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Genetic and Environmental Factors Behind Foliar Chemistry of the Mature Mountain Birch

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Abstract

Previous studies of mountain birch (Betula pubescens spp. czerepanovii) repeatedly have found differences between individual trees in herbivory-related traits, but rarely have yielded estimates of the additive genetic variation of these traits or of their relationship to habitat. We used thirty-year-old birch half-sibs in a northern common garden to estimate the effect of genetics and local microhabitat on resistance-related traits. Genetic estimates of foliar chemistry have been studied only rarely with trees as old as these. Moth performance (Epirrita autumnata), rust (Melampsoridium betulinum) incidence levels, and the general level of natural herbivory damage to individual trees were used as direct measures of birch resistance. Chemical resistance-related traits in plant chemistry included 15 individual phenolics, 16 amino acids, and phenoloxidase activities in the foliage. We also followed birch phenology and growth. Our results show that the genotype of the birch was the most important determinant of phenolic composition and phenoloxidase activity, but that amino acid levels were best explained by the microhabitat of the birch. We also found that the phenology of the birch had a high heritability, although its variation was low. Our results reveal rich genetic variation in birch chemistry.

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References

  • Adler, F. R. and Karban, R. 1994. Defended fortresses or moving targets? Another model of inducible defenses inspired by military metaphors. Am. Nat. 144:813.

    Article  Google Scholar 

  • Aerts, R., Cornelissen, J. H. C., and Dorrepaal, E. 2006. Plant performance in a warmer world: General responses of plants from cold, northern biomes and the importance of winter and spring events. Plant Ecol. 182:65.

    Google Scholar 

  • Agrawal, A. A. 2011. Current trends in the evolutionary ecology of plant defence. Funct. Ecol. 25:420.

    Article  Google Scholar 

  • Ahlholm, J. U., Helander, M., Henriksson, J., Metzler, M., and Saikkonen, K. 2002. Environmental conditions and host genotype direct genetic diversion of ventura ditricha, a fungal endophyte of birch trees. Evolution 56:1566.

    PubMed  Google Scholar 

  • Anttila, U., Julkunen-Tiitto, R., Rousi, M., Yang, S., Rantala, M. J., and Ruuhola, T. 2010. Effects of elevated ultraviolet-B radiation on a plant-herbivore interaction. Oecologia 164:163–175.

    Article  PubMed  Google Scholar 

  • Appel, H. M. 1993. Phenolics in ecological interactions: The importance of oxidation. J. Chem. Ecol. 19:1521.

    Article  CAS  Google Scholar 

  • Ayres, M. P. and Maclean, S. F. J. 1987. Development of birch leaves and the growth energetics of epirrita autumnata (geometridae). Ecology 68:558.

    Article  Google Scholar 

  • Ayres, M. P., Suomela, J., and Maclean, S. F. J. 1987. Growth performance of epirrita autumnata (lepidopteran: Geometridae) on mountain birch: Trees, broods, and tree x brood interactions. Oecologia 74:450.

    Article  Google Scholar 

  • Bank, R. A., Jansen, E. J., Beekman, B., and Te Koppele, J. M. 1996. Amino acid analysis by reverse-phase high-performance liquid chromatography: Improved derivatization and detection conditions with 9-fluoremethyl chloroformate. Anal. Biochem. 240:167.

    Article  PubMed  CAS  Google Scholar 

  • Berenbaum, M. R. 1995. Turnabout is fair play: Secondary roles for primary compounds. J. Chem. Ecol. 21:925.

    Article  CAS  Google Scholar 

  • Berenbaum, M. R. and Zangerl, A. R. 1992. Genetics of secondary metabolism and herbivore resistance in plants., pp. 415, in G. A. Rosenthal and M. R. Berenbaum (eds.), Herbivores: Their Interactions with Secondary Plant Metabolites. Volume II. Ecological and Evolutionary Processes. Academic Press, Inc., San Diego.

    Google Scholar 

  • Bradford, M. M. 1976. Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 72:248.

    Article  PubMed  CAS  Google Scholar 

  • Bryant, J. P., Chapin, S. F. I., and Klein, D. R. 1983. Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357.

