Skip to main content
Log in

Effect of Ectomycorrhiza on Cu and Pb Accumulation in Leaves and Roots of Silver Birch (Betula pendula Roth.) Seedlings Grown in Metal-Contaminated Soil

  • Published:
Water, Air, and Soil Pollution Aims and scope Submit manuscript

Abstract

A pot experiment was conducted to study the effects of high concentrations of available Cu and Pb in soil originated from the vicinity of a copper foundry in Poland (Cu, 2,585–3,725 mg kg−1 d.wt.; Pb, 1,459–1,812 mg kg−1 d.wt.) on the growth and chemical constituents of Betula pendula seedlings. Control plants grew in unpolluted forest soil. Dry matter accumulation in the plants during the growing season and root/leaf mineral content were determined. Colonization of birch roots by ectomycorrhizal (ECM) fungi also was evaluated, as was soil dehydrogenase activity for influence of the metals on soil microorganisms. The heavy metals negatively affected seedling growth, ECM colonization, and soil dehydrogenase activity. A reverse relationship was found between ECM abundance and heavy metal concentrations in birch leaves, indicating the potential of mycorrhizas to protect the aboveground part of young silver birch seedlings from elevated environmental levels of Cu and Pb.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Agerer, R. (Ed.) (1987–2002). Colour atlas of ectomycorrhizae, first to 12th ed., Schwäbisch Gmünd, Einhorn.

  • Bååth, E. (1989). Effects of heavy metals in soil on microbial processes and populations (a review). Water, Air, and Soil Pollution, 47, 335–379.

    Article  Google Scholar 

  • Bahlsberg-Pahlsson, A. M. (1989). Toxicity of heavy metals (Zn, Cu, Sd, Pb) to vascular plants. Water, Air and Soil Pollution, 47, 287–319.

    Article  Google Scholar 

  • Baker, A. J. M., & Brooks, R. R. (1989). Terrestrial higher plants which hyperaccumulate metallic elements—a review of their distribution, ecology and phytochemistry. Biorecovery, 1, 81–126.

    CAS  Google Scholar 

  • Berthelsen, B. O., Olsen, R. A., & Steinnes, E. (1995). Ectomycorrhizal heavy metal accumulation as a contributing factor to heavy metal levels in organic surface soil. The Science of the Total Environment, 170, 141–149.

    Article  CAS  Google Scholar 

  • Blaudez, D., Botton, B., & Chalot, M. (2000). Effects of heavy metals on nitrogen uptake by Paxillus involutus and mycorrhizal birch seedlings. FEMS Microbiology Ecology, 33, 61–67.

    Article  CAS  Google Scholar 

  • Bojarczuk, K., Oleksyn, J., Kieliszewska-Rokicka, B., Zytkowiak, R., & Tjoelker, M. G. (2002). Effect of polluted soil and fertilisation on growth and physiology of silver birch (Betula pendula Roth.) seedlings. Polish Journal of Environmental Studies, 11, 483–492.

    CAS  Google Scholar 

  • Bojarczuk, K., Oleksyn, J., Karolewski, P., & Zytkowiak, R. (2006). Response of silver birch (Betula pendula Roth.) seedlings to experimental variation in aluminum concentration. Polish Journal of Ecology, 54, 189–200.

    CAS  Google Scholar 

  • Cairney, J. W. G., & Meharg, A. A. (1999). Influences of anthropogenic pollution on mycorrhizal fungal communities. Environmental Pollution, 106, 169–182.

    Article  CAS  Google Scholar 

  • Chaperon, S., & Sauvé, S. (2007). Toxicity interaction of metals (Ag, Cu, Hg, Zn) to urease and dehydrogenase activities in soils. Soil Biology and Biochemistry, 39, 2329–2338.

    Article  CAS  Google Scholar 

  • Cudlin, P., Kieliszewska-Rokicka, B., Rudawska, M., Grebenc, T., Alberton, O., Lehto, T., et al. (2007). Fine roots and ectomycorrhizas as indicators of environmental change. Plant Biosystems, 141(3), 406–425.

    Google Scholar 

  • Denny, H. J., & Wilkins, D. A. (1987). Zinc tolerance in Betula species. I. Effect of external concentrations of zinc on growth and uptake. New Phytologist, 106, 517–524.

    CAS  Google Scholar 

  • Derome, J., & Saarsalmi, A. (1999). The effect of liming and correction fertilisation on heavy metal and macronutrient concentrations in soil solution in heavy-metal polluted scots pine stands. Environmental Pollution, 104, 249–259.

