Skip to main content

Advertisement

Log in

Diet Quality Can Play a Critical Role in Defense Efficacy against Parasitoids and Pathogens in the Glanville Fritillary (Melitaea cinxia)

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

Abstract

Numerous herbivorous insect species sequester noxious chemicals from host plants that effectively defend against predators, and against parasitoids and pathogens. Sequestration of these chemicals may be expensive and involve a trade off with other fitness traits. Here, we tested this hypothesis. We reared Glanville fritillary butterfly (Melitaea cinxia L.) larvae on plant diets containing low- and high-levels of iridoid glycosides (IGs) (mainly aucubin and catalpol) and tested: 1) whether IGs affect the herbivore’s defense against parasitoids (measured as encapsulation rate) and bacterial pathogens (measured as herbivore survival); 2) whether parasitoid and bacterial defenses interact; and 3) whether sequestration of the plant’s defense chemicals incurs any life history costs. Encapsulation rates were stronger when there were higher percentages of catalpol in the diet. Implanted individuals had greater amounts of IGs in their bodies as adults. This suggests that parasitized individuals may sequester more IGs, increase their feeding rate after parasitism, or that there is a trade off between detoxification efficiency and encapsulation rate. Larval survival after bacterial infection was influenced by diet, but probably not by diet IG content, as changes in survival did not correlate linearly with the levels of IGs in the diet. However, M. cinxia larvae with good encapsulation abilities were better defended against bacteria. We did not find any life history costs of diet IG concentration for larvae. These results suggest that the sequestering of plant defense chemicals can help herbivorous insects to defend against parasitoids.

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

  • Baden, C. U. and Dobler, S. 2009. Potential benefits of iridoid glycoside sequestration in Longitarsus melanocephalus (Coleoptera, Chrysomelidae). Basic Appl. Ecol. 10: 27-33.

    Article  CAS  Google Scholar 

  • Baer, B. and Schmid-Hempel, P. 2003. Effects of selective episodes in the field on life history traits in the bumblebee Bombus terrestris. Oikos 101: 563-568.

    Article  Google Scholar 

  • Bauce, E., Bidon, Y., and Berthiaume, R. 2002. Effects of food nutritive quality and Bacillus thuringiensis on feeding behaviour, food utilization and larval growth of spruce budworm Choristoneura fumiferana (Clem.) when exposed as fourth- and sixth-instar larvae. Agric. For. Entomol. 4: 57-70.

    Article  Google Scholar 

  • Berenbaum, M. R. and Zangerl, A. R. 1993. Furanocoumarin metabolism in Papilio polyxenes: biochemistry, genetic variability, and ecological significance. Oecologia 95: 370–375.

    Article  Google Scholar 

  • Bowers, M. D., Collinge, S. K., Gamble, S. E., and Schmitt, J. 1992. Effects of genotype, habitat, and seasonal variation on iridoid glycoside content of Plantago lanceolata (Plantaginaceae) and the implications for insect herbivores. Oecologia 91: 201-207.

    Article  Google Scholar 

  • Camara, M. D. 1997. Physiological mechanisms underlying the costs of chemical defence in Junonia coenia Hubner (Nymphalidae): A gravimetric and quantitative genetic analysis. Evol. Ecol. 11: 451-469.

    Article  Google Scholar 

  • Codella, S. G., and Raffa, K. F. 1995. Host plant influence on chemical defense in conifer sawflies (Hymenoptera: Diprionidae). Oecologia 104: 1-11.

    Article  Google Scholar 

  • Cohen, J. A. 1985. Differences and similarities in cardenolide contents of queen and monarch butterflies in Florida and their ecological and evolutionary implications. J. Chem. Ecol. 11: 85-103.

    Article  CAS  Google Scholar 

  • Cotter, S. C., Kruuk, L. E. B., and Wilson, K. 2004a. Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. J. Evol. Biol. 17: 421-429.

    Article  PubMed  CAS  Google Scholar 

  • Cotter, S. C., Hails, R. S., Cory, J. S., and Wilson, K. 2004b. Density-dependent prophylaxis and condition-dependent immune function in Lepidopteran larvae: a multivariate approach. J. Anim. Ecol. 73: 283-293.

