Skip to main content
SpringerLink
Log in

Effect of Iridoid Glycoside Content on Oviposition Host Plant Choice and Parasitism in a Specialist Herbivore

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

Abstract

The Glanville fritillary butterfly Melitaea cinxia feeds upon two host plant species in Å land, Finland, Plantago lanceolataand Veronica spicata, both of which produce iridoid glycosides. Iridoids are known to deter feeding or decrease the growth rate of many generalist insect herbivores, but they often act as oviposition cues to specialist butterflies and are feeding stimulants to their larvae. In this study, two iridoid glycosides (aucubin and catalpol) were analyzed by micellar electrokinetic capillary chromatography. We measured the spatial and temporal variation of iridoid glycosides in natural populations of the host plants of M. cinxia. We also analyzed the aucubin and catalpol content in plants in relation to their use by ovipositing females, and in relation to the incidence of parasitism of M. cinxia larvae in natural populations. The mean concentrations of aucubin and catalpol were higher in P. lanceolata than in V. spicata, and catalpol concentrations were higher than aucubin concentrations in both host species. Plantago lanceolata individuals that were used for oviposition by M. cinxia had higher aucubin concentrations than random plants and neighboring plants. Additionally, oviposition and random plants had higher catalpol concentrations than neighboring plants, indicating that ovipositing females select for high iridoid glycoside plants or that oviposition induces iridoid glycoside production in P. lanceolata. Parasitism by the specialist parasitoid wasp Cotesia melitaearum occurred most frequently in larval groups that were feeding on plants with low concentrations of catalpol, irrespective of year, population, and host plant species. Therefore, parasitoids appear to avoid or perform poorly in host larvae with high catalpol content.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adler, L. S., Schmitt, J., and Bowers, M. D. 1995. Genetic variation in defensive chemistry in Plantago lanceolata (Plantaginaceae) and its effect on the specialist herbivore Junonia coenia (Nymphalidae). Oecologia 101:75–85.

    Google Scholar 

  • Agrawal, A. 2000. Plant defense: signals in insect eggs. TREE 15:357.

    Google Scholar 

  • Awmack, C. S. and Leather, S. R. 2002. Host plant quality and fecundity in herbivorous insects. Annu. Rev. Entomol. 47:817–844.

    Google Scholar 

  • Barbosa, P., Saunders, J. A., Kemper, J., Trumble, R., Olechno, J., and Martinat, P. 1986. Plant allelochemicals and insect parasitoids: effects of nicotine on Cotesia congregata (Say) (Hymenoptera: Braconidae) and Hyposoter annulipes (Cressen) (Hymenoptera: Ichneumonidae). J. Chem. Ecol. 12:1319–1328.

    Google Scholar 

  • Belofsky, G., Bowers, M. D., Janzen, S., and Stermitz, F. 1989. Iridoid glycosides of Aureolaria flava and their sequestration by Euphydryas phaeton butterflies. Phytochemistry 28:1601–1604.

    Google Scholar 

  • Bernays, E. and De Luca, C. 1981. Insect antifeedant properties of an iridoid glycoside: ipolamiide. Experientia 37:1289–1290.

    Google Scholar 

  • Bianco, A. 1990. The chemistry of iridoids, pp. 439–497, in Atta-ur-Rahman (ed.). Studies in Natural Products Chemistry, Vol. 7. Elsevier Science, Amsterdam.

    Google Scholar 

  • Boros, C. A. and Stermitz, F. R. 1990. Iridoids. An updated review. Part I. J. Nat. Prod. 53:1055–1147.

    Google Scholar 

  • Boros, C. A. and Stermitz, F. R. 1991. Iridoids. An updated review. Part II. J. Nat. Prod. 51:1173–1246.

    Google Scholar 

  • Bos, M., Harmens, H., and Vrieling. K. 1986. Gene flow in Plantago I. Gene flow and neighbourhood size in P. lanceolata. Heredity 56:43–54.

    Google Scholar 

  • Bowers, M. D. 1980. Unpalatability as a defense strategy of Euphydryas phaeton (Lepidoptera: Nymphalidae). Evolution 34:586–600.

    Google Scholar 

  • Bowers, M. D. 1983. The role of iridoid glycosides in host-plant specificity of checkerspot butterflies. J. Chem. Ecol. 9:475–493.

    Google Scholar 

  • Bowers, M. D. 1984. Iridoid glycosides and host-plant specificity in larvae of the buckeye butterfly, Junonia coenia (Nymphalidae). J. Chem. Ecol. 10:1567–1577.

