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Journal of Chemical Ecology

, Volume 31, Issue 11, pp 2551–2561 | Cite as

Similarity of Cuticular Lipids Between a Caterpillar and Its Host Plant: A Way to Make Prey Undetectable for Predatory Ants?

  • Augusto Henrique
  • Arantes Portugal
  • José Roberto Trigo
Article

Abstract

Ithomiine butterflies (Nymphalidae) have long-lived, aposematic, chemically protected adults. However, little is known about the defense mechanisms in larvae and other juvenile stages. We showed that larvae Mechanitis polymnia are defended from ants by a chemical similarity between their cuticular lipids and those of the host plant, Solanum tabacifolium (Solanaceae). This is a novel defense mechanism in phytophagous insects. A field survey during one season showed that larval survivorship was up to 80%, which is high when compared with other juvenile stages. In a laboratory bioassay, live larvae on their host plant were not attacked by the predatory ant Camponotus crassus (Formicidae). Two experiments showed that the similarity between the cuticular lipids of M. polymnia and S. tabacifolium protected the larvae from C. crassus: (a) when the caterpillar was switched from a host plant to a non-host plant, the predation rate increased, and (b) when a palatable larva (Spodoptera frugiperda, Noctuidae) was coated with the cuticular lipids of M. polymnia and placed on S. tabacifolium leaves, it no longer experienced a high predation rate. This defensive mechanism can be defined as chemical camouflage, and may have a double adaptive advantage, namely, protection against predation and a reduction in the cost of sequestering toxic compounds from the host plant.

Key Words

Camponotus crassus cuticular hydrocarbons chemical camouflage chemical defense Formicidae Ithomiinae Mechanitis polymnia chemical mimicry Solanaceae Solanum tabacifolium 

Notes

Acknowledgments

This work is part of a Master of Science dissertation by AHAP and was supported by grants from FAPESP (98/01065-7 to JRT and 98/00765-5 to AHAP). The authors thank D. Whitmann, E. Bernays, P.S. Oliveira, A.V.L. Freitas, F. Nogueira-de-Sá, M. Hilker, and four anonymous reviewers for valuable comments on the manuscript. We thank also the Instituto Agronômico de Campinas, Fundação José Pedro de Oliveira de Campinas, Prefeitura Municipal de Jundiaí, and Instituto Botânico de São Paulo for permission to work in their areas.

