. Above-ground and below-ground views of ectomycorrhizal fungi in relation to soil chemistry. Can J Bot 77:1821–1832
Visser S (1995) Ectomycorrhizal fungal succession in jack pine stands following wildfire. New Phytol 129:389–401
Wallenda T, Kottke I (1998) Nitrogen deposition and ectomycorrhizas. New Phytol 139:169–187
Warcup JH (1988) Mycorrhizal associations of isolates of Sebacina vermifera. New Phytol 110:227–231
Wöllecke J (2001) Characterisierung der Mykorrhizazönosen zweier Kiefernforste unterschiedlicher trophie. PhD thesis, Brandenburgischen Technischen Universität, Cottbus
Wurzburger N, Bitartondo MI, Bledsoe CS (2001) Characterization of Pinus ectomycorrhizas from mixed conifer and pygmy forests using morphotyping and molecular methods. Can J Bot 79:1211–1216
Yu T, Nassuth A, Peterson RL (2001) Characterization of the interaction between the dark septate fungus Phialocephala fortinii and Asparagus officinalis roots. Can J Microbiol 47:741–753
Acknowledgements
This work was supported by National Science Foundation EPSCoR Grant No. 9874732 with matching support from the State of Kansas and National Science Foundation OPP Grant No. 0221489. We are grateful to Nicolo Gentili, Francesco Gentili, Anna Jumpponen and Dr. James M. Trappe, who assisted in sample collection and data recording at the field site. Early manuscripts were greatly improved by helpful comments from two anonymous reviewers, Drs. Charles L. Kramer, and James M. Trappe. Anna Jumpponen edited and revised the manuscript.
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Trowbridge, J., Jumpponen, A. Fungal colonization of shrub willow roots at the forefront of a receding glacier. Mycorrhiza 14, 283–293 (2004). https://doi.org/10.1007/s00572-003-0264-3
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DOI: https://doi.org/10.1007/s00572-003-0264-3