Arthropod-Plant Interactions

, Volume 6, Issue 4, pp 507–518 | Cite as

Rapid induced resistance of silver birch affects both innate immunity and performance of gypsy moths: the role of plant chemical defenses

  • Vyacheslav V. Martemyanov
  • Ivan M. Dubovskiy
  • Irina A. Belousova
  • Sergey V. Pavlushin
  • Dmitry V. Domrachev
  • Markus J. Rantala
  • Juha-Pekka Salminen
  • Stanislav A. Bakhvalov
  • Victor V. Glupov
Original Paper

Abstract

In this study we tested the effects of rapid induced resistance of the silver birch, Betula pendula, on the performance and immune defense of the gypsy moth, Lymantria dispar. We also measured the effects of defoliation on the concentrations of plant secondary metabolites, particularly on phenolics and terpenoids. It was found that severe natural defoliation (by moth larvae) of silver birch led to an increase in lipophilic flavonoids on the leaf surface. The concentration of some simple phenolics and monoterpenes (linalool and geraniol) also increased, while that of several glycosides of quercetin decreased. The female pupal weights and survival rates of moths decreased, and larval development time increased, when the insects fed on defoliated trees. However, the feeding of caterpillars with the leaves of defoliated trees led to an increase in lysozyme-like activity in their hemolymph, with an increase in their ability to encapsulate potential parasites. Our data show that the silver birch deploys a rapid chemical defense against gypsy moth larvae. We suggest that lipophilic flavonoids are important compounds in the direct silver birch defense against L. dispar caterpillars. The increased strength of immune defense of insects exposed to trees that had deployed a rapid induced resistance may be an adaptation of the herbivores to resist the rising density of parasites when host population density is high.

Keywords

Plant–insect interaction Betula pendula Lymantria dispar Defoliation Rapid induced resistance Secondary compounds 

