Skip to main content
Log in

Immunological Memory of Mountain Birches: Effects of Phenolics on Performance of the Autumnal Moth Depend on Herbivory History of Trees

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

Abstract

Plants have been suggested to have an immunological memory comparable to animals. The evidence for this, however, is scarce. In our study with the mountain birch—Epirrita autumnata system, we demonstrated that birches exposed as long as 5 yr to feeding of E. autumnata larvae (delayed induced resistance, DIR), responded more strongly to a new challenge than trees without an herbivory history. Pupal weights remained lower, and the duration of the larval period was prolonged in the DIR trees, although immunity, measured as an encapsulation rate, was not affected. We further demonstrated that the effects of birch phenolics on performance of E. autumnata were different in the exposed (DIR) trees from naive control trees, although we found only one significant change in chemistry. The quercetin:kaemferol ratio was increased in DIR trees, suggesting that herbivory caused oxidative stress in birches. In DIR trees, phenolics, especially hydrolyzable tannins (HTs), affected pupal weights negatively, whereas in control trees, the effects were either nonsignificant or positive. HTs also prolonged the duration of the larval period of females, whereas peroxidase (POD) activity prolonged that of males. We suggest that the causal explanation for the induced resistance was an enhanced oxidation of phenolic compounds from the DIR trees in the larval digestive tract. Phenolic oxidation produces semiquinones, quinones, free radicals, and ROS, which may have toxic, antinutritive, and/or repellent properties against herbivores.

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

Similar content being viewed by others

References

  • Appel, H. M. 1993. Phenolics in ecological interactions: The importance of oxidation. J. Chem. Ecol. 19:1521–1552.

    Article  CAS  Google Scholar 

  • Baldwin, I., and Schmelz, E. A. 1996. Immunological “memory” in the induced accumulation of nicotine in wild tobacco. Ecology 77:236–246.

    Article  Google Scholar 

  • Barbehenn, R. V., Jones, C. P., Hagerman, A. E., Karonen, M., and Salminen, J-P. 2006. Ellagitannins have greater oxidative activities than condensed tannins and galloylglucoses at high pH: potential impact on caterpillars. J. Chem. Ecol. 32:2253–2267.

    Article  PubMed  CAS  Google Scholar 

  • Bi, J. L., and Felton, G. W. 1995. Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. J. Chem. Ecol. 21:1511–1530.

    Article  CAS  Google Scholar 

  • Bradford, M. M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle protein–dye binding. Anal. Biochem. 72:248–254.

    Article  PubMed  CAS  Google Scholar 

  • Chan, T., Galati, G., and O’Brien, P. J. 1999. Oxygen activation during peroxidase catalysed metabolism of flavones or flavanones. Chem. -Biol. Interact. 122:15–25.

    Article  PubMed  CAS  Google Scholar 

  • Danell, K., Haukioja, E., and Huss-Danell, K. 1997. Morphological and chemical responses of mountain birch leaves and shoots to winter browsing along a gradient of plant productivity. Ecoscience 4:296–303.

    Google Scholar 

  • Felton, G. W., and Duffey, S. S. 1991. Protective action of midgut catalase in Lepidopteran larvae against oxidative plant defenses. J. Chem. Ecol. 17:1715–1732.

    Article  CAS  Google Scholar 

  • Felton, G. W., Donato, K., Del Vecchio, R. J., and Duffey, S. S. 1989. Activation of foliar oxidases by insect feeding reduces nutritive quality of foliage for noctuid herbivores. J. Chem. Ecol. 15:2667–2694.

    Article  CAS  Google Scholar 

  • Gatehouse, J. A. 2002. Plant resistance towards insect herbivores: a dynamic interaction. New Phytol. 156:145–169.

    Article  CAS  Google Scholar 

  • Gorman, M. J., Cornel, A. J., Collins, F. H., and Paskewitz, S. M. 1996. A shared genetic mechanism for melanotic encapsulation of CM-sepharex beads and the malaria parasite, Plasmodium cynomolgi B, in the mosquito Anopheles gambiae. Exp. Parasitol. 84:380–386.

    Article  PubMed  CAS  Google Scholar 

  • Haukioja, E. 1982. Inducible defenses of white birch to a geometrid defoliator, Epirrita autumnata. pp. 199–203, in J. H. Visser and A. K. Minks (eds.). Proceedings of 5th International Symposium on Insect–Plant Relationship. Pudoc, Wageningen.