    Google Scholar 

  • Bowers, M. D. 1991. Iridoid glycosides, pp. 297–325, in G. A. Rosenthal and M. R. Berenbaum (Eds.). Herbivores: Their Interactions With Secondary Plant Metabolites. Vol. 1: The Chemical Participants. 2nd ed. Academic Press, San Diego, California.

    Google Scholar 

  • Bowers, M. 1992. The evolution of unpalatability and the cost of chemical defense in insects, pp. 216–244, in B. D. Roitberg and M. B. Isman (Eds.). Insect Chemical Ecology: An Evolutionary Approach. Chapman and Hall, New York.

    Google Scholar 

  • Bowers, M. D. and Collinge, S. K. 1992. Fate of iridoid glycosides in different life stages of the buckeye, Junonia coenia (Lepidoptera: Nymphalidae). J. Chem. Ecol. 18:817–831.

    Google Scholar 

  • Bowers, M. D. and Farley, S. 1990. The behaviour of grey jays, Perisoreus canadensis, towards palatable and unpalatable Lepidoptera. Anim. Behav. 39:699–705.

    Google Scholar 

  • Bowers, M. D. and Puttick, G. M. 1986. Fate of ingested iridoid glycosides in lepidopteran herbivores. J. Chem. Ecol. 12:169–178.

    Google Scholar 

  • Bowers, M. D. and Puttick, G. M. 1988. Response of generalist and specialist insects to qualitative allelochemical variation. J. Chem. Ecol. 14:319–334.

    Google Scholar 

  • Bowers, M. D. and Stamp, N. E. 1992. Chemical variation within and between individuals of Plantago lanceolata (Plantaginaceae). J. Chem. Ecol. 18:985–995.

    Google Scholar 

  • Bowers, M. D. and Stamp, N. E. 1993. Effects of plant age, genotype, and herbivory on Plantago performance and chemistry. Ecology 74:1778–1791.

    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.

    Google Scholar 

  • Camara, M. D. 1997a. Physiological mechanisms underlying the costs of chemical defense in Junonia coenia Hübner (Nymphalidae): A gravimetric and quantitative genetic analyzis. Evol. Ecol. 11:451–469.

    Google Scholar 

  • Camara, M. D. 1997b. A recent host range expansion in Junonia coenia Hübner (Nymphalidae): oviposition preference, survival, growth, and chemical defense. Evolution 51:873–884.

    Google Scholar 

  • Camara, M. D. 1997c. Predator responses to sequestered plant toxins in buckeye caterpillars: Are tritrophic interactions locally variable? J. Chem. Ecol. 23:2093–2106.

    Google Scholar 

  • Campbell, B. C. and Duffey, S. F. 1979. Tomatine and parasitic wasps: Potential incompatibility of plant antibiosis with biological control. Science 205:700–702.

    Google Scholar 

  • Campbell, B. C. and Duffey, S. F. 1981. Alleviation of a-tomatine-induced toxicity to the parasitoid Hyposoter exiguae, by phytosterols in the diet of the host, Heliothis zea. J. Chem. Ecol. 7:927–946.

    Google Scholar 

  • Damtoft, S., Jensen, S. R., and Nielsen, B. J. 1983. The biosynthesis of iridoid glucosides from 8-epi-deoxyloganic acid. Biochem. Soc. Trans. 11:593–594.

    Google Scholar 

  • Damtoft, S., Franzyk, H., and Jensen, S. R. 1997. Iridoid glycosides from Picconia excelsa. Phytochemistry 45:743–750.

    Google Scholar 

  • Darrow, K. and Bowers, M. D. 1997. Phenological and population variation in iridoid glycosides of Plantago lanceolata (Plantaginaceae). Biochem. Syst. Ecol. 25:1–11.

    Google Scholar 

  • Darrow, K. and Bowers, M. D. 1999. Effects of herbivore damage and nutrient concentration on induction of iridoid glycosides in Plantago lanceolata. J. Chem. Ecol. 25:1427–1440.

    Google Scholar 

  • Dyer, L. A. 1995. Tasty generalists and nasty specialists? A comparative study of antipredator mechanisms in tropical lepidopteran larvae. Ecology 76:1483–1496.

    Google Scholar 

  • Dyer, L. A. and Bowers, M. D. 1996. The importance of sequestered iridoid glycosides as a defense against an ant predator. J. Chem. Ecol. 22:1527–1539.