    Article  Google Scholar 

  • Cotter, S. C., Simpson S. J., Raubenheimer, D., and Wilson, K. 2011. Macronutrient balance mediates trade-offs between immune function and life history traits. Funct. Ecol. doi:10.1111/j.1365-2435.2010.01766.x.

  • Daly, H. W, Doyen, J. T., and Purcell, A. H. 1998. Introduction to Insect Biology and Diversity. 2nd edn. Oxford University Press, 696 p.

  • De La Fuente, M.-A., Dyer, L. A., and Bowers, M. D. 1994/1995. The iridoid glycoside, catalpol, as a deterrent to the predator Camponotus floridanus (Formicidae). Chemoecology 5/6: 13–18.

  • Després, L., David, J.-P., and Gallet C. 2007. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22: 298-307.

    Article  PubMed  Google Scholar 

  • Duff, R. B., Bacon, J. S. D., Mundie, C. M., Farmer, V. C., Russell, J. D., and Forrester, A. R. 1965. Catalpol and methylcatalpol: naturally occurring glycosides in Plantago and Buddleia species. Biochem. J. 96: 1-5.

    PubMed  CAS  Google Scholar 

  • Fajer, E. D., Bowers, M. D., and Bazzaz, F. A. 1992. The effect of nutrients and enriched CO2 environments on production of carbon-based allelochemicals in Plantago: a test of the carbon/nutrient balance hypothesis. Am. Nat. 140: 707-723.

    Article  PubMed  CAS  Google Scholar 

  • Flyg, C., Kenne, K., and Boman, H. G. 1980. Insect pathogenic properties of Serratia marcescens: phage-resistant mutants with a decreased resistance to Cecropia immunity and a decreased virulence to Drosophila. J. Gen. Microbiol. 120: 173-181.

    PubMed  CAS  Google Scholar 

  • Friman, V.-P., Lindstedt, C., Hiltunen, T., Laakso, J., and Mappes, J. 2009. Predation on multiple trophic levels shapes the evolution of pathogen virulence. PLoS ONE 4: e6761.

    Article  PubMed  Google Scholar 

  • Friman, V.-P., Hiltunen, T., Jalasvuori, M., Lindstedt, C., Laanto, E., Örmälä, A.-M., Laakso, J., Mappes, J., and Bamford, J. K. H. 2011. High temperature and bacteriophages can indirectly select for bacterial pathogenicity in environmental reservoirs. PLoS ONE 6: e17651.

    Article  PubMed  CAS  Google Scholar 

  • Gillespie, J. P., Kanost, M. R., and Trenczek, T. 1997. Biological mediators of insect immunity. Annu. Rev. Entomol. 42: 611–43.

    Article  PubMed  CAS  Google Scholar 

  • Grill, C. P. and Moore, A. J. 1998. Effects of a larval antipredator response and larval diet on adult phenotype in an aposematic ladybird beetle. Oecologia 114: 274-282.

    Article  Google Scholar 

  • Grimont, P. A. D. and Grimont, F. 1978. The genus Serratia. Annu. Rev. Microbiol. 32: 221-248.

    Article  PubMed  CAS  Google Scholar 

  • Hanski, I., Pakkala, T., Kuussaari, M., and Lei, G. 1995. Metapopulation persistence of an endangered butterfly in a fragmented landscape. Oikos 72: 21-28.

    Article  Google Scholar 

  • Harvey, J. A., Van Nouhuys, S., and Biere, A. 2005. Effects of quantitative variation in allelochemicals in Plantago lanceolata on development of a generalist and a specialist herbivore and their endoparasitoids. J. Chem. Ecol. 31: 287-302.

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Karban, R. and English-Loeb, G. 1997. Tachinid parasitoids affect host plant choice by caterpillars to increase caterpillar survival. Ecology 78: 603-611.

    Article  Google Scholar 

  • Klemola, N., Kapari, L., and Klemola, T. 2008. Host plant quality and defence against parasitoids: no relationship between levels of parasitism and a geometrid defoliator immunoassay. Oikos 117: 926-934.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • König, C. and Schmid-Hempel, P. 1995. Foraging activity and immunocompetence in workers of the bumble bee Bombus terrestris L. Proc. R. Soc. Lond., B, Biol. Sci. 260: 225-227.

    Article  Google Scholar 

  • Lambrechts, L., Vulule, J. M., and Koella, J. C. 2004. Genetic correlation between melanization and antibacterial immune responses in a natural population of the malaria vector Anopheles gambiae. Evolution 58: 2377-2381.