  • Haukioja, E. 2005. Plant defenses and population fluctuations of forest defoliators: mechanisms-based scenarios. Ann. Zool. Fenn. 42:313–325.

    Google Scholar 

  • Haukioja, E. and Neuvonen, S. 1985. Induced long-term resistance of birch foliage against defoliators: defensive or incidental? Ecology 66:1303–1308.

    Article  Google Scholar 

  • Haukioja, E., Suomela, J., and Nevonen, S. 1985. Long-term inducible resistance in birch foliage: triggering cues and efficacy on a defoliator. Oecologia 65:363–369.

    Article  Google Scholar 

  • Haukioja, E., Neuvonen, S., Hanhimäki, S., and Niemelä, P. 1988. The autumnal moth in Fennoscandia. pp. 163–178, in A. A. Berryman (ed.). Dynamics of Forest Insect Populations. Patterns, Causes, and Implications. Plenum Press, New York.

    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. 104:125–136.

    Article  CAS  Google Scholar 

  • Heim, K. E., Tagliaferro, A. R., and Bobilya, D. J. 2002. Flavonoid antioxidants: chemistry, metabolism and structure–activity relationship. J. Nutr. Biochem. 13:572–584.

    Article  PubMed  CAS  Google Scholar 

  • Hoover, K., Lee, L. Y., Schulz, C. M., Rocke, D. M., Hammock, B. D., and Duffey, S. S. 1998a. Effects of plant identity and chemical constituents on the efficacy of a baculovirus against Heliothis virescens. J. Chem. Ecol. 24:221–252.

    Article  CAS  Google Scholar 

  • Hoover, K., Kishida, K. T., DiGiorgio, L. A., Workman, J., Alaniz, S. A., Hammock, B. D., and Duffey, S. S. 1998b. Inhibition of baculoviral disease by plant-mediated peroxidase activity and free radical generation. J. Chem. Ecol. 24:1949–2001.

    Article  CAS  Google Scholar 

  • Kaitaniemi, P., Ruohomäki, K., and Haukioja, E. 1997. Consequences of defoliation on phenological interaction between Epirrita autumnata and its host plant, mountain birch. Funct. Ecol. 11:199–208.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Kapari, L., Haukioja, E., Rantala, M. J., and Ruuhola T. 2006. Defoliating insect immune defense interacts with induced plant defenses during a population outbreak. Ecology 87:291–296.

    PubMed  Google Scholar 

  • Karban, R., and Baldwin, I. T. 1997. Induced Responses to Herbivory. University of Chicago Press, Chicago.

    Google Scholar 

  • Karban, R., and Myers, J. H. 1989. Induced plant responses to herbivory. Annu. Rev. Ecol. Syst. 20:331–348.

    Article  Google Scholar 

  • Karban, R., and Niiho, C. 1995. Induced resistance and susceptibility to herbivory: plant memory and altered plant development. Ecology 76:1220–1225.

    Article  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 

  • Klemola, N., Klemola, T., Rantala, M. J., and Ruuhola, T. 2007. Natural host plant quality affects immune defense of the insect herbivore. Entomol. Exp. Appl. 123:167–176.

    Article  Google Scholar 

  • Lempa, K., Agrawal, A. A., Salminen, J. -P., Turunen, T., Ossipov, V., Ossipova, S., Haukioja, E., and Pihlaja, K. 2004. Rapid herbivore-induced changes in mountain birch phenolics and nutritive compounds and their effects on performance of the major defoliator, Epirrita autumnata. J. Chem. Ecol. 30:303–321.

    Article  PubMed  CAS  Google Scholar 

  • Levine, A., Tenhaken, R., Dixon, R., and Lamb, C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593.

    Article  PubMed  CAS  Google Scholar 

  • Liu, L., Gittz, D. C., and Mclure, J. W. 1995. Effects of UV-B on flavonoids, ferulic acid, growth and photosynthesis in barley primary leaves. Physiol. Plant. 93:725–733.