    Article  CAS  Google Scholar 

  • Carmona, D., Lajeunesse, M. J., and Johnson, M. T. J. 2011. Plant traits that predict resistance to herbivores. Funct. Ecol. 25:358.

    Article  Google Scholar 

  • Close, D. C. and McArthur, C. 2002. Rethinking the role of many plant phenolics—Protection from photodamage not herbivores? Oikos 99:166.

    Article  CAS  Google Scholar 

  • Elamo, P., Helander, M., Saloniemi, I., and Neuvonen, S. 1999. Birch family and environmental conditions affect endophytic fungi in leaves. Oecologia 118:151.

    Article  Google Scholar 

  • Elamo, P., Saloniemi, I., Helander, M. L., and Neuvonen, S. 2000. Genetic and environmental variation in rust frequency on mature mountain birch trees. Scand. J. For. Res. 15:510.

    Article  Google Scholar 

  • Elkington, T. T. 1968. Introgressive hybridization between Betula nana L. and B. pubescens Ehrh. in North-West Iceland. New Phytol. 67:109.

    Article  Google Scholar 

  • Feeny, P. 1976. Plant apparency and chemical defence. Rec. Adv. Phytochem. 10:1.

    CAS  Google Scholar 

  • Felton, G. W., Donato, K., del Vecchio, R. J., and Duffey, S. S. 1989. Activation of plant foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J. Chem. Ecol. 15:2667.

    Article  CAS  Google Scholar 

  • Fisher, R. A. 1930. The Genetic Theory of Natural Selection. Charendon Press, Oxford.

    Google Scholar 

  • Geber, M. S. and Griffen, L. R. 2003. Inheritance and natural selection of functional traits. Int. J. Plant Sci. 164:s21.

    Article  Google Scholar 

  • Harborne, J. B. and Williams, C. A. 2000. Review: Advances in flavonoid research since 1992. Phytochemistry 55:481.

    Article  PubMed  CAS  Google Scholar 

  • Haukioja, E. 2003. Putting the insect into the birch-insect interaction. Oecologia 136:161.

    Article  PubMed  Google Scholar 

  • Haukioja, E. 2005. Plant defenses and population fluctuations of forest defoliators: Mechanism-based scenarios. Ann. Zool. Fenn. 42:313.

    Google Scholar 

  • Haukioja, E., Ossipov, V., and Lempa, K. 2002. Interactive effects of leaf maturation and phenolics on consumption and growth of a geometrid moth. Entomol. Exp. Appl. 104:125.

    Article  CAS  Google Scholar 

  • Haviola, S., Saloniemi, I., Ossipov, V., and Haukioja, E. 2006. Additive genetic variation of secondary and primary metabolites in mountain birch. Oikos 112:382.

    Article  CAS  Google Scholar 

  • Haviola, S., Kapari, L., Ossipov, V., Rantala, M. J., Ruuhola, T., and Haukioja, E. 2007. Foliar phenolics are differently associated with epirrita autumnata growth and immunocompetence. J. Chem. Ecol. 33:1013.

    Article  PubMed  CAS  Google Scholar 

  • Houle, D. 1992. Comparing evolvability and variability of quantitative traits. Genetics 130:195.

    PubMed  CAS  Google Scholar 

  • Jonsell, B. 2000a. Betula L, pp. 197, in B. Jonsell (ed.), Flora Nordica, vol. 1: Lycopodiaceae to Polygonaceae. The Royal Swdish Academy of Sciences, Stocholm.

    Google Scholar 

  • Kallio, P. and Lehtonen, J. 1973. Birch forest damage caused by oporinia autumnata (bkh.) in 1965–66 in Utsjoki, N Finland. Rep. Kevo Subarctic Res. Stat. 10:55.

    Google Scholar 

  • Kallio, P. and Mäkinen, Y. 1978. Vascular flora of Inari Lapland. 4. betulaceae. Rep. Kevo Subarctic Res. Stat. 14:38.

    Google Scholar 

  • Kallio, P., Hurme, H., Eurola, S., Norokorpi, Y., and Sepponen, P. 1986. Research activities on the forest line in northern Finland. Arctic 39:52.

    Google Scholar 

  • Karban, R. 2011. The ecology and evolution of induced resistance against herbivores. Funct. Ecol. 25:339.