    Google Scholar 

  • El-Naggar, L. J. and Beal, J. L. 1980. Iridoids. A review. J. Nat. Prod. 43:649–707.

    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.

    Google Scholar 

  • Gange, A. C. and West, H. M. 1994. Interactions between arbuscular mycorrhizal fungi and foliar-feeding insects in Plantago lanceolata L. New Phytol. 128:79–87.

    Google Scholar 

  • Gardner, R. D. and Stermitz, F. R. 1988. Host-plant utilization and iridoid glycoside sequestration by Euphydryas anicia (Lepidoptera: Nymphalidae). J. Chem. Ecol. 14:2147–2168.

    Google Scholar 

  • Hanski, I. 1999. Metapopulation Ecology. Oxford University Press, New York.

    Google Scholar 

  • Herms, D. A. and Mattson, W. J. 1992. The dilemma of plants: to grow or to defend. Q. Rev. Biol. 67:293–335.

    Google Scholar 

  • Inouye, H. 1991. Iridoids, pp. 99–143, in P. M. Dey and J. B. Harborne (Eds.). Methods in Plant Biochemistry, Vol. 7. Academic Press, San Diego, California.

    Google Scholar 

  • Jones, C. G. and Firn, R. D. 1991. On the evolution of plant secondary chemical diversity. Phil. Trans. R. Soc. London B 333:273–280.

    Google Scholar 

  • Judd, W. S., Campbell, C. S., Kellogg, E. A., and Stevens, P. F. 1999. Plant Systematics: A Phylogenetic Approach. Sinauer, Sunderland, Massachusetts.

    Google Scholar 

  • Koricheva, J., Larsson, S., and Haukioja, E. 1998. Insect performance on experimentally stressed woody plants: A meta-analyzis. Annu. Rev. Entomol. 43:195–216.

    Google Scholar 

  • Kuussaari, M., Singer, M., and Hanski, I. 2000. Local specialization and landscape-level influence on host use in an herbivorous insect. Ecology 81:2177–2187.

    Google Scholar 

  • Lei, G.-C. and Camara, M. D. 1999. Behaviour of a specialist parasitoid, Cotesia melitaearum: from individual behaviour to metapopulation processes. Ecol. Entomol. 24:59–72.

    Google Scholar 

  • Lei, G.-C. and Hanski, I. 1997. Metapopulation structure of Cotesia melitaearum, a specialist parasitoid of the butterfly Melitaea cinxia. Oikos 78:91–100.

    Google Scholar 

  • Lei, G.-C., Vikberg, V., Nieminen, M., and Kuussaari, M. 1997. The parasitoid complex attacking Finnish populations of the Glanville fritillary Melitaea cinxia (Lep: Nymphalidae), an endangered butterfly. J. Nat. Hist. 31:635–648.

    Google Scholar 

  • L'Empereur, K. M. and Stermitz, F. R. 1990a. Iridoid glycoside content of Euphydryas anicia (Lepidoptera: Nymphalidae) and its major hostplant, Besseya plantaginea (Scrophulariaceae), at a high plains Colorado site. J. Chem. Ecol. 16:187–197.

    Google Scholar 

  • L'Empereur, K. M. and Stermitz, F. R. 1990b. Iridoid glycoside metabolism and sequestration by Poladryas minuta (Lepidoptera: Nymphalidae) feeding on Penstemon virgatus (Scrophulariaceae). J. Chem. Ecol. 16:1495–1506.

    Google Scholar 

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

    Google Scholar 

  • Nieminen, M., Siljander, M., and Hanski, I. 2003. Structure and dynamics of Melitaea cinxia metapopulations, In P. R. Ehrlich and I. Hanski (Eds.). On the Wings of Checkerspots. Oxford University Press, New York. In press.

    Google Scholar 

  • Olmstead, R. G., dePamphilis, C. W., Wolfe, A. D., Young, N. D., Elisons, W. J., and Reeves, P. A. 2001. Disintegration of the Scrophulariaceae. Am. J. Bot. 88:348–361.

    Google Scholar 

  • Pereyra, P. C. and Bowers, M. D. 1988. Iridoid glycosides as oviposition stimulants for the buckeye butterfly, Junonia coenia (Nymphalidae). J. Chem. Ecol. 14:917–928.

