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The effect of fertilization on the below-ground diversity and community composition of ectomycorrhizal fungi associated with western hemlock (Tsuga heterophylla)

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Abstract

Fertilization typically reduces ectomycorrhizal diversity shortly after its application but less is known about its longer-term influence on fungal species. Long-term effects are important in forests where fertilizer is rarely applied. We compared fungal species composition in western hemlock control plots with plots last fertilized 7 years ago with nitrogen (N) or nitrogen plus phosphorus (N + P). The N + P fertilization had a significant lingering effect, increasing the tree size and foliar P content of the western hemlocks. From ectomycorrhizal roots of 24-year-old trees from northern Vancouver Island, Canada, we identified fungi from 12 samples per treatment, by amplifying, cloning, and sequencing fungal ribosomal DNA fragments, placing sequences with 97% or more identity in the same operational taxonomic unit (OTU). Diversity was high across treatments; we detected 77 fungal OTUs, 52 from ectomycorrhizal genera, among 922 clone sequences. The five most frequent OTUs were similar in abundance across treatments. Only 19 OTUs matched any of the 197 previously reported ectomycorrhizal species of western hemlock. Species composition but not diversity in nitrogen plus phosphorus plots differed significantly from control or nitrogen plots. Two Cortinarius OTUs were indicator species for nitrogen plus phosphorus plots and presence of Cortinarius cinnamomeus was correlated with control or nitrogen plots. After 7 years, fertilization history had made no detectable difference in ectomycorrhizal fungal diversity, but long-lasting changes in environment resulting from fertilization had a lingering effect on fungal ectomycorrhizal species composition.

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References

  • Avis PG, McLaughlin DJ, Dentinger BC, Reich PB (2003) Long-term increase in nitrogen supply alters above- and below-ground ectomycorrhizal communities and increases the dominance of Russula spp. in a temperate oak savanna. New Phytol 160:239–253 doi:10.1046/j.1469-8137.2003.00865.x

    Article  Google Scholar 

  • Baar J (1995) Ectomycorrhizal fungi of Scots pine as affected by litters and humus. Ph.D. Thesis, University of Wageningen, Netherlands

  • Baum C, Makeschin F (2000) Effects of nitrogen and phosphorus fertilization on mycorrhizal formation of two poplar clones (Populus trichocarpa and P. tremula × tremuloides). J Plant Nutr Soil Sci 163:491–497. doi:10.1002/1522-2624(200010)163:5<491::AID-JPLN491>3.0.CO;2-3

    Article  CAS  Google Scholar 

  • Bennett JN, Blevins LL, Barker JE, Blevins DP, Prescott CE (2003) Increases in tree growth and nutrient supply still apparent 10 to 13 years following fertilization and vegetation control of salal-dominated cedar–hemlock stands on Vancouver Island. Can J For Res 33:1516–1524 doi:10.1139/x03-069

    Article  CAS  Google Scholar 

  • Berch SM, Brockley RP, Battigelli JP, Hagerman S, Holl B (2006) Impacts of repeated fertilization on components of the soil biota under a young lodgepole pine stand in the interior of British Columbia. Can J For Res 36:1415–1426 doi:10.1139/X06-037

    Article  CAS  Google Scholar 

  • Bidartondo MI, Ek H, Wallander H, Söderström B (2001) Do nutrient additions alter carbon sink strength of ectomycorrhizal fungi? New Phytol 151:543–550 doi:10.1046/j.1469-8137.2001.00180.x

    Article  CAS  Google Scholar 

  • Blevins LL, Prescott CE (2002) Salal Cedar Hemlock Integrated Research Program Research Update #2: silvicultural practices for regeneration of cedar-hemlock sites in coastal British Columbia. In Vancouver, B.C.: University of British Columbia

  • Blevins LL, Prescott CE, Van Niejenhuis A (2006) The roles of nitrogen and phosphorus in increasing productivity of western hemlock and western redcedar plantations on northern Vancouver Island. For Ecol Manage 234:116–122 doi:10.1016/j.foreco.2006.06.029

    Article  Google Scholar 

  • Bradley RL, Titus BD, Preston CM, Bennett JN (2000) Improvement of nutritional site quality 13 years after single application of fertiliser N and P on regenerating cedar–hemlock cutovers on northern Vancouver Island, B.C. Plant Soil 223:195–206 doi:10.1023/A:1004896116130

    Article  CAS  Google Scholar 

  • Brandrud TE (1995) The effects of experimental nitrogen addition on the ectomycorrhizal fungus flora in an oligotrophic spruce forest at Gårdsjön, Sweden. For Ecol Manage 71:111–122 doi:10.1016/0378-1127(94)06088-Z

