Abstract
Environmental stress affects ectomycorrhizal communities (ECM), but it is not known how general the detected ECM responses are. We investigated ECM fungi on roots of mountain birch, Betula pubescens subsp. czerepanovii (Orlova) Hämet-Ahti, along three environmental gradients, two natural (altitude, seashore) and one human-induced (pollution), within the Kola Peninsula, NW Russia. Chlorophyll fluorescence of birch leaves indicated no environmental stress even in the conditions that were presumed most stressful in terms of abiotic environment, where the biomass and population density of birches were strongly reduced. Although neither overall ECM colonisation nor root fungal biomass showed stress-related patterns, colonisation by Cenococcum geophilum tended to decrease with abiotic stress. ECM morphotype diversity declined with abiotic stress, and along altitudinal gradient this decline was related to an increase in proportion of morphotypes with high fungal biomass. Polycormic birches had higher ECM colonisation than monocormic birches at high stress sites only. ECM morphotype diversity increased with foliar nitrogen concentration at low stress sites, but not at high stress sites. Birches with higher chlorophyll fluorescence had lower chitin concentration in their roots (indicating lower proportion of fungal structures) at high stress sites only. Our results suggest that at high stress sites (1) mechanical shelter created by polycormic trees may favour ECM fungi and (2) mountain birches maintain lower ECM diversity than at low stress sites.
Similar content being viewed by others
References
Adams, W. W., Winter, K., & Lanzl, A. (1989). Light and the maintenance of photosynthetic competence in leaves of Populus balsamifera L. during short-term exposures to high concentrations of sulfur dioxide. Planta, 177, 91–97.
Agerer, R. (1987). Colour atlas of ectomycorrhizae. Schwäbisch Gmünd: Einhorn.
Agerer, R. (2001). Exploration types of ectomycorrhizae. Mycorrhiza, 11, 107–114.
Andersen, C. P., & Rygiewicz, P. T. (1991). Stress interactions and mycorrhizal plant response: Understanding carbon allocation priorities. Environmental Pollution, 73, 217–244.
Bakker, M. R., Augusto, L., & Achat, D. L. (2006). Fine root distribution of trees and understory in mature stands of maritime pine (Pinus pinaster) on dry and humid sites. Plant and Soil, 286, 37–51.
Bougher, N. L., Grove, T. S., & Malajczuk, N. (1990). Growth and phosphorus acquisition of karri (Eucalyptus diversicolor F. Muell.) seedlings inoculated with ectomycorrhizal fungi in relation to phosphorus supply. New Phytologist, 114, 77–85.
Cairney, J. W. G., & Meharg, A. A. (1999). Influences of anthropogenic pollution on mycorrhizal fungal communities. Environmental Pollution, 106, 169–182.
Coleman, M. D., Bledsoe, C. S., & Lopushinsky, W. (1989). Pure culture response of ectomycorrhizal fungi to imposed water stress. Canadian Journal of Botany, 67, 29–39.
Couteaux, M. M., Sarmiento, L., Bottner, P., Avecedo, D., & Thiery, J. M. (2002). Decomposition of standard plant material along an altitudinal transect (65–3968 m) in the tropical Andes. Soil Biology and Biochemistry, 34, 69–78.
Douhan, G. W., & Rizzo, D. M. (2005). Phylogenetic divergence in a local population of the ectomycorrhizal fungus Cenococcum geophilum. New Phytologist, 166, 263–271.
Eissenstat, D. M., Wells, C. E., Yanai, R. D., & Whitbeck, J. L. (2000). Building roots in a changing environment: implications for root longevity. New Phytologist, 147, 33–42.
Ekblad, A., Wallander, H., & Näsholm, T. (1998). Chitin and ergosterol combined to measure total and living fungal biomass in ectomycorrhizas. New Phytologist, 138, 143–149.
Eränen, J. K., & Kozlov, M. V. (2007). Competition and facilitation in industrial barrens: Variation in performance of mountain birch seedlings with distance from nurse plants. Chemosphere, 67, 1088–1095.
