BACKGROUND AND AIMS: Picea abies, Pinus mugo and Rhododendron ferrugineum co-exist at the alpine tree line, and can have different mycorrhizal communities. The activity and diversity of mycorrhizal fungi are considered to be important factors in regulation of soil function. METHODS: At a tree line site and a lower elevation site in the Austrian Alps, the community structure of ectomycorrhiza on Picea abies and Pinus mugo was determined. The activity of surface enzymes was determined on ectomycorrhizal and ericoid mycorrhizal roots. In soils, the activity of a range of enzymes, nitrogen (N) mineralization and biomass decomposition were determined. RESULTS: The community structure of the ectomycorrhizal community of Picea abies and Pinus mugo differed strongly, but the average activity of surface enzymes of the ectomycorrhizal communities was similar. A lower root surface enzyme activity was determined on Rhododendron ferrugineum. Soil N-mineralization under Rhododendron ferrugineum was significantly lower than under Picea abies and Pinus mugo. In soil, the activity of a range of enzymes did not differ at the tree line but differed between the tree line and the lower elevation sites. CONCLUSION: The different ectomycorrhizal communities on Picea abies and Pinus mugo and ericoid mycorrhizas on Rhododendron ferrugineum support similar ecosystem functions in soil.

Department of Ecology Mongolian University of Life Science Zaisan Mailbox 57 Khan Uul district Ulaanbaator 17024 Mongolia

Department of Landscape Carbon Deposition Global Change Research Institute Academy of Sciences of the Czech Republic Na Sádkách 7 370 05 Ceské Budejovice Czech Republic

Institute of Forest Ecology University of Natural Resources and Life Sciences Vienna Peter Jordan Straße 82 1190 Vienna Austria

See more in PubMed

Agerer R. Colour atlas of ectomycorrhizae. Germany: Einhorn-Verlag Eduard Dietenberger GmbH; 1997.

Agerer R. Exploration types of ectomycorrhizae. Mycorrhiza. 2001;11:107–114. doi: 10.1007/s005720100108. DOI

Agerer R. Diversity of ectomycorrhizae as seen from below and above ground: the exploration types. Z Mykol. 2007;73:61–88.

Aggangan NS, Dell B, Malajczuk N. Effects of soil pH on the ectomycorrhizal response of Eucalyptus Urophylla seedlings. New Phytol. 1996;134:539–546. doi: 10.1111/j.1469-8137.1996.tb04372.x. DOI

Ajwa H, Dell C, Rice C. Changes in enzyme activities and microbial biomass of tallgrass prairie soil as related to burning and nitrogen fertilization. Soil Biol Biochem. 1999;31:769–777. doi: 10.1016/S0038-0717(98)00177-1. DOI

Alexander I, Hardy K. Surface phosphatase activity of Sitka spruce mycorrhizas from a serpentine site. Soil Biol Biochem. 1981;13:301–305. doi: 10.1016/0038-0717(81)90066-3. DOI

Baldrian P. Ectomycorrhizal fungi and their enzymes in soils: is there enough evidence for their role as facultative soil saprotrophs? Oecologia. 2009;161:657–660. doi: 10.1007/s00442-009-1433-7. PubMed DOI

Baldrian P, Šnajdr J, Merhautová V, Dobiášová P, Cajthaml T, Valášková V. Responses of the extracellular enzyme activities in hardwood forest to soil temperature and seasonality and the potential effects of climate change. Soil Biol Biochem. 2013;56:60–68. doi: 10.1016/j.soilbio.2012.01.020. DOI

Bartlett EM, Lewis D. Surface phosphatase activity of mycorrhizal roots of beech. Soil Biol Biochem. 1973;5:249–257. doi: 10.1016/0038-0717(73)90008-4. DOI

Baxter JW, Dighton J. Ectomycorrhizal diversity alters growth and nutrient acquisition of grey birch (Betula populifolia) seedlings in host–symbiont culture conditions. New Phytol. 2001;152:139–149. doi: 10.1046/j.0028-646x.2001.00245.x. PubMed DOI

Bending GD, Read DJ. Effects of the soluble polyphenol tannic acid on the activities of ericoid and ectomycorrhizal fungi. Soil Biol Biochem. 1996;28:1595–1602. doi: 10.1016/S0038-0717(96)00257-X. DOI

Bending GD, Read DJ. Nitrogen mobilization from protein-polyphenol complex by ericoid and ectomycorrhizal fungi. Soil Biol Biochem. 1996;28:1603–1612. doi: 10.1016/S0038-0717(96)00258-1. DOI

Bending GD, Read DJ. Lignin and soluble phenolic degradation by ectomycorrhizal and ericoid mycorrhizal fungi. Mycol Res. 1997;101:1348–1354. doi: 10.1017/S0953756297004140. DOI