    Article  Google Scholar 

  • Karlsson, P. S. and Weih, M. 1996. Relationship between nitrogen economy and performance in the mountain birch betula pubescens ssp. tortuosa. Ecol. Bull. 45:71.

    CAS  Google Scholar 

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

    Article  Google Scholar 

  • Kause, A., Saloniemi, I., Haukioja, E., and Hanhimäki, S. 1999b. How to become large quickly: Quantitative genetics of growth and foraging in a flush feeding lepidopteran larva. J. Evol. Biol. 12:471.

    Article  Google Scholar 

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

    Google Scholar 

  • Laitinen, M., Julkunen-Tiitto, R., and Rousi, M. 2000. Variation in phenolic compounds within a birch (betula pendula) population. J. Chem. Ecol. 26:1609.

    Article  CAS  Google Scholar 

  • Lande, R. and Arnold, S. J. 1983. The measurement of selection on correlated characters. Evolution 37:1210.

    Article  Google Scholar 

  • Linhart, Y. B. and Grant, M. C. 1996. Evolutionary significance of local genetic differentiation in plants. Annu. Rev. Ecol. Syst. 27:237.

    Article  Google Scholar 

  • Macdonald, A. D. and Mothersill, D. H. 1983. Shoot development in Betula papyrifera. I. Short-shoot organogenisis. Can. J. Bot. 61:3049.

    Article  Google Scholar 

  • Moilanen, J. and Salminen, J. 2008. Ecologically neglected tannins and their biologically relevant activity: Chemicalstructures of plant ellagitannins reveal their in vitro oxidative activity at high pH. Chemoecology 18:73.

    Article  CAS  Google Scholar 

  • Mousseau, T. A. and Roff, D. A. 1987. Natural selection and the heritability of fitness components. Heredity 59:181.

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Tenow, O. 1972. The outbreaks of oporinia autumnata bkh. and operophtera spp. (lep.; geometridae) in the scandinavian mountain chain and northern Finland 1862–1968. Dissertation. University of Uppsala.

  • Nurmi, K., Ossipov, V., Haukioja, E., and Pihaja, 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.

    Article  CAS  Google Scholar 

  • Pigliucci, M. 2001. Phenotypic Plasticity—Beyond Nature and Nurture. The Johns Hopkins University Press, Baltimore.

    Google Scholar 

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

    Article  Google Scholar 

  • Riihimäki, J., Vehvilainen, H., Kaitaniemi, P., and Koricheva, J. 2006. Host tree architecture mediates the effect of predators on herbivore survival. Ecol. Entomol. 31:227.

    Article  Google Scholar 

  • Riipi, M., Ossipov, V., Lempa, K., Haukioja, E., Koricheva, J., Ossipova, S., and Pihlaja, K. 2002. Seasonal changes in birch leaf chemistry: Are there trade-offs between leaf growth and accumulation of phenolics? Oecologia 130:380.

    Article  Google Scholar 

  • Riipi, M., Haukioja, E., Lempa, K., Ossipov, V., Ossipova, S., and Pihlaja, K. 2004. Ranking of individual mountain birch trees in terms of leaf chemistry: Seasonal and annual variation. Chemoecology 14:31.

    Article  CAS  Google Scholar 

  • Roff, D. A. and Mousseau, T. A. 1987. Quantitative genetics and fitness: Lessons from drosophila. Heredity 58:103.

    Article  PubMed  Google Scholar 

  • Roslin, T., Gripenberg, S., Salminen, J., Karonen, M., O’Hara, R. B., Pihlaja, K., and Pulkkinen, P. 2006. Seeing the trees for the leaves—Oaks as mosaic for a host-specific moth. Oikos 113:106.

    Article  Google Scholar 

  • Ruohomäki, K., Chapin, S. F. I., Haukioja, E., Neuvonen, S., and Suomela, J. 1996. Delayed inducible resistance in mountain birch in response to fertilization and shade. Ecology 77:2302.

    Article  Google Scholar 

  • Ruuhola, T. and Yang, S. 2006. Wound-induced oxidative responses in mountain birch leaves. Ann. Bot. 97:29.

    Article  PubMed  CAS  Google Scholar 

  • Ruuhola, T., Ossipov, V., Lempa, K., and Haukioja, E. 2003. Amino acids during development of mountain birch leaves. Chemoecology 13:95.