Erland, S., & Taylor, A. F. S. (2002). Diversity of ectomycorrhizal fungal communities in relation to the abiotic environment. In M. G. A. Van der Heijden, & I. R. Sanders (Eds.) Mycorrhizal ecology (pp. 163–200). Berlin: Springer.
Ermakov, V. I. (1981). Functional importance of sinuosity of main stems in northern birches. In A. D. Volkov, V. I. Ermakov, G. M. Kozubov, Y. E. Novitskaya, M. A. Tikhova, M. A. Stcherbakova, & A. A. Yatsenko-Khmelevskij (Eds.) All-Union Conference of problems of woody plant adaptations to extremal environmental conditions. Abstracts of presentations (pp. 33–36). Petrozavodsk: Forest Institute (in Russian).
Gehring, C. A., & Whitham, T. G. (1994). Interactions between aboveground herbivores and the mycorrhizal mutualists of plants. Trends in Ecology and Evolution, 9, 251–255.
Gehring, C. A., & Whitham, T. G. (2002). Mycorrhizae-herbivore interactions: Population and community consequences. In M. G. A. Van der Heijden, & I. R. Sanders (Eds.) Mycorrhizal ecology (pp. 295–320). Berlin: Springer.
Godbold, D. L., & Berntson, G. M. (1997). Elevated atmospheric CO2 concentration changes ectomycorrhizal morphotype assemblage in Betula papyrifera. Tree Physiology, 17, 347–350.
Godbold, D. L., Jentschke, G., Winter, K., & Marschner, P. (1998). Ectomycorrhizas and amelioration of metal stress in forest trees. Chemosphere, 36, 757–762.
Gorissen, A., & Kuyper, Th. W. (2000). Fungal species-specific responses of ectomycorrhizal Scots pine (Pinus sylvestris) to elevated [CO2]. New Phytologist, 146, 163–168.
Herold, A. (1980). Regulation of photosynthesis by sink activity—the missing link. New Phytologist, 86, 131–144.
Hoch, G., Popp, M., & Körner, C. (2002). Altitudinal increase of mobile carbon pools in Pinus cembra suggests sink limitation of growth at the Swiss treeline. Oikos, 98, 361–374.
Holopainen, T., Heinonen-Tanski, H., & Halonen, A. (1996). Injuries to Scots pine mycorrhizas and chemical gradients in forest soil in the environment of a pulp mill in Central Finland. Water Air and Soil Pollution, 87, 111–130.
Högberg, M. N., & Högberg, P. (2002). Extramatrical ectomycorrhizal mycelium contributes one-third of microbial biomass and produces, together with associated roots, half the dissolved carbon in a forest soil. New Phytologist, 54, 791–795.
Jany, J. L., Garbaye, J., & Martin, F. (2002). Cenococcum geophilum populations show a high degree of genetic diversity in beech forests. New Phytologist, 154, 651–659.
Jentschke, G., Fritz, E., & Godbold, D. L. (1991). Distribution of lead in mycorrhizal and non-mycorrhizal Norway-spruce seedlings. Physiologia Plantarum, 81, 417–422.
Johnson, B. N., & McGill, W. B. (1990). Comparison of ergosterol and chitin as quantitative estimates of mycorrhizal infection and Pinus contorta seedling response to inoculation. Canadian Journal of Forest Research, 20, 1125–1131.
Jones, M. D., Durall, D. M., & Cairney, J. W. G. (2003). Ectomycorrhizal fungal communities in young forest stands regenerating after clearcut logging. New Phytologist, 157, 399–422.
Jones, M. D., Durall, D. M., & Tinker, P. B. (1991). Fluxes of carbon and phosphorus between symbionts in willow ectomycorrhizas and their changes with time. New Phytologist, 119, 99–106.
Jones, M. D., & Hutchinson, T. C. (1986). The effect of mycorrhizal infection on the response of Betula papyrifera to nickel and copper. New Phytologist, 102, 429–442.