References

  1. Barbehenn RV, Jaros A, Lee G, Mozola C, Weir Q, Salminen J-P (2009) Hydrolyzable tannins as “quantitative defenses”: limited impact against Lymantria dispar caterpillars on hybrid poplar. J Insect Physiol 55:297–304PubMedCrossRefGoogle Scholar
  2. Berenbaum MR (1995) Turnabout is fair play: secondary roles for primary compounds. J Chem Ecol 21:925–940CrossRefGoogle Scholar
  3. Bradford JM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254Google Scholar
  4. Doane CC, McManus ML (1981) The gypsy moth: research toward integrated pest management. Department of Agriculture, Forest Service, Science and Education Agency. Animal and Plant Health Inspection Service, Washington, USAGoogle Scholar
  5. Doskotch RW, Cheng H-Y, Odell TM, Girard L (1980) Nerolidol: an antifeeding sesquiterpene alcohol for gypsy moth larvae from Melaleuca leucadendron. J Chem Ecol 6:845–851CrossRefGoogle Scholar
  6. Dubovskiy IM, Krukova NA, Glupov VV (2008) Phagocytic activity and encapsulation rate of Galleria mellonella larvae hemocytes during bacterial infection by Bacillus thuringiensis. J Invert Pathol 98:360–362CrossRefGoogle Scholar
  7. Haukioja E (1991) Induction of defenses in trees. Ann Rev Entomol 36:25–42CrossRefGoogle Scholar
  8. Haukioja E (2005) Plant defenses and population fluctuations of forest defoliators: mechanism-based scenarios. Ann Zool Fenn 42:313–325Google Scholar
  9. Kaitaniemi P, Ruohomäki K, Ossipov V, Haukioja E, Pihlaja K (1998) Delayed induced changes in the biochemical composition of host plant leaves during an insect outbreak. Oecologia 116:182–190CrossRefGoogle Scholar
  10. Kapari L, Haukioja E, Rantala MJ, Ruuhola T (2006) Defoliating insect immune defense interacts with induced plant defense during a population outbreak. Ecology 87:291–296PubMedCrossRefGoogle Scholar
  11. Keane S, Ryan MF (1999) Purification, characterization, and inhibition by monoterpenes of acetylcholinesterase from the wax moth, Galleria mellonella (L.). Insect Biochem Mol Biol 29:1097–1104CrossRefGoogle Scholar
  12. Keinänen M, Julkunen-Tiitto R, Mutikainen P, Walls M, Ovaska J, Vapaavuori E (1999) Trade-offs in phenolic metabolism of silver birch: Effects of fertilization, defoliation, and genotype. Ecology 80:1970–1986Google Scholar
  13. Keinänen M, Julkunen-Tiitto R (1996) Effect of sample preparation method on birch (Betula pendula Roth) leaf phenolics. J Agric Food Chem 44:2724–2727CrossRefGoogle Scholar
  14. Keinänen M, Julkunen-Tiitto R (1998) High-performance liquid chromatographic determination of flavonoids in Betula pendula and Betula pubescens leaves. J Chromatogr A 793:370–377CrossRefGoogle Scholar
  15. Lahtinen M, Salminen J-P, Kapari L, Lempa K, Ossipov V, Sinkkonen J, Valkama E, Haukioja E, Pihlaja K (2004) Defensive effect of surface flavonoid aglycones of Betula pubescens leaves against first-instar Epirrita autumnata larvae. J Chem Ecol 30:2257–2268PubMedCrossRefGoogle Scholar
  16. Lahtinen M, Lempa K, Salminen J-P, Pihlaja K (2006) HPLC analysis of leaf surface flavonoids for the preliminary classification of birch species Phytochem Anal 17:197–203Google Scholar
  17. Larsson S (2002) Resistance in trees to insects—an overview of mechanisms and interactions. In: Wagner MR et al (eds) Mechanisms and deployment of resistance in trees to insects. Kluwer Academic Publishers, Netherlands, pp 1–29CrossRefGoogle Scholar
  18. Lazarević J, Perić-Mataruga V, Stojković B, Tucić N (2002) Adaptation of the gypsy moth to an unsuitable host plant. Entomol Exp App 102:75–86CrossRefGoogle Scholar
  19. Lee KP, Cory JS, Wilson K, Raubenheimerand D, Simpson SJ (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc R Soc London Ser B 273:823–829CrossRefGoogle Scholar
  20. Lempa K, Agrawal AA, Salminen J-P, Turunen T, Ossipov V, Ossipova S, Haukioja E, 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 30:303–321PubMedCrossRefGoogle Scholar
  21. Likens ST, Nickerson GB (1964) Detection of certain hop oil constituents in brewing products. Proc Am Brewing Chem 5:5–13Google Scholar
  22. Martemyanov VV, Bakhvalov SA (2007) Interrelationships of plant–insect–parasite systems and their influence on the development and population dynamics of forest defoliators. Eurasian Entomol J 6:205–221Google Scholar
  23. Martemyanov VV, Bakhvalov SA, Dubovskiy IM, Glupov VV, Salakhutdinov NF, Tolstikov GA (2006) Effect of tannic acid on the development and resistance of the gypsy moth Lymantria dispar L. to viral infection. Dokl Biochem Biophys 409:219–222PubMedCrossRefGoogle Scholar
  24. Martemyanov VV, Dubovskiy IM, Rantala, MJ, Salminen JP, Belousova IA, Pavlushin SV, Bakhvalov SA, Glupov VV (2012) The effects of defoliation-induced delayed changes in silver birch foliar chemistry on gypsy moth fitness, immune response, and resistance to baculovirus infection. J Chem Ecol 38:295–305Google Scholar
  25. Mutikainen P, Walls M, Ovaska J, Keinanen M, Julkunen-Tiitto R, Vapaavuori E (2000) Herbivore resistance in Betula pendula: effect of fertilization, defoliation, and plant genotype. Ecology 81:49–65Google Scholar
  26. Neuvonen S, Haukioja E (1991) The effects of inducible resistance in host foliage on birch-feeding herbivores. In: Tallamy DW, Raupp MJ (eds) Phytochemical induction by herbivores. Wiley, New York, pp 277–291Google Scholar