    CAS  Google Scholar 

  • Ruuhola, T., Salminen, J., Haviola, S., Yang, S., and Rantala, M. J. 2007. Immunological memory of mountain birches: Effects of phenolics on performance on the autumnal moth depend on herbivory history of trees. J. Chem. Ecol. 33:1160.

    Article  PubMed  CAS  Google Scholar 

  • Ruusila, V., Morin, J., van Ooik, T., Saloniemi, I., Ossipov, V., and Haukioja, E. 2005. A short-lived herbivore on a long-living host: Tree resistance to herbivory depends on leaf age. Oikos 108:99.

    Article  Google Scholar 

  • Salminen, J. and Karonen, M. 2011. Chemical ecology of tannins and other phenolics: We need a change in approach. Funct. Ecol. 25:325.

    Article  Google Scholar 

  • Salminen, J., Ossipov, V., Loponen, J., Haukioja, E., and Pihlaja, K. 1999. Characterisation of hydrolysable tannins from leaves of betula pubescens by high-performance liquid chromatography—Mass spectrometry. J. Chromatogr. A. 864:283.

    Article  CAS  Google Scholar 

  • Salminen, J., Ossipov, V., Haukioja, E., and Pihlaja, K. 2001. Seasonal variation in the content of hydrolysable tannins in leaves of betula pubescens. Phytochemistry 57:15.

    Article  PubMed  CAS  Google Scholar 

  • SAS Institute 1990. SAS/STAT User’s Guide. 6th version. SAS Institute, Cary.

    Google Scholar 

  • Senn, J., Hanhimäki, S., and Haukioja, E. 1992. Among-tree variation in leaf phenology and morphology and its correlation with insect performance in the mountain birch. Oikos 63:215.

    Article  Google Scholar 

  • Shelton, A. L. 2004. Variation in chemical defences of plants may improve the effectiveness of defence. Evol. Ecol. Res. 6:709.

    Google Scholar 

  • Sulkinoja, M. and Valanne, T. 1987. Leafing and bud size in betula provenances of different latitudes and altitudes. Rep. Kevo Subarctic Res. Stat. 20:27.

    Google Scholar 

  • Suomela, J., Ossipov, V., and Haukioja, E. 1995. Variation among and within mountain birch trees in foliage phenols, carbohydrates, and amino acids, and in growth of epirrita autumnata larvae. J. Chem. Ecol. 21:1421.

    Article  CAS  Google Scholar 

  • Sveinbjörnsson, B., Kauhanen, H., and Nordell, O. 1996. Treeline ecology of mountain birch in the torneträsk area. Ecol. Bull. 45:65.

    Google Scholar 

  • Tenow, O. 1996. Hazards to a mountain birch forest—Abisko in perspective. Ecol. Bull. 45:104.

    Google Scholar 

  • Underwood, N. 2004. Variance and skew of the distribution of plant quality influence herbivore population dynamics. Ecology 85:686.

    Article  Google Scholar 

  • Virtanen, T. and Neuvonen, S. 1999. Performance of moth larvae on birch in relation to altitude, climate, host quality and parasitoids. Oecologia 120:92.

    Article  Google Scholar 

  • Yang, S., Haviola, S., and Ruuhola, T. 2007. Temporal and spatial variation in mountain birch foliar enzyme activities during the larval period of epirrita autumnata. Chemoecology 17:71.

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to Alice Liu, who started the fertilization treatments. We also thank the staff of the Kevo Subarctic Research Station, especially for creating and maintaining the tree-line gardens and for providing research facilities and a good atmosphere; as well as our summer assistants, Ulla Anttila, Pauliina Wäli, and Mikko Oikamo, for making this study possible. The language of the manuscript was checked by Ellen Valle. The study was supported financially by the Academy of Finland (TR and MJR) and by the Finnish Cultural Foundation (SH). The experiments presented comply with current Finnish legislation.

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Haviola, S., Neuvonen, S., Rantala, M.J. et al. Genetic and Environmental Factors Behind Foliar Chemistry of the Mature Mountain Birch. J Chem Ecol 38, 902–913 (2012). https://doi.org/10.1007/s10886-012-0148-0

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