Bills G, Holtzman G, Miller O., Jr Comparison of ectomycorrhizal-basidiomycete communities in red spruce versus northern hardwood forests of West Virginia. Can J Bot. 1986;64:760–768. doi: 10.1139/b86-098. DOI

Boettcher S, Kalisz PJ. Single-tree influence on soil properties in the mountains of eastern Kentucky. Ecology. 1990;71:1365–1372. doi: 10.2307/1938273. DOI

Buée M, Courty P, Mignot D, Garbaye J. Soil niche effect on species diversity and catabolic activities in an ectomycorrhizal fungal community. Soil Biol Biochem. 2007;39:1947–1955. doi: 10.1016/j.soilbio.2007.02.016. DOI

Burke DJ, Weintraub MN, Hewins CR, Kalisz S. Relationship between soil enzyme activities, nutrient cycling and soil fungal communities in a northern hardwood forest. Soil Biol Biochem. 2011;43:795–803. doi: 10.1016/j.soilbio.2010.12.014. DOI

Cairney J, Meharg A. Influences of anthropogenic pollution on mycorrhizal fungal communities. Environ Pollut. 1999;106:169–182. doi: 10.1016/S0269-7491(99)00081-0. PubMed DOI

Clemmensen KE, Finlay RD, Dahlberg A, Stenlid J, Wardle DA, Lindahl BD. Carbon sequestration is related to mycorrhizal fungal community shifts during long-term succession in boreal forests. New Phytol. 2015;205:1525–1536. doi: 10.1111/nph.13208. PubMed DOI

Cornelissen J, Aerts R, Cerabolini B, Werger M, Van Der Heijden M. Carbon cycling traits of plant species are linked with mycorrhizal strategy. Oecologia. 2001;129:611–619. doi: 10.1007/s004420100752. PubMed DOI

Courty PE, Pritsch K, Schloter M, Hartmann A, Garbaye J. Activity profiling of ectomycorrhiza communities in two forest soils using multiple enzymatic tests. New Phytol. 2005;167:309–319. doi: 10.1111/j.1469-8137.2005.01401.x. PubMed DOI

Courty PE, Franc A, Garbaye J. Temporal and functional pattern of secreted enzyme activities in an ectomycorrhizal community. Soil Biol Biochem. 2010;42:2022–2025. doi: 10.1016/j.soilbio.2010.07.014. DOI

Cullings K, Courty PE. Saprotrophic capabilities as functional traits to study functional diversity and resilience of ectomycorrhizal community. Oecologia. 2009;161:661–664. doi: 10.1007/s00442-009-1434-6. PubMed DOI

DeLuca T, Nilsson M, Zackrisson O. Nitrogen mineralization and phenol accumulation along a fire chronosequence in northern Sweden. Oecologia. 2002;133:206–214. doi: 10.1007/s00442-002-1025-2. PubMed DOI

Di Marino E (2008) The ectomycorrhizal community structure in beech coppices of different age. PhD Thesis. In Faculty of Biology. Ludwig-Maximilians-universität München, München, Germany

Dick W. Organic carbon, nitrogen, and phosphorus concentrations and pH in soil profiles as affected by tillage intensity. Soil Sci Soc Am J. 1983;47:102–107. doi: 10.2136/sssaj1983.03615995004700010021x. DOI

Dighton J. Phosphatase production by mycorrhizal fungi. Plant Soil. 1983;71:455–462. doi: 10.1007/BF02182686. DOI

Dodd J, Burton C, Burns R, Jeffries P. Phosphatase activity associated with the roots and the rhizosphere of plants infected with vesicular-arbuscular mycorrhizal fungi. New Phytol. 1987;107:163–172. doi: 10.1111/j.1469-8137.1987.tb04890.x. DOI

Fransson PM, Taylor AF, Finlay RD. Effects of continuous optimal fertilization on belowground ectomycorrhizal community structure in a Norway spruce forest. Tree Physiol. 2000;20:599–606. doi: 10.1093/treephys/20.9.599. PubMed DOI

Gardes M, Bruns T. Community structure of ectomycorrhizal fungi in a Pinus muricata forest: above-and below-ground views. Can J Bot. 1996;74:1572–1583. doi: 10.1139/b96-190. DOI

German DP, Weintraub MN, Grandy AS, Lauber CL, Rinkes ZL, Allison SD. Optimization of hydrolytic and oxidative enzyme methods for ecosystem studies. Soil Biol Biochem. 2011;43:1387–1397. doi: 10.1016/j.soilbio.2011.03.017. DOI