    Article  CAS  Google Scholar 

  • Eltrop, L., Brown, G., Joachim, O., & Brinkmann, K. (1991). Lead tolerance of Betula and Salix in the mining area of Mechernich/Germany. Plant and Soil, 131, 275–285.

    Article  CAS  Google Scholar 

  • Ericksson, T., Rytter, L., & Vapaavuori, E. (1996). Physiology of carbon allocation in trees. Biomass and Bioenergy, 11, 115–127.

    Article  Google Scholar 

  • Fomina, M., Ritz, K., & Gadd, G. M. (2005). Negative fungal chemotropism to toxic metals. FEMS Microbiology Letters, 193, 207–211.

    Article  Google Scholar 

  • Forde, B., & Lorenzo, H. (2001). The nutritional control of root development. Plant and Soil, 232, 51–68.

    Article  CAS  Google Scholar 

  • Foy, S. D., Chaney, R. L., & White, M. C. (1978). The physiology of metal toxicity in plants. Annual Review of Plant Physiology, 29, 511–566.

    Article  CAS  Google Scholar 

  • Gadd, G. M. (1993). Interactions of fungi with toxic metals. New Phytologist, 124, 25–60.

    Article  CAS  Google Scholar 

  • Garcia, C., & Hernandez, T. (1997). Biological and biochemical indicators in derelict soils subject to erosion. Soil Biology and Biochemistry, 29, 171–177.

    Article  CAS  Google Scholar 

  • Godbold, D. L., Jentschke, G., Winter, S., & Marschner, P. (1998). Ectomycorrhizas and amelioration of metal stress in forest trees. Chemosphere, 36, 757–762.

    Article  CAS  Google Scholar 

  • Hartley, J. W., Cairney, G., & Meharg, A. A. (1997). Do ectomycorrhizal fungi exhibit adaptive tolerance to potentially toxic metals in the environment? Plant and Soil, 189, 303–319.

    Article  CAS  Google Scholar 

  • 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 the forest soil. New Phytologist, 54, 791–795.

    Article  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Hytönen, J., Saarsalmi, A., & Rossi, P. (1995). Biomass production and nutrient uptake of short-rotation plantations. Silva Fennica, 29, 17–39.

    Google Scholar 

  • Ingleby, K., Mason, P.A., Last, F.T. & Fleming, L.V. (1990). Identification of ectomycorrhizas. ITE Research, De la Bastide and Kendrick Publication no.5. HMSO, London.

  • Jany, J. L., Garbaye, J., & Martin, F. (2002). Cenococcum geophilum populations show a high degree of genetic diversity in beech forests. New Phytologist, 54, 791–795.

    Google Scholar 

  • Joner, E. J., & Leyval, C. (2003). Rhizosphere gradients of polycyclic aromatic hydrocarbon (PAH) dissipation in two industrial soils, and the impact of arbuscular mycorrhiza. Environmental Science and Technology, 37, 490–502.

    Article  Google Scholar 

  • Kabata-Pendias, A. (1995). Podstawy oceny chemicznego zanieczyszczenia gleb. Metale ciężkie, siarka i WWA. Warszawa: Biblioteka Monitoringu Środowiska, PIOŚ, IUNG.

    Google Scholar 

  • Kabata-Pendias, A., & Pendias, H. (eds). (2001). Trace element in soils and plants (3rd ed.). Boca Raton: CRC.

    Google Scholar 

  • Kashem, M. A., Singh, B. R., Kondo, T., Imamul Hug, S. M., & Kawai, S. (2007). Comparison of extractability of Cd, Cu, Pb and Zn with sequential extraction in contaminated and non-contaminated soils. International Journal of Environmental Science Technology, 4, 169–176.

    CAS  Google Scholar 

  • Kieliszewska-Rokicka, B., Rudawska, M., Leski, T., & Kurczyńska, E. U. (1998). Effect of low pH and aluminium on growth of Pinus sylvestris L. seedlings mycorrhizal with Suillus luteus (L. ex Fr.) S.F. Gray. Chemosphere, 36, 751–756.

    Article  CAS  Google Scholar 

  • Kieliszewska-Rokicka, B., Rudawska, M., Staszewski, T., Kurczyńska, E., Karliński, L., & Kubiesa, P. (2004). Ectomycorrhizal associations in Norway spruce stands influenced by long lasting air pollution (Silesian Mountains, Poland). Ekologia, 23, 142–149.

    Google Scholar 

  • Klink, A., Letachowicz, B., Krawczyk, J., & Wisłocka, M. (2006). The content of heavy metals in soil and silver birch leaves (Betula pendula Roth.) from Wałbrzych and Głogów. Polish Journal Environmental Studies, 15, 347–350.

