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The Effects of Defoliation-Induced Delayed Changes in Silver Birch Foliar Chemistry on Gypsy Moth Fitness, Immune Response, and Resistance to Baculovirus Infection

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Abstract

We tested the effects of defoliation-induced changes in silver birch, Betula pendula, foliar chemistry (delayed induced resistance, DIR) on the fitness and immune defense of the gypsy moth, Lymantria dispar. We measured larval developmental time, pupal weight, rate of survival to the adult stage, and five characteristics of larval immune defense: (1) encapsulation response; (2) phenoloxidase activity; (3) hemocyte concentration and (4) lysozyme-like activity in the hemolymph; and (5) resistance to infection by L. dispar nucleopolyhedrovirus (LdMNPV). The latter is an entomopathogenic baculovirus that often causes epizootics during outbreaks of L. dispar. We also measured the involvement of foliage non-tannin phenolic compounds in resistance of B. pendula to herbivory as well as the relationship between the compounds we identified and L. dispar development, growth, and survival. Leaves of B. pendula with previous defoliation history contained increased levels of myricetin glycoside, two flavonoid aglycones (acacetin and tetrahydroxy-flavone dimethyl ether), as well as one unidentified simple phenolic. The concentrations of two glycosides of quercetin, as well as the content of one unidentified flavonoid glycoside were significantly decreased under defoliation treatment. DIR of B. pendula retarded larval growth rate and increased lysozyme-like activity in the hemolymph, but did not affect encapsulation response, phenoloxidase activity, or hemocyte count. We did not find any DIR-mediated tritrophic interactions among birch, gypsy moth, and LdMNPV. After viral inoculation, the mean hemocyte counts in larvae reared on an individual tree correlated significantly with the survival of larvae reared on that same tree, indicating that hemocyte density in hemolymph might be associated with resistance to viral infection. We found a strong positive correlation between the concentration of 1-(4″-hydroxyphenyl)-3′-oxopropyl-β-D-glucopyranose and L. dispar survival rate, which may indicate an unlikely role of this dominant non-tannin phenolic in B. pendula defense against L. dispar. Our study also shows that several immune characteristics of insects that function as barriers against different groups of parasites are differently affected by plant induced defenses. This underscores the importance of considering multiple factors when characterizing barriers to insect immunity.

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Acknowledgments

We thank Ekaterina Chertkova, Ekaterina Grizanova, and Elena Bojarisheva for help with the laboratory and field studies and Dr. Derek Dunn for critical comments on an earlier version of this manuscript. We are grateful to John D. Podgwaite and Will Sillitoe for help with the English language and for valuable comments on previous versions of the manuscript. We especially thank Teija Ruuhola and Vadim Efimov for assistance with the statistical analyses and three anonymous reviewers for helpful comments. The work was supported financially by the Kone Foundation, Russian Foundation for Basic Research (Grant No. 09-04-00767), and a government grant from the Russian Federation (No. MК-2372.2011.4) and from the Academy of Finland (to MJR).

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Authors and Affiliations

  1. Laboratory of Insect Pathology, Institute of Systematics and Ecology of Animals SB RAS, 630091, Novosibirsk, Frunze \Str. 11, Russia

    Vyacheslav V. Martemyanov, Ivan M. Dubovskiy, Irina A. Belousova, Sergey V. Pavlushin, Stanislav A. Bakhvalov & Victor V. Glupov

  2. Section of Ecology, Department of Biology, University of Turku, FIN-20014, Turku, Finland

    Markus J. Rantala

  3. Department of Chemistry, University of Turku, FIN-20014, Turku, Finland

    Juha-Pekka Salminen

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  1. Vyacheslav V. Martemyanov
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  2. Ivan M. Dubovskiy
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  3. Markus J. Rantala
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  4. Juha-Pekka Salminen
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  5. Irina A. Belousova
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  7. Stanislav A. Bakhvalov
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  8. Victor V. Glupov
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Correspondence to Vyacheslav V. Martemyanov.

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Martemyanov, V.V., Dubovskiy, I.M., Rantala, M.J. et al. 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, 295–305 (2012). https://doi.org/10.1007/s10886-012-0090-1

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