Journal of Chemical Ecology

, Volume 38, Issue 1, pp 116–125 | Cite as

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

  • Minna Laurentz
  • Joanneke H. Reudler
  • Johanna Mappes
  • Ville Friman
  • Suvi Ikonen
  • Carita Lindstedt


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.


Aucubin Catalpol Chemical defense Encapsulation rate Immunological defense Iridoid glycosides Plantago lanceolata Serratia marcescens Tritrophic interactions 



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.

Supplementary material

10886_2012_66_MOESM1_ESM.doc (32 kb)
Table S1 Temperature and light conditions in the environmental chamber during the experiment (DOC 32 kb)
10886_2012_66_MOESM2_ESM.doc (40 kb)
Table S2 Correlations between ig-levels and nutritional quality of the diets (DOC 40.0 kb)


  1. Baden, C. U. and Dobler, S. 2009. Potential benefits of iridoid glycoside sequestration in Longitarsus melanocephalus (Coleoptera, Chrysomelidae). Basic Appl. Ecol. 10: 27-33.CrossRefGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. Berenbaum, M. R. and Zangerl, A. R. 1993. Furanocoumarin metabolism in Papilio polyxenes: biochemistry, genetic variability, and ecological significance. Oecologia 95: 370–375.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. Codella, S. G., and Raffa, K. F. 1995. Host plant influence on chemical defense in conifer sawflies (Hymenoptera: Diprionidae). Oecologia 104: 1-11.CrossRefGoogle Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.PubMedCrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.
  12. Daly, H. W, Doyen, J. T., and Purcell, A. H. 1998. Introduction to Insect Biology and Diversity. 2nd edn. Oxford University Press, 696 p.Google Scholar
  13. 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.Google Scholar
  14. Després, L., David, J.-P., and Gallet C. 2007. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22: 298-307.PubMedCrossRefGoogle Scholar
  15. 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.PubMedGoogle Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. 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.PubMedGoogle Scholar
  18. 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.PubMedCrossRefGoogle Scholar
  19. 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.PubMedCrossRefGoogle Scholar
  20. Gillespie, J. P., Kanost, M. R., and Trenczek, T. 1997. Biological mediators of insect immunity. Annu. Rev. Entomol. 42: 611–43.PubMedCrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. Grimont, P. A. D. and Grimont, F. 1978. The genus Serratia. Annu. Rev. Microbiol. 32: 221-248.PubMedCrossRefGoogle Scholar
  23. Hanski, I., Pakkala, T., Kuussaari, M., and Lei, G. 1995. Metapopulation persistence of an endangered butterfly in a fragmented landscape. Oikos 72: 21-28.CrossRefGoogle Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. 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.PubMedCrossRefGoogle Scholar
  26. Karban, R. and English-Loeb, G. 1997. Tachinid parasitoids affect host plant choice by caterpillars to increase caterpillar survival. Ecology 78: 603-611.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 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.PubMedGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. Lill, J. T., Marquis, R. J., and Ricklefs, R. E. 2002. Host plants influence parasitism of forest caterpillars. Nature 417: 170-173.PubMedCrossRefGoogle Scholar
  33. 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.PubMedCrossRefGoogle Scholar
  34. 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.PubMedCrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. Marttila, O. 2005. Suomen päiväperhoset elinympäristössään. Käsikirja. Auris, Joutseno, 272 p.Google Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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.PubMedCrossRefGoogle Scholar
  39. 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.PubMedGoogle Scholar
  40. 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.PubMedCrossRefGoogle Scholar
  41. Nishida, R. 2002. Sequestration of defensive substances from plants by Lepidoptera. Annu. Rev. Entomol. 47: 57-92.PubMedCrossRefGoogle Scholar
  42. 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
  43. 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.PubMedCrossRefGoogle Scholar
  44. Rantala, M. J. and Kortet, R. 2004. Male dominance and immunocompetence in a field cricket. Behav. Ecol. 15: 187-191.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. 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.CrossRefGoogle Scholar
  47. 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. PubMedCrossRefGoogle Scholar
  48. 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.CrossRefGoogle Scholar
  49. Rolff, J. and Siva-Jothy, M. T. 2003. Invertebrate ecological immunology. Science 301: 472-475.PubMedCrossRefGoogle Scholar
  50. Rolff, J. and Siva-Jothy, M. T. 2004. Selection on insect immunity in the wild. Proc. R. Soc. Lond. B 271: 2157-2160.CrossRefGoogle Scholar
  51. 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
  52. 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.PubMedCrossRefGoogle Scholar
  53. Siva-Jothy, M. T., Moret, Y., and Rolff, J. 2005. Insect immunity: an evolutionary ecology perspective. Adv. Insect Physiol. 32: 1-48.CrossRefGoogle Scholar
  54. 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.PubMedCrossRefGoogle Scholar
  55. 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.CrossRefGoogle Scholar
  56. 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.CrossRefGoogle Scholar
  57. 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.PubMedCrossRefGoogle Scholar
  58. 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.CrossRefGoogle Scholar
  59. 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.PubMedCrossRefGoogle Scholar
  60. 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.CrossRefGoogle Scholar
  61. 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.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Minna Laurentz
    • 1
  • Joanneke H. Reudler
    • 1
  • Johanna Mappes
    • 1
  • Ville Friman
    • 1
    • 2
  • Suvi Ikonen
    • 3
  • Carita Lindstedt
    • 1
    • 4
  1. 1.Centre of Excellence in Evolutionary Research, Department of Biological and Environmental SciencesUniversity of JyväskyläJyväskyläFinland
  2. 2.Department of ZoologyThe Tinbergen BuildingOxfordUK
  3. 3.Department of BiosciencesUniversity of HelsinkiLammiFinland
  4. 4.Department of ZoologyUniversity of CambridgeCambridgeUK

Personalised recommendations