    Google Scholar 

  • Kloke, A. (1980). Orientierungsdaten für tolerierbare Gesamtgehalte einiger Elemente in Kulturboden. Mitteilungen des Verbandes deutscher landwirtschaftlicher Untersuchungs- und Forschungsanstalten, 1, 9–11.

  • Komosa, A., & Szewczuk, A. (2002). Effect of soil potassium level and different potassium fertilizer forms on nutritional status, growth and yield of apple trees in the first three years after planting. Journal of Fruit and Ornamental Plant Research, 10, 41–54.

    CAS  Google Scholar 

  • Kopponen, P., Utriainen, M., Lukkari, K., Suntioinen, S., Karenlampi, L., & Karenlampi, S. (2001). Clonal differences in copper and zinc tolerance of birch in metal-supplemented soils. Environmental Pollution, 112, 89–97.

    Article  CAS  Google Scholar 

  • Leski, T., Rudawska, M., & Kieliszewska-Rokicka, B. (1995). Intraspecific aluminum response in Suillus luteus (L.) S.F. Gray., an ECM symbiont of Scots Pine. Acta Societatis Botanicorum Poloniae, 64, 97–105.

    Google Scholar 

  • Lindsay, W. L., & Norvell, W. A. (1978). Development of DTPA soil test for zink, iron, manganese, and cooper. Soil Science Society America Journal, 42, 421–428.

    CAS  Google Scholar 

  • Marguí, E., Queralt, I., Carvalho, M. L., & Hidalgo, M. (2007). Assessment of metal availability to vegetation (Betula pendula Roth) in Pb–Zn ore concentrate residues with different features. Environmental Pollution, 145, 179–184.

    Article  Google Scholar 

  • Meharg, A. A., & Cairney, J. W. G. (2000). Ectomycorrhizas—extending the capabilities of rhizosphere remediation? Soil Biology and Biochemistry, 32, 1475–1484.

    Article  CAS  Google Scholar 

  • Meyer, F. H. (1987). Extreme Standorte und Ektomykorrhiza (insbesondere Cenococcum geophilum). Angewandte Botanik, 61, 39–46.

    Google Scholar 

  • Oleksyn, J., Zytkowiak, R., Reich, P. B., Tjoelker, M. G., & Karolewski, P. (2000). Ontogenic patterns of leaf CO2 exchange, morphology and chemistry in Betula pendula trees. Trees, 14, 271–281.

    Article  Google Scholar 

  • Page, B. D., & Mitchel, M. J. (2008). Influence of a calcium gradient on soil inorganic nitrogen in the Adirondack mountains, New York. Ecological Applications, 18, 1604–1614.

    Article  Google Scholar 

  • Pennanen, T., Frostegard, A., Fritze, H., & Bååth, E. (1996). Phospolipid fatty acid composition and heavy metal tolerance of soil microbial communities along two heavy metal-polluted gradients in coniferous forests. Applied and Environmental Microbiology, 62, 420–428.

    CAS  Google Scholar 

  • Perez-Moreno, J., & Read, D. J. (2000). Mobilization and transfer of nutrients from litter to tree seedlings via vegetative mycelium of ectomycorrhizal plants. New Phytologist, 145, 301–309.

    Article  CAS  Google Scholar 

  • Perucci, P. (1992). Enzyme activity and microbial biomass in afield soil amended with municipal refuse. Biology and Fertility of Soils, 14, 54–60.

    Article  CAS  Google Scholar 

  • Prach, K., & Pyšek, P. (2001). Using spontaneous succession for restoration of human-disturbed habitats: Experience for central Europe. Ecological Engineering, 17, 55–62.

    Article  Google Scholar 

  • Pulford, I. D., & Dickinson, N. M. (2005). Phytoremediation technologies using trees. In M. N. V. Prasad, K. S. Sajwan & R. Naidu (Eds.), Trace elements in the environment (pp. 383–403). Boca Raton: Taylor and Francis.

    Google Scholar 

  • Regvar, M., Vogel-Mikuš, K., Kugonič, N., Turk, B., & Baltič, F. (2006). Vegetational and mycorrhizal successions at a metal polluted site: Indications for the direction of phytostabilisation? Environmental Pollution, 144, 976–984.