    Article  CAS  Google Scholar 

  • Markham, K. R., Ryan, K. G., Bloor, S. J., and Mitchell, K. A. 1998a. An increase in the luteolin:apigenin ratio in Marchantia polymorpha on UV-B enhancement. Phytochemistry 48:791–794.

    Article  CAS  Google Scholar 

  • Markham, K. R., Tanner, G. J., Caasi-lit, M., Whitecross, M. I., Nayudu, M., and Mitchell, K. A. 1998b. Possible protective role of 3′4′ -dihydroxyflavones induced by enhanced UV-B in a UV-tolerant rice cultivar. Phytochemistry 49:1913–1919.

    Article  CAS  Google Scholar 

  • Martin, J. S., Martin, M. M., and Bernays, E. A. 1987. Failure of tannic acid to inhibit digestion or reduce digestibility of plant protein in gut fluids of insect herbivores: implications for theories of plant defense. J. Chem. Ecol. 13:605–621.

    Article  CAS  Google Scholar 

  • Myers, J. H. 1998. Synchrony in outbreaks of forest Lepidoptera: a possible example of the Moran effect. Ecology 79:1111–1117.

    Article  Google Scholar 

  • Nappi, A. J., Vass, E., Frey, F., and Carton, Y. 1995. Superoxidase anion generation in Drosophila during melanotic encapsulation of parasites. Eur. J. Cell Biol. 68:450–456.

    PubMed  CAS  Google Scholar 

  • Olsson, L. C., Veit, M., and Bornman, J. F. 1999. Epidermal transmittance and phenolic composition in leaves of atrazine-tolerant and atrazine-sensitive cultivars of Brassica napus grown under enhanced UV-B radiation. Physiol. Plant. 107:259–266.

    Article  CAS  Google Scholar 

  • Orozco-Cárdenas, M. L., Nárvaez-Vásquez, J., and Ryan, C. A. 2001. Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin and methyl jasmonate. Plant Cell 13:179–191.

    Article  PubMed  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 

  • Paskewitz, S., and Riehle, M. A. 1994. Response of plasmodium refractory and susceptible strains of Anopheles gambiae to inoculated Sephadex beads. Dev. Comp. Immunol. 18:369.

    Article  PubMed  CAS  Google Scholar 

  • Pourcel, L., Routaboul, J. -M., Cheynier, V., Lepiniec, L., and Debeaujon, I. 2006. Flavonoid oxidation in plants: biochemical properties to physiological functions. Trends Plant Sci. 12:29–36.

    Article  PubMed  Google Scholar 

  • Rantala, M. J., and Roff, D. A. 2005. An analysis of trade-off in immune function, body size and development time in the Mediterranean field cricket, Gryllus bimaculatus. Funct. Ecol. 19:323–330.

    Article  Google Scholar 

  • Rantala, M. J. and Roff, D. A. 2007. Inbreeding and extreme outbreeding causes sex differences in immune defense and life history traits in Epirrita autumnata. Heredity 98:329–336.

    Article  PubMed  CAS  Google Scholar 

  • Rantala, M. J., Jokinen, I., Kortet, R., Vainikka, A., and Suhonen, J. 2002. Do pheromones reveal male immunocompetence. Proc. R. Soc. Lond. B. 269:1681–1685.

    Article  Google Scholar 

  • Rantala, M. J., Roff D. A., and Rantala, L. M. 2007. Forceps size and immune function in the European earwig Forficula auricularia. Biol. J. Linn. Soc. 90:509–516.

    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 130:380–390.

    Article  Google Scholar 

  • Ruohomäki, K., Chapin, III, F. S., Haukioja, E., Neuvonen, S., and Suomela, J. 1996. Delayed inducible resistance in mountain birch in response to fertilization and shade. Ecology 77:2302–2311.

    Article  Google Scholar 

  • Ruohomäki, K., Tanhuanpää, M., Ayres, M. P., Kaitaniemi, P., Tammaru, T., and Haukioja, E. 2000. Causes of cyclicity of Epirrita autumnata (Lepidoptera, Geometridae): grandiose theory and tedious practice. Pop. Ecol. 42:211–223.

    Article  Google Scholar 

  • Ruuhola, T. and Yang, S. 2006. Wound-induced oxidative responses in mountain birch leaves. Ann. Bot. 97:29–37.