Kernaghan, G. (2001). Ectomycorrhizal fungi at tree line in the Canadian Rockies II. Identification of ectomycorrhizae by anatomy and PCR. Mycorrhiza, 10, 217–229.
Kielisziewska-Rokicka, B., Rudawska, M., & Leski, T. (1997). Ectomycorrhiza of young and mature Scots pine trees in industrial regions in Poland. Environmental Pollution, 98A, 315–324.
Kitao, M., Lei, T. T., & Koike, T. (1997). Effects of manganese toxicity on photosynthesis of white birch (Betula platyphylla var. japonica) seedlings. Physiologia Plantarum, 101, 249–256.
Klironomos, J. N., & Allen, M. F. (1995). UV-B-mediated changes on below-ground communities associated with the roots of Acer saccharum. Functional Ecology, 9, 923–930.
Kozlov, M. V. (2004). Leaf fall in white birch (Betula pubescens) is independent of leaf asymmetry. Canadian Journal of Botany, 82, 910–913.
Kozlov, M. V. (2005). Pollution resistance of mountain birch, Betula pubescens subsp. czerepanovii, near the copper-nickel smelter: Natural selection or phenotypic acclimation? Chemosphere, 59, 189–197.
Kozlov, M. V., Haukioja, E., Bakhtiarov, A. V., Stroganov, D. N., & Zimina, S. N. (2000). Root vs. canopy uptake of heavy metals by birch in an industrially polluted area: Contrasting behaviour of nickel and copper. Environmental Pollution, 107, 413–420.
Körner, C. (2003). Alpine plant life. Berlin: Springer.
Kraigher, H., Batic, F., & Agerer, R. (1996). Types of ectomycorrhizae and mycobioindication of forest site pollution. Phyton (Horn, Austria), 36, 115–120.
Kuikka, K., Härmä, E., Markkola, A., Rautio, P., Roitto, M., Saikkonen, K., et al. (2003). Severe defoliation of Scots pine reduces reproductive investment by ectomycorrhizal symbionts. Ecology, 84, 2051–2061.
Lamhamedi, M. S., Godbout, C., & Fortin, J. A. (1994). Dependence of Laccaria bicolor basidiome development on current photosynthesis of Pinus strobus seedlings. Canadian Journal of Forest Research, 24, 1798–1804.
Langley, J. A., Chapman, S. K., & Hungate, B. A. (2006). Ectomycorrhizal colonization slows root decomposition: the post-mortem fungal legacy. Ecological Letters, 9, 955–959.
Larcher, W. (1995). Physiological plant ecology: Ecophysiology and stress physiology of functional groups. Berlin: Springer.
Last, F. T., Pelham, J., Mason, P. A., & Ingleby, K. (1979). Influence of leaves on sporophore production by forming sheathing mycorrhizas with Betula spp. Nature, 280, 168–169.
Lilleskov, E. A., Fahey, T. J., Horton, T. R., & Lovett, G. M. (2002). Belowground ectomycorrhizal fungal community change over a nitrogen deposition gradient in Alaska. Ecology, 83, 104–115.
Markkola, A., Kuikka, K., Rautio, P., Härmä, E., Roitto, M., & Tuomi, J. (2004). Defoliation increases carbon limitation in ectomycorrhizal symbiosis of Betula pubescens. Oecologia, 140, 234–240.
McEnroe, N. A., & Helmisaari, H.-S. (2001). Decomposition of coniferous forest litter along a heavy metal pollution gradient, south-west Finland. Environmental Pollution, 113, 11–18.
Meyer, F. H. (1987). Extreme Standorte und Ektomykorrhiza (insbesondere Cenococcum geophilum). Angewandte Botanik, 61, 39–46.
Muhsin, T. M., & Zwiazek, J. J. (2002). Colonisation with Hebeloma crustuliniforme increases water conductance and limits shoot sodium uptake in white spruce (Picea glauca) seedlings. Plant and Soil, 238, 217–225.