    Article  Google Scholar 

  • Bruns TD (1995) Thoughts on the processes that maintain local species diversity of ectomycorrhizal fungi. Plant Soil 170:63–73 doi:10.1007/BF02183055

    Article  CAS  Google Scholar 

  • Cairney JWG (1999) Intraspecific physiological variation: implications for understanding functional diversity in ectomycorrhizal fungi. Mycorrhiza 9:125–135 doi:10.1007/s005720050297

    Article  Google Scholar 

  • Cheng X, Bledsoe CS (2002) Seasonal and site effects on oak fine root production and ectomycorrhizal colonization in California oak woodland. In Gen. Tech. Rep.: USDA Forest Service, pp 99–106

  • de Román M, de Miguel AM (2005) Post-fire, seasonal and annual dynamics of the ectomycorrhizal community in a Quercus ilex L. forest over a 3-year period. Mycorrhiza 15:471–482 doi:10.1007/s00572-005-0353-6

    Article  PubMed  Google Scholar 

  • Durall DM, Jones MD, Wright EF, Kroeger P, Coates KD (1999) Species richness of ectomycorrhizal fungi in cutblocks of different sizes in the Interior Cedar–Hemlock forests of northwestern British Columbia: sporocarps and ectomycorrhizae. Can J For Res 29:1322–1332 doi:10.1139/cjfr-29-9-1322

    Article  Google Scholar 

  • Edwards IP, Cripliver JL, Gillespie AR, Johnsen KH, Scroller M, Turco RF (2004) Nitrogen availability alters macrofungal basidiomycete community structure in optimally fertilized lobolly pine forest. New Phytol 162:755–770 doi:10.1111/j.1469-8137.2004.01074.x

    Article  Google Scholar 

  • Ek H (1997) The influence of nitrogen fertilization on the carbon economy of Paxillus involutus in ectomycorrhizal associations with Betula pendula. New Phytol 135:133–142 doi:10.1046/j.1469-8137.1997.00621.x

    Article  CAS  Google Scholar 

  • Fransson PMA, Taylor AFS, Finlay RD (2000) Effects of continuous optimal fertilization on belowground ectomycorrhizal community structure in a Norway spruce forest. Tree Physiol 20:599–606

    Article  PubMed  Google Scholar 

  • Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manage 196:159–171 doi:10.1016/j.foreco.2004.03.018

    Article  Google Scholar 

  • Gill RS, Lavender DP (1983) Urea fertilization and foliar nutrient composition of Western Hemlock (Tsuga heterophylla (Raf.) Sarc.). For Ecol Manage 6:333–341 doi:10.1016/0378-1127(83)90041-5

    Article  CAS  Google Scholar 

  • Green RN, Klinka K (1994) A field guide to site identification and interpretation for the Vancouver forest region. Ministry of Forests, Victoria, B.C.

    Google Scholar 

  • Hagerberg D, Thelin G, Wallander H (2003) The production of ectomycorrhizal mycelium in forests: relation between forest nutrient status and local mineral sources. Plant Soil 252:279–290 doi:10.1023/A:1024719607740

    Article  CAS  Google Scholar 

  • Harvey AE, Jurgensen MF, Larsen MJ (1978) Seasonal distribution of ectomycorrhizae in a mature Douglas-fir/Larch forest soil in western Montana. For Sci 24:203–208

    Google Scholar 

  • Kårén O, Nylund J-E (1997) Effects of ammonium sulphate on the community structure and biomass of ectomycorrhizal fungi in a Norway spruce stand in southwestern Sweden. Can J Bot 75:1628–1642 doi:10.1139/b97-875

    Article  Google Scholar 

  • Kernaghan G, Berch SM, Carter R (1995) Effect of urea fertilization on ectomycorrhizae of 20-year-old Tsuga heterophylla. Can J For Res 25:891–901 doi:10.1139/x95-098

    Article  Google Scholar 

  • King JS, Albaugh TJ, Allen HL, Buford M, Strain BR, Dougherty P (2002) Below-ground carbon input to soil is controlled by nutrient availability and fine root dynamics in loblolly pine. New Phytol 154:389–398 doi:10.1046/j.1469-8137.2002.00393.x

    Article  Google Scholar 

  • Kranabetter JM, Kroeger P (2001) Ectomycorrhizal mushroom response to partial cutting in a western hemlock–western redcedar forest. Can J For Res 31:978–987 doi:10.1139/cjfr-31-6-978