    PubMed  Google Scholar 

  • Lee, K. P., Simpson, S. J., and Wilson, K. 2008. Dietary protein-quality influences melanization and immune function in an insect. Funct. Ecol. 22: 1052-1061.

    Article  Google Scholar 

  • Lill, J. T., Marquis, R. J., and Ricklefs, R. E. 2002. Host plants influence parasitism of forest caterpillars. Nature 417: 170-173.

    Article  PubMed  CAS  Google Scholar 

  • Lindstedt, C., Mappes, J., Päivinen, J., and Varama, M. 2006: Effects of group size and pine defence chemicals on diprionid sawfly survival against ant predation. Oecologia 150: 519-526.

    Article  PubMed  Google Scholar 

  • Lindstedt, C., Reudler Talsma, J. H., Ihalainen, E., Lindström, L., and Mappes, J. 2010. Diet quality affects warning coloration indirectly: excretion costs in a generalist herbivore. Evolution 64: 68-78.

    Article  PubMed  Google Scholar 

  • Marak, H. B., Biere, A., and Van Damme, J. M. M. 2000. Direct and correlated responses to selection on iridoid glycosides in Plantago lanceolata L. J. Evol. Biol. 13: 985-996.

    Article  CAS  Google Scholar 

  • Marttila, O. 2005. Suomen päiväperhoset elinympäristössään. Käsikirja. Auris, Joutseno, 272 p.

    Google Scholar 

  • Mcvean, R. I. K., Sait, S. M., Thompson, D. J., and Begon, M. 2002. Dietary stress reduces the susceptibility of Plodia interpunctella to infection by granulovirus. Biol. Control 25: 81-84.

    Article  Google Scholar 

  • Mody, K., Unsicker, S. B., and Linsenmair, K. E. 2007. Fitness related diet-mixing by intraspecific host-plant-switching of specialist insect herbivores. Ecology 88: 1012-1020.

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Nieminen, M., Suomi, J., Van Nouhyus, S., Sauri, P., and Riekkola, M.-L. 2003. Effect of iridoid glycoside content on oviposition host plant choice and parasitism in a specialist herbivore. J. Chem. Ecol. 29: 823-844.

    Article  PubMed  CAS  Google Scholar 

  • Nishida, R. 2002. Sequestration of defensive substances from plants by Lepidoptera. Annu. Rev. Entomol. 47: 57-92.

    Article  PubMed  CAS  Google Scholar 

  • Ojala, K., Julkunen-Tiitto, R., Lindström, L., and Mappes, J. 2005. Diet affects the immune defence and life-history traits of an Arctiid moth Parasemia plantaginis. Evol. Ecol. Res. 7: 1153-1170.

    Google Scholar 

  • Poirié, M., Carton, Y., and Dubuffet, A. 2009. Virulence strategies in parasitoid Hymenoptera as an example of adaptive diversity. C. R. Biol. 332: 311-320.

    Article  PubMed  Google Scholar 

  • Rantala, M. J. and Kortet, R. 2004. Male dominance and immunocompetence in a field cricket. Behav. Ecol. 15: 187-191.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Reudler Talsma, J. H., Biere, A., Harvey, J. A., and Van Nouhuys, S. 2008. Oviposition cues for a specialist butterfly–plant chemistry and size J. Chem. Ecol. 34: 1202-1212.

    Article  CAS  Google Scholar 

  • Reudler, J. H., Biere, A., Harvey, J. A., and Van Nouhuys, S. 2011. Differential performance of specialist and generalist herbivores and their parasitoids on Plantago lanceolata. J. Chem. Ecol. 37: 765-778.

    Article  PubMed  CAS  Google Scholar 

  • Rigby, M. C. and Jokela, J. 2000. Predator avoidance and immune defence: costs and trade-offs in snails. Proc. R. Soc. Lond. B 267: 171-176.

    Article  CAS  Google Scholar 

  • Rolff, J. and Siva-Jothy, M. T. 2003. Invertebrate ecological immunology. Science 301: 472-475.

    Article  PubMed  CAS  Google Scholar 

  • Rolff, J. and Siva-Jothy, M. T. 2004. Selection on insect immunity in the wild. Proc. R. Soc. Lond. B 271: 2157-2160.

