Skip to main content
Log in

The Significance of Ectomycorrhizas in Chemical Quality of Silver Birch Foliage and Above-Ground Insect Herbivore Performance

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

We tested whether the ectomycorrhizal (ECM) infection level of roots of silver birch (Betula pendula) affects performance of above-ground insect herbivores by increasing available plant biomass, by enhancing availability of nutrients, or by modifying concentration of defense compounds, i.e., phenolics, in birch foliage. Insect performance was determined for a phloem-feeding generalist (Lygus rugulipennis, the European tarnished plant bug), a phloem-feeding specialist (Calaphis flava, the birch aphid), and a chewing generalist (Epirrita autumnata, the autumnal moth larva). Silver birch plantlets had either natural ECM infection level (on average 24% of short roots with ECM), reduced ECM infection level with fungicide (F−, 9% ECM), or enhanced ECM infection level after inoculation with the fungus Paxillus involutus (PI+, 45% ECM) or Leccinum versipelle (LV+, 42% ECM). In general, the most pronounced effect of ECM was observed on growth of plantlets, i.e., stem growth decreased. In PI+-treated plants, leaf biomass also decreased. The effect of mycorrhizal colonization on the host plant’s nitrogen (N) and phosphorous (P) concentration was dependent on the mycorrhizal species and experiment. Fungicide treatment did not cause a consistent decrease in nutrients. Finally, defense of birch against herbivory, expressed as foliar phenolic concentration in plantlets, was not modified by ECM. However, E. autumnata had a significantly higher relative growth rate on PI+ plantlets with high leaf N concentration than on LV+ plantlets with low leaf N concentration. The birch aphid C. flava produced significantly less nymphs on birches with enhanced ECM infection levels (PI+ and LV+ plantlets) than on controls. In summary, our data show that the ECM infection level mainly affects the growth parameters of plantlets, whereas effects on leaf chemical quality are minor. Our data show that effects of ECM infection of birch roots on aboveground herbivores are multifaceted and depend on the fungal species forming ectomycorrhiza and also on the degree of specialization and feeding guild of insects.

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.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Allen, S. E. 1989. Chemical Analysis of Ecological Materials. Blackwell, Oxford.

    Google Scholar 

  • Bennett, A. E., Alers-Garcia, J., and Bever, J. D. 2006. Three-way interactions among mutualistic mycorrhizal fungi, plants, and plant enemies: hypotheses and synthesis. Am. Nat. 167:141–152.

    Article  PubMed  Google Scholar 

  • Bennett, A. E., and Bever, J. D. 2007. Mycorrhizal species differentially alter plant growth and response to herbivory. Ecology 88:210–218.

    Article  PubMed  Google Scholar 

  • Bezemer, T. M., and Van Dam, N. M. 2005. Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol. Evol. 20:617–624.

    Article  PubMed  Google Scholar 

  • Blaudez, D., Chalot, M., Dizengremel, P., and Botton, B. 1998. Structure and function of the ectomycorrhizal association between Paxillus involutus and Betula pendula - II. Metabolic changes during mycorrhiza formation. New Phytol. 138:543–552.

    Article  CAS  Google Scholar 

  • Borowicz, V. A. 1997. A fungal root symbiont modifies plant resistance to an insect herbivore. Oecologia 112:534–542.

    Article  Google Scholar 

  • Corrêa, A., Strasser, R. J., and Martins-Loução, M. A. 2006. Are mycorrhiza always beneficial? Plant Soil 279:65–73.

    Article  CAS  Google Scholar 

  • Daughtridge, A. D., Boese, S. R., Pallardy, S. G., and Garrett, H. E. 1986. A rapid staining technique for assessment of ectomycorrhizal infection of oak roots. Can. J. Bot. 64:1101–1103.

    Article  Google Scholar 

  • Day, K. R., Armour, H., and Docherty, M. 2004. Population responses of a conifer-dwelling aphid to seasonal changes in its host. Ecol. Entomol. 29:555–565.

    Article  Google Scholar 

  • Gange, A. C. 2001. Species-specific responses of a root- and shoot-feeding insect to arbuscular mycorrhizal colonization of its host plant. New Phytol. 150:611–618.

    Article  Google Scholar 

  • Gange, A. C., and West, H. M. 1994. Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol. 128:79–87.

    Article  Google Scholar 

  • Gange, A. C., Stagg, P. G., and Ward, L. K. 2002. Arbuscular mycorrhizal fungi affect phytophagous insect specialism. Ecol. Lett. 5:11–15.

    Article  Google Scholar 

  • Gange, A. C., Brown, V. K., and Aplin, D. M. 2005a. Ecological specificity of arbuscular mycorrhizae: evidence from foliar- and seed-feeding insects. Ecology 86:603–611.

    Article  Google Scholar 

  • Gange, A. C., Gane, D. R. J., Chen, Y. L., and Gong, M. Q. 2005b. Dual colonization of Eucalyptus urophylla ST Blake by arbuscular and ectomycorrhizal fungi affects levels of insect herbivore attack. Agric. For. Entomol. 7:253–263.