    Article  CAS  Google Scholar 

  • Rossel, D., Tarradellas, J., Bitton, G., & Morel, J. L. (1997). Use of enzymes in ecotoxicology: A case for dehydrogenase and hydrolytic enzymes. In J. Tarradellas, G. Bitton & D. Rossel (Eds.), Soil ecotoxicology (1st ed., pp. 179–192). Boca Raton: CRC Lewis.

    Google Scholar 

  • Rosselli, W., Keller, C., & Boschi, K. (2003). Phytoextraction capacity of trees growing on a metal contaminated soil. Plant and Soil, 256(265), 2003.

    Google Scholar 

  • Rudawska, M., & Leski, T. (2005). Trace elements in fruiting bodies of ectomycorrhizal fungi growing in Scots pine (Pinus sylvestris L.) stands in Poland. Science of the Total Environment, 339, 103–115.

    Article  CAS  Google Scholar 

  • Ruotsalainen, A. L., Markkola, A. M., & Kozlov, M. V. (2009). Mycorrhizal colonization of mountain birch (Betula pubescens ssp. czerepanovii) along three environmental gradients: Does life in harsh environments alter plant–fungal relationships? Environmental Monitoring Assessment, 148, 215–232.

    Article  CAS  Google Scholar 

  • Saarsalmi, A. (1995). Nutrition of deciduous tree species grown in short rotation stands. Academic dissertation, University of Joensuu, Finland, 60 p

  • Simon, E. (1978). Heavy metals in soil, vegetation development and heavy metal tolerance in plant populations from metaliferous areas. New Phytologist, 81, 175–188.

    Article  CAS  Google Scholar 

  • Smith, S. E., & Read, D. J. (1997). Mycorrhizal symbiosis (2nd ed.). New York: Academic.

    Google Scholar 

  • Susarla, S., Medina, V. F., & McCutcheon, S. C. (2002). Phytoremediation: An ecological solution to organic chemical contamination. Ecological Engineering, 18, 647–658.

    Article  Google Scholar 

  • Staudenrausch, S., Kaldorf, M., Renker, C., & Luis, P. (2005). Diversity of ectomycorrhizal community at a uranium mining heap. Biology and Fertility of Soils, 41, 439–446.

    Article  Google Scholar 

  • Szarek-Łukaszewska, G., & Grodzińska, K. (2007). Vegetation of a post-mining open pit (Zn/Pb ores): Three-year study of colonization. Polish Journal of Ecology, 55, 261–282.

    Google Scholar 

  • Von Thalmann, A. (1968). Zur Bestimmung der Dehydrogenaseaktivitat im Boden mittels Triphenyltetrazoliumchlorid (TTC). Landwirtschaftliche Forschung, 21, 249.

    CAS  Google Scholar 

  • Tickle, A., Fergusson, M., & Drucker, G. (1995). Acid rain and nature conservation in Europe. A preliminary study of protected areas at risk from acidification. Gland: WWF International. 96 p.

    Google Scholar 

  • Trevors, J. T. (1984). Dehydrogenase activity in soil. A comparison between the INT and TTC assay. Soil Biology and Biochemistry, 16, 673–674.

    Article  CAS  Google Scholar 

  • Turnau, K., Mleczko, P., Blaudez, D., Chalot, M., & Botton, B. (2002). Heavy metal bounding properties of Pinus sylvestris mycorrhizas from industrial wastes. Acta Societatis Botanicorum Poloniae, 71, 253–261.

    CAS  Google Scholar 

  • Tyler, G. (1978). Leaching rates of heavy metal ions in forest soil. Water Air Soil Pollution, 9, 137–148.

    Article  CAS  Google Scholar 

  • Van Tichelen, K. K., Colpaert, J. V., & Vangronsveld, J. (2001). Ectomycorrhizal protection of Pinus sylvestris against copper toxicity. New Phytologist, 150, 203–213.

    Article  Google Scholar 

  • Wilkinson, D. M., & Dickinson, N. M. (1995). Metal resistance in trees: The role of mycorrhizae. Oikos, 72, 298–300.

    Article  Google Scholar 

Download references

Acknowledgments

This work was financially supported by Ministry of Science and Higher Education (grant no. NN 309 29 65 34) and by Institute of Dendrology (statutory project).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Barbara Kieliszewska-Rokicka.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bojarczuk, K., Kieliszewska-Rokicka, B. Effect of Ectomycorrhiza on Cu and Pb Accumulation in Leaves and Roots of Silver Birch (Betula pendula Roth.) Seedlings Grown in Metal-Contaminated Soil. Water Air Soil Pollut 207, 227–240 (2010). https://doi.org/10.1007/s11270-009-0131-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11270-009-0131-8

Keywords

Navigation