    Article  Google Scholar 

  • Kranabetter JM, Wylie T (1998) Ectomycorrhizal community structure across forest openings on naturally regenerated western hemlock seedlings. Can J Bot 76:189–196 doi:10.1139/cjb-76-2-189

    Google Scholar 

  • Kranabetter JM, Friesen J, Gamiet S, Kroeger P (2005) Ectomycorrhizal mushroom distribution by stand age in western hemlock–lodgepole pine forests of northwestern British Columbia. Can J For Res 35:1527–1539 doi:10.1139/x05-095

    Article  Google Scholar 

  • Kropp BR (1981a) Fungi from decayed wood as ectomycorrhizal symbionts of western hemlock. Can J For Res 12:36–39 doi:10.1139/x82-005

    Article  Google Scholar 

  • Kropp BR (1981b) Rotten wood as mycorrhizal inoculum for containerized western hemlock. Can J For Res 12:428–431

    Article  Google Scholar 

  • Kropp BR, Trappe JM (1982) Ectomycorrhizal fungi of Tsuga heterophylla. Mycologia 74:479–488 doi:10.2307/3792970

    Article  Google Scholar 

  • Leckie SE, Prescott CE, Grayston SJ (2004) Forest floor microbial community response to tree species and fertilization of regenerating coniferous forests. Can J For Res 34:1426–1435 doi:10.1139/x04-028

    Article  Google Scholar 

  • Lewis T (1982) Ecosystems of the Port McNeill block 4 of Tree License 25. In Internal report. Western Forest Products Ltd, Vancouver, BC

  • Lilleskov EA, Bruns TD (2003) Root colonization dynamics of two ectomycorrhizal fungi of contrasting life history strategies are mediated by addition of organic nutrient patches. New Phytol 159:141–151 doi:10.1046/j.1469-8137.2003.00794.x

    Article  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 doi:10.1890/1051-0761(2001)011[0397:EFACCO]2.0.CO;2

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 doi:10.1046/j.1469-8137.2002.00367.x

    Article  CAS  Google Scholar 

  • Liu YJ, Rogers SO, Ammirati JF (1997) Phylogenetic relations in Dermocybe and related Cortinarius taxa based on nuclear ribosomal DNA internal transcribed spacers. Can J Bot 75:519–532

    Article  CAS  Google Scholar 

  • Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10 doi:10.1007/BF00011685

    Article  CAS  Google Scholar 

  • Majdi H, Damm E, Nylund J-E (2001) Longevity of mycorrhizal roots depend on branching order and nutrient availability. New Phytol 150:195–202 doi:10.1046/j.1469-8137.2001.00065.x

    Article  Google Scholar 

  • Mallik AU, Prescott CE (2001) Growth inhibitory effects of salal on western hemlock and western red cedar. Agron J 93:85–92

    Article  Google Scholar 

  • McCune B, Mefford M (1999) PC-ORD. Multivariate analysis of ecological data. MjM Software Design, Gleneden Beach, Oregon USA

    Google Scholar 

  • McCune B, Grace JB, Urban DL (2002) Analysis of ecological communities. MjM Software Design, Glenedon Beach, Oregon USA

    Google Scholar 

  • McWilliams J, Green B, Lewis T (2007) Phase II review of ecosystem classification in TFL6. In: B.A. Blackwell and Associates Ltd, prepared for Western Forest Products Inc, pp 1–103

  • Mehmann B, Egli S, Braus GH, Brunner I (1995) Coincidence between molecularly or morphologically classified ectomycorrhizal morphotypes and fruitbodies in a Spruce forest. In: Stocchi V, Bonfante P, Nuti M (eds) Biotechnology of ectomycorrhizae: molecular approaches. Plenum, New York, pp 41–52

    Chapter  Google Scholar 

  • Molina R (1980) Ectomycorrhizal inoculation of containerized western conifer seedlings. Corvallis, Oregon: USDA Forest Service Research Note PNW-357, Pacific Northwest Forest & Range Experiment Station, pp 1–10

  • Molina R, Trappe JM (1982) Patterns of ectomycorrhizal host specificity and potential among Pacific Northwest conifers and fungi. For Sci 28:423–458

    Google Scholar 

  • Nara K, Nakaya H, Wu B, Zhou Z, Hogetsu T (2003) Underground primary succession of ectomycorrhizal fungi in a volcanic desert on Mount Fuji. New Phytol 159:743–756 doi:10.1046/j.1469-8137.2003.00844.x

    Article  CAS  Google Scholar 

  • Negrave RW (2004) Effects of establishment density, fertilization and scarification on growth and foliar nutrient concentrations of juvenile western redcedar and western hemlock plantations on CH and HA sites. In Final Report: Western Forest Products Limited