    Article  Google Scholar 

  • Gehring, C. A., Cobb, N. S., and Whitham, T. G. 1997. Three-way interactions among ectomycorrhizal mutualists, scale insects and resistant and susceptible pinyon pines. Am. Nat. 149:824–841.

    Article  PubMed  CAS  Google Scholar 

  • Harborne, J. B. 1991. Flavonoid pigments, pp. 389–429, in G.A. Rosenthal, and M.R. Berenbaum (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites. Academic Press, New York.

    Google Scholar 

  • Holopainen, J. K., Rikala, R., Kainulainen, P., and Oksanen, J. 1995. Resource partitioning to growth, storage and defence in nitrogen-fertilized Scots pine and susceptibility of the seedlings to the tarnished plant bug Lygus rugulipennis. New Phytol. 131:521–532.

    Article  Google Scholar 

  • Johnson, N. C., Graham, J. H., and Smith, F. A. 1997. Functioning of mycorrhizal associations along the mutualism-parasitism continuum. New Phytol. 135:575–586.

    Article  Google Scholar 

  • Jones, C. G., and Last, F. T. 1991. Ectomycorrhizae and trees: implications for aboveground herbivory, pp. 65–103, in B. Barbosa, V.A. Krischik, and C.G. Jones (eds.). Microbial Mediation of Plant-Herbivore Interactions. Wiley, New York.

    Google Scholar 

  • Jonsson, L. M., Nilsson, M. -C., Wardle, D. A., and Zackrisson, O. 2001. Context dependent effects of ectomycorrhizal species richness on tree seedling productivity. Oikos 93:353–364.

    Article  Google Scholar 

  • Kainulainen, P., Holopainen, J., Palomäki, V., and Holopainen, T. 1996. Effects of nitrogen fertilization on secondary chemistry and ectomycorrhizal state of Scots pine seedlings and on growth of grey pine aphid. J. Chem. Ecol. 22:617–636.

    Article  CAS  Google Scholar 

  • Kaitaniemi, P., Ruohomäki, K., Ossipov, V., Haukioja, E., and Pihlaja, K. 1998. Delayed induced changes in the biochemical composition of host plant leaves during an insect outbreak. Oecologia 116:182–190.

    Article  Google Scholar 

  • Karley, A. J., Douglas, A. E., and Parker, W. E. 2002. Amino acid composition and nutritional quality of potato leaf phloem sap for aphids. J. Exp. Biol. 205:3009–3018.

    PubMed  CAS  Google Scholar 

  • Kause, A., Ossipov, V., Haukioja, E., Lempa, K., Hanhimäki, S., and Ossipova, S. 1999. Multiplicity of biochemical factors determining quality of growing birch leaves. Oecologia 120:102–112.

    Article  Google Scholar 

  • Keinänen, M., Julkunen-Tiitto, R., Mutikainen, P., Walls, M., Ovaska, J., and Vapaavuori, E. 1999. Trade-offs in phenolic metabolism of silver birch: effects of fertilization, defoliation, and genotype. Ecology 80:1970–1986.

    Google Scholar 

  • Lavola, A., Julkunen-Tiitto, R., and Pääkkönen, E. 1994. Does ozone stress change the primary and secondary metabolites of birch (Betula pendula Roth.)? New Phytol. 126:637–642.

    Article  CAS  Google Scholar 

  • Le Quere, A., Wright, D. P., Soderstrom, B., Tunlid, A., and Johansson, T. 2005. Global patterns of gene regulation associated with the development of ectomycorrhiza between birch (Betula pendula Roth.) and Paxillus involutus (Batsch) fr. Mol. Plant Microbe Interact. 18:659–673.

    Article  PubMed  CAS  Google Scholar 

  • Manninen, A. -M. 1999. Susceptibility of Scots pine seedlings to specialist and generalist insect herbivores – Importance of plant defence and mycorrhizal status. PhD dissertation. University of Kuopio, Finland.

  • Manninen, A. -M., Holopainen, T., and Holopainen, J. K. 1998a. Susceptibility of ectomycorrhizal and nonmycorrhizal Scots pine (Pinus sylvestris) seedlings to a generalist insect herbivore, Lygus rugulipennis, at two nitrogen availability levels. New Phytol. 140:55–63.

    Article  Google Scholar 

  • Manninen, A. -M., Laatikainen, T., and Holopainen, T. 1998b. Condition of Scots pine fine roots and mycorrhiza after fungicide application and low-level ozone exposure in a 2-year field experiment. Trees 12:347–355.

    Article  Google Scholar 

  • Manninen, A. -M., Vuorinen, M., and Holopainen, J. K. 1998c. Variation in growth, chemical defense, and herbivore resistance in Scots pine provenances. J. Chem. Ecol. 24:1315–1331.