References

  1. Bowers, M. D. 1993Aposematic caterpillars: life-styles of the warningly colored and unpalatableStamp, N.Casey, T. M. eds. Caterpillars. Ecological and Evolutionary Constraints on ForagingChapman & HallNew York, NY331371Google Scholar
  2. Brown, K. S.,Jr. 1984Adult obtained pyrrolizidine alkaloids defend Ithomiinae butterflies against a spider predatorNature309707709CrossRefGoogle Scholar
  3. Brown, K. S.,Jr. 1985Chemical ecology of dehydropyrrolizidine alkaloids in adult Ithomiinae (Lepidoptera: Nymphalidae)Rev. Bras. Biol.44435460Google Scholar
  4. Brown, K. S.,Jr. 1987Chemistry at the Solanaceae/Ithomiinae interfaceAnn. Mo. Bot. Gard.74359397Google Scholar
  5. Brown, K. S.,Jr., Freitas, A. V. L. 1994Juvenile stages of Ithomiinae: overview and systematics (Lepidoptera: Nymphalidae)Trop. Lep.5920Google Scholar
  6. Buckner, J. S. 1993Cuticular polar lipids of insectsStanley-Samuelson, D. W.Nelson, D. R. eds. Insect Lipids: Chemistry, Biochemistry and BiologyUniversity of Nebraska PressLincoln, NE227270Google Scholar
  7. Cornell, V. H., Hawkins, B. A. 1995Survival patterns and mortality sources of herbivorous insects: some demographic trendsAm. Nat.145563593CrossRefGoogle Scholar
  8. Dettner, K., Liepert, C. 1994Chemical mimicry and camouflageAnnu. Rev. Entomol.39129154CrossRefGoogle Scholar
  9. Drummond, B. A.,III, Brown, K. S.,Jr. 1987Ithomiinae (Lepidoptera: Nymphalidae): Summary of known larval foodplantsAnn. Mo. Bot. Gard.74341358Google Scholar
  10. Endler, J. A. 1981An overview of the relationships between mimicry and crypsisBiol. J. Linn. Soc.162331Google Scholar
  11. Espelie, K. E., Bernays, E. A., Brown, J. J. 1991Plant and insect cuticular lipids serve as behavioral cues for insectsArch. Insect Biochem. Physiol.17223233CrossRefGoogle Scholar
  12. Evans, D. L., Schmidt, J. O. 1990Insect Defenses. Adaptative Mechanisms and Strategies of Prey and PredatorsState University of New York PressAlbany, NYGoogle Scholar
  13. Fishlyn, D. A., Phillips, D. W. 1980Chemical camouflaging and behavioral defenses against a predatory seastar by 3 species of gastropods from the surf-grass Phyllospadix communityBiol. Bull.1583448Google Scholar
  14. Freitas, A. V. L., Oliveira, P. S. 1996Ants as selective agents on herbivore biology: effects on the behaviour of a non-myrmecophilous butterflyJ. Anim. Ecol.65205210Google Scholar
  15. Freitas, A. V. L., Trigo, J. R., Brown, K. S.,Jr., Witte, L., Hartmann, T., Barata, L. E. S. 1996Tropane and pyrrolizidine alkaloids in the ithomiines Placidula euryanassa and Miraleria cymothoe (Lepidoptera: Nymphalidae)Chemoecology76167CrossRefGoogle Scholar
  16. Haverty, M. I., Thorne, B. L., Nelson, L. J. 1996Hydrocarbons of Nasutitermes acajutlae and comparison of methodologies for sampling cuticular hydrocarbons of Caribbean termites for taxonomic and ecological studiesJ. Chem. Ecol.2220812110CrossRefGoogle Scholar
  17. Hay, M. E., Duffy, E., Fenical, W. 1990Host-plant specialization decreases predation on a marine amphipod: an herbivore in plant's clothingEcology71733743Google Scholar
  18. Hölldobler, B., Wilson, E. O. 1990The AntsThe Belknap Press of Harward UniversityCambridge, MAGoogle Scholar
  19. Howard, R. W. 1993Cuticular hydrocarbons and chemical communicationStanley-Samuelson, D. W.Nelson, D. R. eds. Insect Lipids: Chemistry, Biochemistry and BiologyUniversity of Nebraska PressLincoln, NE179226Google Scholar
  20. Howard, R. W., Blomquist, G. J. 2005Ecological, behavioral, and biochemical aspects of insects hydrocarbonsAnnu. Rev. Entomol.50371393CrossRefPubMedGoogle Scholar
  21. Howard, R. W., McDaniel, C. A., Blomquist, G. J. 1980Chemical mimicry as an integrating mechanism: cuticular hydrocarbons of a termitophile and its hostScience210431433Google Scholar
  22. Kusnezov, N. 1951El género Camponotus en la ArgentinaActa Zool. LilloanaXII183255Google Scholar
  23. Lenoir, A., D'Ettorre, P., Errard, C. 2001Chemical ecology and social parasitism in antsAnnu. Rev. Entomol.46573599CrossRefPubMedGoogle Scholar
  24. Masters, A. R. 1990Pyrrolizidine alkaloids in artificial nectar protect adult ithomiine butterflies from a spider predatorBiotropica22298304Google Scholar
  25. Masters, A. R. 1992. Chemical defense in Ithomiinae butterflies (Nymphalidae: Ithomiinae). PhD dissertation, University of Florida, Gainesville, FL.Google Scholar
  26. Nash, R. J., Rothschild, M., Porter, E. A., Watson, A. A., Waigh, R. D., Waterman, P. G. 1993Calystegines in Solanum and Datura species and the deaths-head hawk-mothPhytochemistry3412811283CrossRefGoogle Scholar
  27. Orivel, J., Dejean, A. 2000Myrmecophily in Hesperiidae. The case of Vettius tertianus in ant gardensLife Sci.323705715Google Scholar
  28. Orr, A. G., Trigo, J. R., Witte, L., Hartmann, T. 1996Sequestration of pyrrolizidine alkaloids by larvae of Tellervo zoilus (Lepidoptera: Ithomiinae) and their role in the chemical protection of adults against the spider Nephila maculata (Araneidae)Chemoecology76873CrossRefGoogle Scholar
  29. Portugal, A. H. A. 2001. Defesa química em larvas da borboleta Mechanitis polymnia (Nymphalidae: Ithomiinae). MSc dissertation. Universidade Estadual de Campinas. Campinas, São Paulo, BrazilGoogle Scholar
  30. Salazar, B. A., Whitman, D. W. 2001Defensive tactics of caterpillars against predators and parasitoidsAnanthakrishnan, T. N. eds. Insect and Plant Defense DynamicsScience Publishers Inc.Portland, OR161207Google Scholar
  31. Singer, T. 1998Roles of hydrocarbons in the recognition systems of insectsAm. Zool.38394405Google Scholar
  32. Smiley, J. T. 1985Heliconius caterpillars mortality during establishment on plants with and without attending antsEcology67516521Google Scholar
  33. Stachowicz, J. J., Hay, M. E. 1999Reducing predation through chemically mediated camouflage: indirect effects of plant defenses on herbivoresEcology80495509Google Scholar
  34. Stowe, M. K. 1988Chemical mimicrySpencer, K. C. eds. Chemical Mediation of CoevolutionAcademic PressNew York, NY513580Google Scholar
  35. Trigo, J. R., Brown, K. S.,Jr. 1990Variation of pyrrolizidine alkaloids in Ithomiinae: a comparative study between species feeding on Apocynaceae and SolanaceaeChemoecology12229CrossRefGoogle Scholar
  36. Trigo, J. R., Brown, K. S.,Jr., Witte, L., Hartmann, T., Ernst, L., Barata, L. E. S. 1996Pyrrolizidine alkaloids: different acquisition and use patterns in Apocynaceae and Solanaceae feeding ithomiine butterflies (Lepidoptera: Nymphalidae)Biol. J. Linn. Soc.5899123CrossRefGoogle Scholar
  37. Meer, R. K., Morel, L. 1998Nestmate recognition in antsMeer, R. K.Breed, M. D.Winston, M. L.Espelie, K. E. eds. Pheromone Communication in Social Insects. Ants, Wasps, Bees, and TermitesWestview PressBoulder, CO79103Google Scholar
  38. Meer, R. K., Wojcik, D. P. 1982Chemical mimicry in the myrmecophilous beetle Myrmecaphodius excavaticollisScience218806808Google Scholar
  39. Vane-Wright, R. I. 1976An unified classification of mimetic resemblancesBiol. J. Linn. Soc.82556Google Scholar
  40. Young, H. P., Schal, C. 1997Cuticular hydrocarbon synthesis in relation to feeding and developmental stage in nymphs of Blattella germanica (Dictyoptera: Blattellidae)Ann. Entomol. Soc. Am.90655663Google Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • Augusto Henrique
    • 1
  • Arantes Portugal
    • 1
  • José Roberto Trigo
    • 1
  1. 1.Laboratório de Ecologia Química, Departamento de Zoologia, Instituto de BiologiaUniversidade Estadual de Campinas (UNICAMP)CampinasBrazil

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