  27. Ojala K, Julkunen-Tiitto R, Lindström L, Mappes J (2005) Diet affects the immune defence and life-history traits of an Arctiid moth Parasemia plantaginis. Evol Ecol Res 7:1153–1170Google Scholar
  28. Osier TL, Lindroth RL (2001) Effects of genotype, nutrient availability, and defoliation on aspen phytochemistry and insect performance. J Chem Ecol 27:1289–1313PubMedCrossRefGoogle Scholar
  29. Ossipov V, Nurmi K, Loponen J, Haukioja E, Pihlaja K (1996) HPLC separation and identification of phenolic compounds from leaves of Betula pubescens and Betula pendula. J Chromatogr A 721:59–68CrossRefGoogle Scholar
  30. Ossipov V, Haukioja E, Ossipova S, Hanhimäki S, Pihlaja K (2001) Phenolic and phenolic-related factors as determinants of suitability of mountain birch leaves to an herbivorous insect. Biochem Syst Ecol 29:223–240PubMedCrossRefGoogle Scholar
  31. Parry D, Herms DA, Mattson WJ (2003) Responses of an insect folivore and its parasitoids to multiyear experimental defoliation of aspen. Ecology 84:1768–1783CrossRefGoogle Scholar
  32. Rantala MJ, Roff DA (2007) Inbreeding and extreme outbreeding causes sex differences in immune defence and life history traits in Epirrita autumnata. Heredity 98:329–336PubMedCrossRefGoogle Scholar
  33. Roden DB, Mattson WJ (2008) Rapid induced resistance and host species effects on gypsy moth, Lymantria dispar (L.): implications for outbreaks on three tree species in the boreal forest. For Ecol Manag 255:1868–1873CrossRefGoogle Scholar
  34. Rosenthal GA, Berenbaum MR (1992) Herbivores, their interactions with secondary plant metabolites. The chemical participants, vol I. Academic Press, New YorkGoogle Scholar
  35. Ruuhola T, Yang S, Rantala MJ (2010) Increase in substrate availability down-regulates PO activity in Epirrita autumnata. Chemoecology 20:11–18CrossRefGoogle Scholar
  36. Ryan MF, Byrne O (1988) Plant-insect coevolution and inhibition of acetylcholinesterase. J Chem Ecol 14:1965–1975CrossRefGoogle Scholar
  37. Salminen J-P, Ossipov V, Loponen J, Haukioja E, Pihlaja K (1999) Characterisation of hydrolysable tannins from leaves of Betula pubescens by high-performance liquid chromatography–mass spectrometry. J Chromatogr A 864:283–291CrossRefGoogle Scholar
  38. Siva-Jothy MT, Thompson JW (2002) Short-term nutrient deprivation affects immune function. Physiol Entomol 27:206–212CrossRefGoogle Scholar
  39. Smilanich AM, Dyer LE, Gentry GL (2009) The insect immune response and other putative defenses as effective predictors of parasitism. Ecology 90:1434–1440PubMedCrossRefGoogle Scholar
  40. Stevens MT, Lindroth RL (2005) Induced resistance in the indeterminate growth of aspen (Populus tremuloides). Oecologia 145:298–306PubMedCrossRefGoogle Scholar
  41. Stockhoff BA (1993) Ontogenetic change in dietary selection for protein and lipid by gypsy moth larvae. J Insect Physiol 39:677–686CrossRefGoogle Scholar
  42. Tkachev AV (2008) The investigation of plant volatiles. Izdatelsko-poligraficheskoe predprijatie “Ofset”. Novosibirsk, RussiaGoogle Scholar
  43. Trudeau D, Washburn JO, Volkman LE (2001) Central role of hemocytes in Autographa californica M nucleopolyhedrovirus pathogenesis in Heliothis virescens and Helicoverpa zea. J Virol 75:996–1003PubMedCrossRefGoogle Scholar
  44. Valkama E, Salminen J-P, Koricheva J, Pihlaja K (2003) Comparative analysis of leaf trichome structure and composition of epicuticular flavonoids in Finnish birch species. Ann Bot 91:643–655PubMedCrossRefGoogle Scholar
  45. Valkama E, Salminen JP, Koricheva J, Pihlaja K (2004) Changes in leaf trichomes and epicuticular flavonoids during leaf development in three birch taxa. Ann Bot 94:233–242PubMedCrossRefGoogle Scholar
  46. Valkama E, Koricheva J, Salminen J-P, Helander M, Saloniemi I, Saikkonen K, Pihlaja K (2005) Leaf surface traits: overlooked determinants of birch resistance to herbivores and foliar microfungi? Trees 19:191–197CrossRefGoogle Scholar
  47. Vuorinen T, Nerg A-M, Syrjälä L, Peltonen P, Holopainen JK (2007) Epirrita autumnata induced VOC emission of silver birch differ from emission induced by leaf fungal pathogen. Arthropod-Plant Interact 1:159–165CrossRefGoogle Scholar
  48. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216PubMedGoogle Scholar
  49. Wilson K, Cotter ShC, Reeson AF, Pell JuK (2001) Melanism and disease resistance in insects. Ecol Lett 4:637–649CrossRefGoogle Scholar
  50. Yang S, Ruuhola T, Rantala MJ (2007) Impacts of starvation on immune defense and other life history traits of an outbreaking geometrid, Epirrita autumnata: a possible ultimate trigger of the crash phase of population cycle. Ann Zool Fenn 44:89–96Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Vyacheslav V. Martemyanov
    • 1
    • 3
  • Ivan M. Dubovskiy
    • 1
  • Irina A. Belousova
    • 1
  • Sergey V. Pavlushin
    • 1
  • Dmitry V. Domrachev
    • 2
  • Markus J. Rantala
    • 3
  • Juha-Pekka Salminen
    • 4
  • Stanislav A. Bakhvalov
    • 1
  • Victor V. Glupov
    • 1
  1. 1.Laboratory of Insect PathologyInstitute of Systematics and Ecology of Animals SB RASNovosibirskRussia
  2. 2.Laboratory of Terpene CompoundsVorozhtsov Novosibirsk Institute of Organic Chemistry SB RASNovosibirskRussia
  3. 3.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland
  4. 4.Laboratory of Organic Chemistry and Chemical Biology, Department of ChemistryUniversity of TurkuTurkuFinland

Personalised recommendations