  • O'Brien HE, Parrent JL, Jackson JA, Moncalvo J-M, Vilgalys R (2005) Fungal community analysis by large-scale sequencing of environmental samples. Appl Environ Microbiol 71:5544–5550 doi:10.1128/AEM.71.9.5544-5550.2005

    Article  PubMed  PubMed Central  Google Scholar 

  • O'Dell TE, Ammirati JF, Schreiner EG (1999) Species richness and abundance of ectomycorrhizal basidiomycete sporocarps on a moisture gradient in the Tsuga heterophylla zone. Can J Bot 77:1699–1711 doi:10.1139/cjb-77-12-1699

    Article  Google Scholar 

  • Peintner U, Moncalvo J-M, Vilgalys R (2004) Toward a better understanding of the infrageneric relationships in Cortinarius (Agaricales, Basidiomycota). Mycologia 96:1042–1058 doi:10.2307/3762088

    Article  CAS  PubMed  Google Scholar 

  • 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 doi:10.1046/j.1469-8137.2001.00030.x

    Article  Google Scholar 

  • Pojar J, Klinka K, Dermarchi DA (1991) Coastal western hemlock zone. In: Meidinger D, Pojar J (eds) Ecosystems of British Columbia. Ministry of Forests, Victoria, BC, pp 95–111

    Google Scholar 

  • Prescott CE, McDonald MA, Weetman GF (1993) Availability of N and P in the forest floors of adjacent stands of western red cedar–western hemlock and western hemlock–amabilis fir on northern Vancouver Island. Can J For Res 23:605–610 doi:10.1139/x93-080

    Article  CAS  Google Scholar 

  • Swofford D (2003) PAUP*. Phylogenetic analysis using parsimony* (and other methods). Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  • Taylor AFS (2002) Fungal diversity in ectomycorrhizal communities: sampling effort and species detection. Plant Soil 244:19–28 doi:10.1023/A:1020279815472

    Article  CAS  Google Scholar 

  • Tedersoo L, Kõljalg U, Hallenberg N, Larsson K-H (2003) Fine scale distribution of ectomycorrhizal fungi and roots across substrate layers including coarse woody debris in a mixed forest. New Phytol 159:153–165 doi:10.1046/j.1469-8137.2003.00792.x

    Article  CAS  Google Scholar 

  • Trappe JM (1962) Fungus associates of ectotrophic mycorrhizae. Bot Rev 28:538–606 doi:10.1007/BF02868758

    Article  Google Scholar 

  • Trappe JM (2004) Habitat and host associations of Craterellus tubaeformis in northwestern Oregon. Mycologia 96:498–509 doi:10.2307/3762170

    Article  CAS  PubMed  Google Scholar 

  • Wallenda T, Kottke I (1998) Nitrogen deposition and ectomycorrhizas. New Phytol 139:169–187 doi:10.1046/j.1469-8137.1998.00176.x

    Article  CAS  Google Scholar 

  • Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH (2004) Ecological linkages between aboveground and below ground biota. Science 304:1629–1633 doi:10.1126/science.1094875

    Article  CAS  PubMed  Google Scholar 

  • Zar JH (1999) Biostatistical analysis. Prentice Hall, Upper Saddle River, New Jersey

    Google Scholar 

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Acknowledgments

Grants from the National Science and Research Council of Canada and from British Columbia’s Forest Science Program provided research funding. Western Forest Products Ltd. sponsored an NSERC Industrial Postgraduate Scholarship to S. Wright and provided accommodation at the study site. Annette van Niejenhuis (Western Forest Products Ltd.) provided on-site support. SeaRa Lim assisted with the molecular work and Carol Wright assisted with the fieldwork. We thank Gary Bradfield for helping with multivariate analyses and Cindy Prescott and Suzanne Simard (all from University of British Columbia) for constructive comments throughout this project.

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  1. Department of Botany, The University of British Columbia, Vancouver, BC, V6T 1Z4, Canada

    Shannon H. A. Wright & Mary L. Berbee

  2. Research Branch Laboratory, Ministry of Forestry, 4300 North Road, Victoria, BC, V8Z 5J3, Canada

    Shannon M. Berch

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  1. Shannon H. A. Wright
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Correspondence to Shannon H. A. Wright.

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Wright, S.H.A., Berch, S.M. & Berbee, M.L. The effect of fertilization on the below-ground diversity and community composition of ectomycorrhizal fungi associated with western hemlock (Tsuga heterophylla). Mycorrhiza 19, 267–276 (2009). https://doi.org/10.1007/s00572-008-0218-x

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