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

Journal of Chemical Ecology

Volumn 38, Issue 1, 2012, Pages 116-125

  Laurentz, Minna ^a   Reudler, Joanneke H ^a   Mappes, Johanna ^a   Friman, Ville ^a,b   Ikonen, Suvi ^c   Lindstedt, Carita ^a,d  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b The Tinbergen Building ^*  (United Kingdom)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

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

Indexed keywords

IRIDOID;

BACTERIAL DISEASE; BUTTERFLY; CHEMICAL DEFENSE; DETOXIFICATION; DIET; ENCAPSULATION; FITNESS; HERBIVORE; HOST PLANT; HOST-PARASITOID INTERACTION; HOST-PATHOGEN INTERACTION; LARVA; LIFE HISTORY TRAIT; LINEARITY; PARASITISM; PLANT DEFENSE; SURVIVAL; TRADE-OFF; TROPHIC INTERACTION;

ANIMAL; ANIMAL DISEASE; ARTICLE; DIET; FEMALE; HOST PARASITE INTERACTION; HYMENOPTERA; IMMUNOLOGY; LARVA; LEPIDOPTERA; MALE; METABOLISM; MICROBIOLOGY; PARASITOLOGY; PHYSIOLOGY; SERRATIA MARCESCENS;

ANIMALS; DIET; FEMALE; HOST-PARASITE INTERACTIONS; HYMENOPTERA; IRIDOID GLYCOSIDES; LARVA; LEPIDOPTERA; MALE; SERRATIA MARCESCENS;

BACTERIA (MICROORGANISMS); HEXAPODA; MELITAEA CINXIA; PLANTAGO; PLANTAGO LANCEOLATA; SERRATIA MARCESCENS;

EID: 84856371125     PISSN: 00980331     EISSN: 15731561     Source Type: Journal    
DOI: 10.1007/s10886-012-0066-1     Document Type: Article

References (61)

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.
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.
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.
4. Berenbaum, M. R. and Zangerl, A. R. 1993. Furanocoumarin metabolism in Papilio polyxenes: biochemistry, genetic variability, and ecological significance. Oecologia 95: 370-375.
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.
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.
7. Codella, S. G., and Raffa, K. F. 1995. Host plant influence on chemical defense in conifer sawflies (Hymenoptera: Diprionidae). Oecologia 104: 1-11.
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.
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.
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.
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.
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.
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.
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.
16. 2 environments on production of carbon-based allelochemicals in Plantago: a test of the carbon/nutrient balance hypothesis. Am. Nat. 140: 707-723.
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.
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.
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.
20. Gillespie, J. P., Kanost, M. R., and Trenczek, T. 1997. Biological mediators of insect immunity. Annu. Rev. Entomol. 42: 611-43.
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.
22. Grimont, P. A. D. and Grimont, F. 1978. The genus Serratia. Annu. Rev. Microbiol. 32: 221-248.
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.
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.
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.
26. Karban, R. and English-Loeb, G. 1997. Tachinid parasitoids affect host plant choice by caterpillars to increase caterpillar survival. Ecology 78: 603-611.
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.
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.
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.
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.
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.
32. Lill, J. T., Marquis, R. J., and Ricklefs, R. E. 2002. Host plants influence parasitism of forest caterpillars. Nature 417: 170-173.
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.
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.
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.
36. Marttila, O. 2005. Suomen päiväperhoset elinympäristössään. Käsikirja. Auris, Joutseno, 272 p.
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.
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.
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.
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.
41. Nishida, R. 2002. Sequestration of defensive substances from plants by Lepidoptera. Annu. Rev. Entomol. 47: 57-92.
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.
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.
44. Rantala, M. J. and Kortet, R. 2004. Male dominance and immunocompetence in a field cricket. Behav. Ecol. 15: 187-191.
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.
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.
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.
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.
49. Rolff, J. and Siva-Jothy, M. T. 2003. Invertebrate ecological immunology. Science 301: 472-475.
50. Rolff, J. and Siva-Jothy, M. T. 2004. Selection on insect immunity in the wild. Proc. R. Soc. Lond. B 271: 2157-2160.
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.
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.
53. Siva-Jothy, M. T., Moret, Y., and Rolff, J. 2005. Insect immunity: an evolutionary ecology perspective. Adv. Insect Physiol. 32: 1-48.
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.
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.
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.
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.
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.
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.
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.
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.