Gregorich E, Monreal C, Carter M, Angers D, Ellert B. Towards a minimum data set to assess soil organic matter quality in agricultural soils. Can J Soil Sci. 1994;74:367–385. doi: 10.4141/cjss94-051. DOI

Grogan P, Baar J, Bruns T. Below-ground ectomycorrhizal community structure in a recently burned bishop pine forest. J Ecol. 2000;88:1051–1062. doi: 10.1046/j.1365-2745.2000.00511.x. DOI

Harsch MA, Bader MY. Treeline form–a potential key to understanding treeline dynamics. Glob Ecol Biogeogr. 2011;20:582–596. doi: 10.1111/j.1466-8238.2010.00622.x. DOI

Haselwandter K. Mycorrhizal infection and its possible ecological significance in climatically and nutritionally stressed alpine plant communities. Angew Bot. 1987;61:107–114.

Haselwandter K. Trees at their upper limit. The Netherlands: Springer; 2007. Mycorrhiza in the alpine timberline ecotone: nutritional implications; pp. 57–66.

Ho I, Zak B. Acid phosphatase activity of six ectomycorrhizal fungi. Can J Bot. 1979;57:1203–1205. doi: 10.1139/b79-144. DOI

Holtmeier K, Broll G. Altitudinal and polar treelines in the northern hemisphere causes and response to climate change (Obere und polare Baumgrenze auf der nördlichen Hemisphäre Ursachen und Antwort auf den Klimawandel) Polarforschung. 2010;79:139–153.

Johnson D, IJdo M, Genney DR, Anderson IC, Alexander IJ. How do plants regulate the function, community structure, and diversity of mycorrhizal fungi? J Exp Bot. 2005;56:1751–1760. doi: 10.1093/jxb/eri192. PubMed DOI

Jones MD, Twieg BD, Ward V, Barker J, Durall DM, Simard SW. Functional complementarity of Douglas-fir ectomycorrhizas for extracellular enzyme activity after wildfire or clearcut logging. Funct Ecol. 2010;24:1139–1151. doi: 10.1111/j.1365-2435.2010.01699.x. DOI

Kainulainen P, Holopainen J, Palomäki V, Holopainen T. Effects of nitrogen fertilization on secondary chemistry and ectomycorrhizal state of scots pine seedlings and on growth of grey pine aphid. J Chem Ecol. 1996;22:617–636. doi: 10.1007/BF02033574. PubMed DOI

Kaiser C, Koranda M, Kitzler B, Fuchslueger L, Schnecker J, Schweiger P, Rasche F, Zechmeister-Boltenstern S, Sessitsch A, Richter A. Belowground carbon allocation by trees drives seasonal patterns of extracellular enzyme activities by altering microbial community composition in a beech forest soil. New Phytol. 2010;187:843–858. doi: 10.1111/j.1469-8137.2010.03321.x. PubMed DOI PMC

Ken K, William JS. Enzymes in the environment. New York: CRC Press; 2002. Bioindicators and sensors of soil health and the application of Geostatistics; pp. 391–394.

Kerley SJ, Read DJ. The biology of mycorrhiza in the Ericaceae. XX. Plant and mycorrhizal necromass as nitrogenous substrates for the ericoid mycorrhizal fungus Hymenoscyphus ericae and its host. New Phytol. 1998;139:353–360. doi: 10.1046/j.1469-8137.1998.00189.x. PubMed DOI

Kernaghan G, Harper K. Community structure of ectomycorrhizal fungi across an alpine/subalpine ecotone. Ecography. 2001;24:181–188. doi: 10.1034/j.1600-0587.2001.240208.x. DOI

Kernaghan G, Widden P, Bergeron Y, Légaré S, Paré D. Biotic and abiotic factors affecting ectomycorrhizal diversity in boreal mixed-woods. Oikos. 2003;102:497–504. doi: 10.1034/j.1600-0706.2003.12415.x. DOI

Keuskamp JA, Dingemans BJ, Lehtinen T, Sarneel JM, Hefting MM. Tea bag index: a novel approach to collect uniform decomposition data across ecosystems. Methods Ecol Evol. 2013;4:1070–1075. doi: 10.1111/2041-210X.12097. DOI

Leake J, Read D. Proteinase activity in mycorrhizal fungi. New Phytol. 1990;115:243–250. doi: 10.1111/j.1469-8137.1990.tb00449.x. PubMed DOI

Leake J, Read D. The mycota IV environmental and microbial relationships. Berlin: Springer; 1997. Mycorrhizal fungi in terrestrial habitats; pp. 281–301.