Northup, R. R., Zengshou, Y., Dahlgren, R. A., & Vogt, K. A. (1995). Polyphenol control of nitrogen release from pine litter. Nature, 377, 227–229.
Öquist, G., & Wass, R. (1988). A portable, microprocessor operated instrument for measuring chlorophyll fluorescence kinetics in stress physiology. Physiologia Plantarum, 73, 211–217.
Parke, J. L., Lindeman, R. G., & Black, C. H. (1983). The role of ectomycorrhizas in drought tolerance of Douglas- fir seedlings. New Phytologist, 25, 83–95.
Pigott, C. D. (1982). Survival of mycorrhiza formed by Cenococcum geophilum Fr. in dry soils. New Phytologist, 92, 513–517.
Rigina, O., & Kozlov, M. V. (1999). The impacts of air pollution on the northern taiga forests of the Kola peninsula, Russian Federation. In L. Innes, & J. Oleksyn (Eds.) Forest dynamics in heavily polluted regions (pp. 37–65). Wallingford: CAB International.
Ruotsalainen, A. L., & Kozlov, M. V. (2007). Fungi and air pollution—is there a general pattern? In D. Rhodes (Ed.) New topics in environmental research (pp. 57–103). New York, Hauppage: Nova Science.
Rygiewicz, P. T., & Andersen, C. P. (1994). Mycorrhizae alter quality and quantity of carbon allocated belowground. Nature, 369, 58–60.
Saikkonen, K., Ahonen-Jonnarth, U., Markkola, A., Helander, M., Tuomi, J., Roitto, M., et al. (1999). Defoliation and mycorrhizal symbiosis: A functional balance between carbon sources and below-ground sinks. Ecological Letters, 2, 19–26.
Saleh-Rastin, N. (1976). Salt tolerance of the mycorrhizal fungus Cenococcum graniforme (Sow.) Ferd. European Journal of Forest Pathology, 6, 184–187.
SAS Institute (1990). SAS/Stat. User’s guide, Version 6.0. SAS Institute, Cary, NC.
Setälä, H., Rissanen, J., & Markkola, A. M. (1997). Conditional outcomes in the relationship between pine and ectomycorrhizal fungi in relation to biotic and abiotic environment. Oikos, 80, 112–122.
Smith, S. E., & Read, D. J. (1997). Mycorrhizal symbiosis. London: Academic.
Tarvainen, O., Markkola, A., Ahonen-Jonnarth, U., Jumpponen, A., & Strömmer, R. (2004). Changes in ectomycorrhizal colonisation and root peroxidase activity in Pinus sylvestris seedlings planted in forest humus. Scandinavian Journal of Forest Research, 19, 400–408.
Tuomi, J., Kytöviita, M.-M., & Härdling, R. (2001). Cost efficiency of nutrient acquisition and the advantage of mycorrhizal symbiosis for the host plant. Oikos, 92, 62–70.
Valkama, J., & Kozlov, M. V. (2001). Impact of climatic factors on the developmental stability of mountain birch growing in a contaminated area. Journal of Applied Ecology, 38, 665–673.
Vrålstad, T., Holst-Jensen, A., & Schumacher, T. (1998). The postfire discomycete Geopyxis carbonaria (Ascomycota) is a biotrophic root associate with Norway spruce (Picea abies) in nature. Molecular Ecology, 7, 609–616.
Wieckowska, E. (1968). Determination of chitin in mushrooms. Mikologia Stosowana, 1, 65–71 (in Polish).
Zvereva, E. L., & Kozlov, M. V. (2007). Facilitation of bilberry by mountain birch in habitat severely disturbed by pollution: Importance of sheltering. Environ Experimental Botany, 60, 170–176.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Ruotsalainen, A.L., Markkola, A.M. & Kozlov, M.V. Mycorrhizal colonisation of mountain birch (Betula pubescens ssp. czerepanovii) along three environmental gradients: does life in harsh environments alter plant-fungal relationships?. Environ Monit Assess 148, 215–232 (2009). https://doi.org/10.1007/s10661-007-0152-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10661-007-0152-y