    Article  PubMed  CAS  Google Scholar 

  • Ryan, C. A. 2000. The systemin signaling pathway: differential activation of plant defensive genes. Biochim. Biophys. Acta 1477:112–121.

    PubMed  CAS  Google Scholar 

  • Ryan, K. G., Markham, K. R., Bloor, S. J. Bradley, J. M., Mitchell, K. A., and Jordan, B. R. 1998. UV-B radiation induced increase in quercetin:kaemferol ratio in wild-type and transgenic lines of Petunia. Photochem. Photobiol. 68:323–330.

    Article  CAS  Google Scholar 

  • Salminen, J. -P., Ossipov, V., Loponen, J., Haukioja, E., and Pihlaja, K. 1999. Characterisation of hydrolyzable tannins from leaves of Betula pubescens by high-performance liquid chromatography-mass spectrometry. J. Chromatogr. A 864:283–291.

    Article  CAS  Google Scholar 

  • Salminen, J. -P., Ossipov, V., Haukioja, E., and Pihlaja, K. 2001. Seasonal variation in the content of hydrolyzable tannins in leaves of Betula pubescens. Phytochemistry 57:15–22.

    Article  PubMed  CAS  Google Scholar 

  • Salminen, J. -P., Ossipov, V., and Pihlaja, K. 2002. Distribution of hydrolyzable tannins in the foliage of Finnish birch species. Z. Naturforsch. 57c:248–256.

    Google Scholar 

  • Schweigert, N., Zehnder, A. J. B., and Eggen, R. I. L. 2001. Chemical properties of catechols and their molecular modes of toxic action in cells, from microorganisms to mammal. Environ. Microbiol. 3:81–91.

    Article  PubMed  CAS  Google Scholar 

  • Seppänen, E. J. 1970. Suomen suurperhostoukkien ravintokasvit (The food-plants of the larvae of the Macrolepidoptera of Finland). Animalia Fennica 14, Werner Söderström.

  • Söderhäll, K., and Cerenius, L. 1998. Role of the phenoloxidase-activating system in invertebrate immunity. Curr. Opin. Immunol. 10:23–28.

    Article  PubMed  Google Scholar 

  • Tallamy, D. W., and Raupp, M. J. 1991. Phytochemical induction by herbivores. John Wiley and Sons Inc., New York.

    Google Scholar 

  • Tammaru, T. 1998. Determination of adult size in a folivorous moth: constraints at instar level? Ecol. Entomol. 23:80–89.

    Article  Google Scholar 

  • Tenow, O. 1972. The outbreaks of Oporinia antumnata Bkh. and Operophtera spp. (Lep: Geometridae) in the Scandinavian mountain chain and northern Finland 1862–1986. PhD Thesis. Zool. Bridr. Uppsala, Suppl. 2:1–107.

  • Vaarama, A., and Valanne, T. 1973. On the taxonomy, biology and origin of Betula tortuosa Ledeb. Rep. Kevo Subarctic Res. Stat. 10:70–84.

    Google Scholar 

  • Wielgolaski, F. E. 2005. History and environment of the Nordic mountain birch. pp. 3–18, in F. E. Wielgolaski (ed.). Plant Ecology, Herbivory, and Human Impact in Nordic Mountain Birch Forests. Springer-Verlag, Berlin.

    Chapter  Google Scholar 

  • Zar, J. H. 1999. Biostatistical Analysis. Prentice Hall Int. Inc., London.

    Google Scholar 

Download references

Acknowledgements

The research was conducted in Kevo Subarctic Research Station, and we thank the staff for help and co-work. We also thank the department of Physiology and Genetics for providing the facilities for the enzymatic assays. We also thank our field assistants Ulla Anttila, Tia Lampela, Liisa Rantala and Mikko Oikamo, and Piia Saarinen for doing the phenolic analyses. Salla-Riikka Vesterlund kindly checked the English language. The study was supported financially by the Academy of Finland, Kone and Emil Aaltonen Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Teija Ruuhola.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ruuhola, T., Salminen, JP., Haviola, S. et al. Immunological Memory of Mountain Birches: Effects of Phenolics on Performance of the Autumnal Moth Depend on Herbivory History of Trees. J Chem Ecol 33, 1160–1176 (2007). https://doi.org/10.1007/s10886-007-9308-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-007-9308-z

Keywords

Navigation