Leake J, Donnelly D, Saunders E, Boddy L, Read D. Rates and quantities of carbon flux to ectomycorrhizal mycelium following 14C pulse labeling of Pinus sylvestris seedlings: effects of litter patches and interaction with a wood-decomposer fungus. Tree Physiol. 2001;21:71–82. doi: 10.1093/treephys/21.2-3.71. PubMed DOI

Lindahl BD, Ihrmark K, Boberg J, Trumbore SE, Högberg P, Stenlid J, Finlay RD. Spatial separation of litter decomposition and mycorrhizal nitrogen uptake in a boreal forest. New Phytol. 2007;173:611–620. doi: 10.1111/j.1469-8137.2006.01936.x. PubMed DOI

Lodge D. The influence of soil moisture and flooding on formation of VA-endo-and ectomycorrhizae in Populus and Salix. Plant Soil. 1989;117:243–253. doi: 10.1007/BF02220718. DOI

Mason P, Last F, Pelham J, Ingleby K. Ecology of some fungi associated with an ageing stand of birches (Betula pendula and B. pubescens) Forest Ecol Manag. 1982;4:19–39. doi: 10.1016/0378-1127(82)90026-3. DOI

Mason P, Wilson J, Last F, Walker C. The concept of succession in relation to the spread of sheathing mycorrhizal fungi on inoculated tree seedlings growing in unsterile soils. Plant Soil. 1983;71:247–256. doi: 10.1007/BF02182659. DOI

Massicotte HB, Molina R, Luoma DL, Smith JE. Biology of the ectomycorrhizal genus, Rhizopogon. II. Patterns of host-fungus specificity following spore inoculation of diverse hosts grown in monoculture and dual culture. New Phytol. 1994;126:677–690. doi: 10.1111/j.1469-8137.1994.tb02962.x. DOI

Moser M. Die ektotrophe Ernährungsweise an der Waldgrenze. Mitt Forstl Bundes-Versanst Wien. 1967;75:357–380.

Moser M. Arctic and alpine mycology. Seattle: University of Washington press; 1982. Mycoflora of the transitional zone from subalpine forests to alpine tundra; pp. 371–384.

Parrent JL, Morris WF, Vilgalys R. CO2-enrichment and nutrient availability alter ectomycorrhizal fungal communities. Ecology. 2006;87:2278–2287. doi: 10.1890/0012-9658(2006)87[2278:CANAAE]2.0.CO;2. PubMed DOI

Peay KG, Kennedy PG, Bruns TD. Rethinking ectomycorrhizal succession: are root density and hyphal exploration types drivers of spatial and temporal zonation? Fungal Ecol. 2011;4:233–240. doi: 10.1016/j.funeco.2010.09.010. DOI

Phuyal M, Artz RR, Sheppard L, Leith ID, Johnson D. Long-term nitrogen deposition increases phosphorus limitation of bryophytes in an ombrotrophic bog. Plant Ecol. 2008;196:111–121. doi: 10.1007/s11258-007-9338-1. DOI

Pritsch K, Garbaye J. Enzyme secretion by ECM fungi and exploitation of mineral nutrients from soil organic matter. Ann For Sci. 2011;68:25–32. doi: 10.1007/s13595-010-0004-8. DOI

Read DJ, Leake JR, Perez-Moreno J. Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Can J Bot. 2004;82:1243–1263. doi: 10.1139/b04-123. DOI

Schimel JP, Weintraub MN. The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model. Soil Biol Biochem. 2003;35:549–563. doi: 10.1016/S0038-0717(03)00015-4. DOI

Sinsabaugh R, Moorhead D. Resource allocation to extracellular enzyme production: a model for nitrogen and phosphorus control of litter decomposition. Soil Biol Biochem. 1994;26:1305–1311. doi: 10.1016/0038-0717(94)90211-9. DOI

Stevenson TM, Kazmierczak F, Leonard NJ. Defined dimensional alterations in enzyme substrates. General synthetic methodology for the bent dihydro-lin-benzopurines. J Organomet Chem. 1986;51:616–620. doi: 10.1021/jo00355a009. DOI

Tabatabai MA, Dick WA. Enzymes in the environment: activity, ecology and applications. New York: Marcel Dekker; 2002. Enzymes in soil; pp. 567–596.

Voříšková J, Brabcová V, Cajthaml T, Baldrian P. Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytol. 2014;201:269–278. doi: 10.1111/nph.12481. PubMed DOI

Wallenstein MD, McMahon SK, Schimel JP. Seasonal variation in enzyme activities and temperature sensitivities in Arctic tundra soils. Glob Chang Biol. 2009;15:1631–1639. doi: 10.1111/j.1365-2486.2008.01819.x. DOI

Wurzburger N, Hendrick RL. Rhododendron thickets alter N cycling and soil extracellular enzyme activities in southern Appalachian hardwood forests. Pedobiologia. 2007;50:563–576. doi: 10.1016/j.pedobi.2006.10.001. DOI