    Article  CAS  Google Scholar 

  • Manninen, A. -M., Holopainen, T., and Holopainen, J. K. 1999. Performance of grey pine aphid, Schizolachnus pineti, on ectomycorrhizal and nonmycorrhizal Scots pine seedlings at different levels of nitrogen availability. Entomol. Exp. Appl. 93:117–120.

    Article  Google Scholar 

  • Manninen, A. -M., Holopainen, T., and Holopainen, J. K. 2000. The role of low-level ozone exposure and mycorrhizas in chemical quality and insect herbivore performance on Scots pine seedlings. Glob. Chang. Biol. 6:111–121.

    Article  Google Scholar 

  • Markkola, A. -M. 1996. Resource allocation in ectomycorrhizal symbiosis in Scots pine affected by environmental changes. PhD dissertation. University of Oulu, Finland.

  • Mutikainen, P., Walls, M., Ovaska, J., Keinänen, M., Julkunen-Tiitto, R., and Vapaavuori, E. 2000. Herbivore resistance in Betula pendula: effect of fertilization, defoliation, and plant genotype. Ecology 81:49–65.

    Google Scholar 

  • Nurmi, K., Ossipov, V., Haukioja, E., and Pihlaja, K. 1996. Variation of total phenolic content and individual low-molecular-weight phenolics in foliage of mountain birch trees (Betula pubescens ssp. tortuosa). J. Chem. Ecol. 22:2023–2040.

    Article  CAS  Google Scholar 

  • Nylund, J. -E., and Wallander, H. 1992. Ergosterol analysis as a means of quantifying mycorrhizal biomass. Method Microbiol. 24:77–88.

    Article  CAS  Google Scholar 

  • Ossipov, V., Haukioja, E., Ossipova, S., Hanhimäki, S., and Pihlaja, K. 2001. Phenolic and phenolic-related factors as determinants of suitability of mountain birch leaves to an herbivorous insect. Biochem. Syst. Ecol. 29:223–240.

    Article  PubMed  CAS  Google Scholar 

  • Palermo, B. L., Clancy, K. M., and Koch, G. W. 2003. The potential role of ectomycorrhizal fungi in determining Douglas-fir resistance to defoliation by the western spruce budworm (Lepidoptera: Tortricidae). J. Econ. Entomol. 96:783–791.

    PubMed  Google Scholar 

  • Pääkkönen, E., Paasisalo, S., Holopainen, T., and Kärenlampi, L. 1993. Growth and stomatal responses of birch (Betula pendula Roth.) clones to ozone in open-air and chamber fumigations. New Phytol. 125:615–623.

    Article  Google Scholar 

  • Peltonen, P. A., Vapaavuori, E., and Julkunen-Tiitto, R. 2005. Accumulation of phenolic compounds in birch leaves is changed by elevated carbon dioxide and ozone. Glob. Chang. Biol. 11:1305–1324.

    Article  Google Scholar 

  • Peltonen, P. A., Vapaavuori, E., Julkunen-Tiitto, R., and Holopainen, J. K. 2006. Effects of elevated carbon dioxide and ozone on aphid oviposition preference and birch bud exudate phenolics. Glob. Chang. Biol. 12:1670–1679.

    Article  Google Scholar 

  • Price, P. W. 1991. The plant vigor hypothesis and herbivore attack. Oikos 62:244–251.

    Article  Google Scholar 

  • Rabin, L. B., and Pacovsky, R. S. 1985. Reduced larva growth of two lepidoptera (Noctuidae) on excised leaves of soybean infected with a mycorrhizal fungus. J. Econ. Entomol. 78:1358–1363.

    Google Scholar 

  • Read, D. J., and Perez-Moreno, J. 2003. Mycorrhizas and nutrient cycling in ecosystems - a journey towards relevance. New Phytol. 157:475–492.

    Article  Google Scholar 

  • Rieske, L. K. 2001. Influence of symbiotic fungal colonization on oak seedling growth and suitability for insect herbivory. Environ. Entomol. 30:849–854.

    Article  Google Scholar 

  • Smith, S. E., and Read, D. J. 1997. Mycorrhizal Symbiosis. Academic, Cambridge.

    Google Scholar 

  • Van Der Meijden, E. 1996. Plant defense, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomol. Exp. Appl. 80:307–310.

    Article  Google Scholar 

  • Waldbauer, G. P. 1968. The consumption and utilization of food by insects. Adv. Insect. Physiol. 5:229–288.

    Article  Google Scholar 

Download references

Acknowledgements

This study was financially supported by the Research Council for the Environment and Natural resources (project no. 17549/94), the Academy of Finland. We thank Inga Korhonen, Mirja Korhonen, Terttu Matilainen and the staff at the Kuopio University Research Garden for valuable technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anne-Marja Nerg.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nerg, AM., Kasurinen, A., Holopainen, T. et al. The Significance of Ectomycorrhizas in Chemical Quality of Silver Birch Foliage and Above-Ground Insect Herbivore Performance. J Chem Ecol 34, 1322–1330 (2008). https://doi.org/10.1007/s10886-008-9542-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-008-9542-z

Keywords

Navigation