    Article  Google Scholar 

  • Saastamoinen, M., Van Nouhuys, S., Nieminen, M., O’hara, B., and Suomi, J. 2007. Development and survival of a specialist herbivore, Melitaea cinxia, on host plants producing high and low concentrations of iridoid glycosides. Ann. Zool. Fenn. 44: 70-80.

    Google Scholar 

  • Singer, M. S., Mace, K. C., and Bernays, E. A. 2009. Self-medication as adaptive plasticity: increased ingestion of plant toxins by parasitized caterpillars. PLoS ONE 4: e4796.

    Article  PubMed  Google Scholar 

  • Siva-Jothy, M. T., Moret, Y., and Rolff, J. 2005. Insect immunity: an evolutionary ecology perspective. Adv. Insect Physiol. 32: 1-48.

    Article  CAS  Google Scholar 

  • Smilanich, A. M., Dyer, L. A., Chambers, J. Q., and Bowers, M. D. 2009. Immunological cost of chemical defence and the evolution of herbivore diet breadth. Ecol. Lett. 12: 612-621.

    Article  PubMed  Google Scholar 

  • Suomi, J., Sirén, H., Wiedmer, S. K., and Riekkola, M.-L. 2001. Isolation of aucubin and catalpol from Melitaea cinxia larvae and quantification by micellar electrokinetic capillary chromatography. Anal. Chim. Acta 429: 91-99.

    Article  CAS  Google Scholar 

  • Suomi, J., Wiedmer, S. K., Jussila, M., and Riekkola, M.-L. 2002. Analysis of eleven iridoid glycosides by micellar electrokinetic capillary chromatography (MECC) and screening of plant samples by partial filling (MECC)-electrospray ionisation mass spectrometry. J. Chromatogr. 970: 287-296.

    Article  CAS  Google Scholar 

  • Suomi, J., Sirén, H., Jussila, M., Wiedmer, S. K., and Riekkola, M.-L. 2003. Determination of iridoid glycosides in larvae and adults of butterfly Melitaea cinxia by partial filling micellar electrokinetic capillary chromatography–electrospray ionisation mass spectrometry. Anal. Bioanal. Chem. 376: 884-889.

    Article  PubMed  CAS  Google Scholar 

  • Theodoratus, D. H. and Bowers, M. D. 1999. Effects of sequestered iridoid glycosides on prey choice of the prairie wolf spider, Lycosa carolinensis. J. Chem. Ecol. 25: 283-295.

    Article  CAS  Google Scholar 

  • Tundis R., Loizzo M. R., Menichini F., Statti G. A., and Menichini F. 2008 Biological and pharmacological activities of iridoids: recent developments. Mini Rev. Med. Chem. 8: 399-420.

    Article  PubMed  CAS  Google Scholar 

  • Van Nouhuys, S. and Hanski, I. 2002. Colonization rates and distances of a host butterfly and two specific parasitoids in a fragmented landscape. J. Anim. Ecol. 71: 639-650.

    Article  Google Scholar 

  • Von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D., and Wittzell, H. 1999. Good genes, oxidative stress and condition-dependent sexual signals. Proc. R. Soc. Lond. B 266: 1-12.

    Article  Google Scholar 

Download references

Acknowledgements

We thank Arjen Biere for the plant seeds and Hannu Pakkanen for help with the chemical analyses. We are grateful to three anonymous reviewers and to Robert Hegna and Sheena Cotter for their comments on improving our manuscript. The study was funded by Suomen Biologian Seura Vanamo ry, the Societas pro Fauna et Flora Fennica, the Academy of Finland and the Centre of Excellence for Evolutionary Research, Jyväskylä.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carita Lindstedt.

Electronic Supplementary Materials

Below is the link to the electronic supplementary material.

Table S1

Temperature and light conditions in the environmental chamber during the experiment (DOC 32 kb)

Table S2

Correlations between ig-levels and nutritional quality of the diets (DOC 40.0 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Laurentz, M., Reudler, J.H., Mappes, J. et al. Diet Quality Can Play a Critical Role in Defense Efficacy against Parasitoids and Pathogens in the Glanville Fritillary (Melitaea cinxia). J Chem Ecol 38, 116–125 (2012). https://doi.org/10.1007/s10886-012-0066-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-012-0066-1

Keywords

Navigation