    Google Scholar 

  • Puttick, G. M. and Bowers, M. D. 1988. Effect of qualitative and quantitative variation in allelochemicals on a generalist insect: Iridoid glycosides and the southern armyworm. J. Chem. Ecol. 14:335–351.

    Google Scholar 

  • Stamp, N. 1992. Relative susceptibility to predation of two species of caterpillars on plantain. Oecologia 92:124–129.

    Google Scholar 

  • Stamp, N. E. and Bowers, M. D. 1994. Effects of cages, plant age and mechanical clipping on plantain chemistry. Oecologia 99:66–71.

    Google Scholar 

  • Stamp, N. E. and Bowers, M. D. 2000. Do enemies of herbivores influence plant growth and chemistry? Evidence from a seminatural experiment. J. Chem. Ecol. 26:2367–2386.

    Google Scholar 

  • Stephenson, A. G. 1981. Toxic nectar deters nectar thieves of Catalpa speciosa. Am. Midl. Nat. 105:381–383.

    Google Scholar 

  • Stephenson, A. G. 1982. Iridoid glycosides in the nectar of Catalpa speciosa are unpalatable to nectar thieves. J. Chem. Ecol. 8:1025–1034.

    Google Scholar 

  • Stermitz, F. R., Gardner, D. R., Odendaal, F. J., and Ehrlich, P. R. 1986. Euphydryas anicia (Lepidoptera: Nymphalidae) utilization of iridoid glycosides from Castilleja and Besseya (Schrophulariaceae) host plants. J. Chem. Ecol. 12:1459–1468.

    Google Scholar 

  • Suomi, J., Sirén, H., Hartonen, K., and Riekkola, M.-L. 2000. Extraction of iridoid glycosides and their determination by micellar electrokinetic capillary chromatography. J. Chromatogr. A 868:73–83.

    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.

    Google Scholar 

  • Teramura, A. H. 1983. Experimental ecological genetics in Plantago IX. Differences in growth and vegetative reproduction in Plantago lanceolata L. (Plantaginaceae) from adjacent habitats. Am. J. Bot. 70:53–58.

    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.

    Google Scholar 

  • Thorpe, K. W. and Barbosa, P. 1986. Effects of consumption of high and low nicotine tobacco by Manduca sexta (Lepidoptera: Sphingidae) on the survival of gregarious endoparasitoid Cotesia congregata. J. Chem. Ecol. 12:1329–1337.

    Google Scholar 

  • van Nouhuys, S. and Hanski, I. 1999. Host diet affects extinctions and colonizations in a parasitoid metapopulation. J. Anim. Ecol. 68:1248–1258.

    Google Scholar 

  • van Nouhuys, S. and Hanski, I. 2002. Multitrophic interactions in space: metacommunity dynamics in fragmented landscapes, pp. 124–147, in T. Tscharntke and B. A. Hawkins (Eds.). Multitrophic Level Interactions. Cambridge University Press, Cambridge.

    Google Scholar 

  • van Nouhuys, S. and Hanski, I. 2003. Natural enemies of checkerspot butterflies, In P. R. Ehrlich and I. Hanski (Eds.). On the Wings of Checkerspots. Oxford University Press, New York, In press.

    Google Scholar 

  • van Tienderen, P. H. 1992. Variation in a population of Plantago lanceolata along a topographical gradient. Oikos 64:560–572.

    Google Scholar 

  • Zangerl, A. R. and Berenbaum, M. R. 1993. Plant chemistry, insect adaptations to plant chemistry, and host plant utilization patterns. Ecology 74:47–54.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Ecology and Systematics, Division of Population Biology, Biocenter 3, University of Helsinki, P.O. Box 65, FIN-00014, Finland

    Marko Nieminen & Saskya Van Nouhuys

  2. Department of Chemistry, Laboratory of Analytical Chemistry, P.O. Box 55, FIN-00014, University of Helsinki, Finland

    Johanna Suomi, Pauliina Sauri & Marja-Liisa Riekkola

Authors
  1. Marko Nieminen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Johanna Suomi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Saskya Van Nouhuys
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pauliina Sauri
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marja-Liisa Riekkola
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marko Nieminen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nieminen, M., Suomi, J., Van Nouhuys, S. et al. Effect of Iridoid Glycoside Content on Oviposition Host Plant Choice and Parasitism in a Specialist Herbivore. J Chem Ecol 29, 823–844 (2003). https://doi.org/10.1023/A:1022923514534

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1022923514534

Search

Navigation