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Journal of Chemical Ecology

, Volume 31, Issue 12, pp 2835–2846 | Cite as

Phenological Variation in Chemical Defense of the Pipevine Swallowtail, Battus philenor

  • James A. Fordyce
  • Zachary H. Marion
  • Arthur M. Shapiro
Article

Abstract

Larvae of the pipevine swallowtail, Battus philenor, feed on plants in the genus Aristolochia, which contains aristolochic acids, toxic alkaloids unique to the Aristolochiaceae. Pipevine swallowtails sequester these compounds and, as a consequence, are chemically defended against many natural enemies. In California, the primary aristolochic acid present in the butterfly is aristolochic acid I. Newly eclosed adult females possess greater amounts of these sequestered toxins compared to males. However, over the course of the flight season, the aristolochic acid content of females in the population declines, whereas male aristolochic acid content remains relatively constant. Transference of sequestered aristolochic acids to eggs by females might explain the decline of these sequestered chemical defenses observed over time. We found no evidence that males transfer aristolochic acids to females via the spermatophore. The possibility that females at the end of the flight season may be automimics of males is discussed. Temporal variation in the aristolochic acid defenses exhibited by this pipevine swallowtail population is both age- and sex-dependent.

Key Words

Aristolochic acid chemical defense sequestration phenological variation pipevine swallowtail Battus philenor automimicry 

Notes

Acknowledgments

We thank Chris Nice, Michelle Boercker, Mary Caflisch, Lisa McDonald, and two anonymous reviewers for helpful comments and suggestions. Thanks to Shorty Boucher and Dan Tolson of the University of California Natural Reserve System for providing access to Stebbins Cold Canyon Reserve. This study was supported by the University of Tennessee, Center for Population Biology (UC-Davis), and the U.S. National Science Foundation (DEB-9306721 to A.M.S. and DBI-0317483 to A.M.S. and James Quinn).

References

  1. Alonso-Mejía, A., Brower, L. P. 1994From model to mimic-age-dependent unpalatability in monarch butterfliesExperientia50176181CrossRefGoogle Scholar
  2. Brower, J. V. Z. 1958Experimental studies of mimicry in some North American butterflies. Part II. Battus philenor and Papilio troilus and P. polyxenes and P. glaucusEvolution12123136Google Scholar
  3. Brower, L. P. 1984Chemical defence in butterfliesVane-Wright, R. I.Ackery, P. R. eds. The Biology of ButterfliesAcademic PressNew York109134Google Scholar
  4. Brower, L. P., Brower, J. V. Z. 1962The relative abundance of model and mimic butterflies in natural populations of the Battus philenor mimicry complexEcology43154158Google Scholar
  5. Chen, Z. L., Zhu, D. Y. 1987Aristolochia alkaloidsBrossi, A. eds. The Alkaloids: Chemistry and PharmacologyAcademic PressSan Diego2965Google Scholar
  6. Codella, S. G., Lederhouse, R. C. 1989Intersexual comparison of mimetic protection in the black swallowtail butterfly, Papilio polyxenes: Experiments with captive blue jay predatorsEvolution43410420Google Scholar
  7. Dixon, C. A., Erickson, J. M., Kellett, D. N., Rothschild, M. 1978Some adaptations between Danaus-Plexippus and its food plant, with notes on Danaus chrysippus and Euploea core (Insecta Lepidoptera)J. Zool.185437467Google Scholar
  8. Dussourd, D. E., Harvis, C. A., Meinwald, J., Eisner, T. 1989Paternal allocation of sequestered plant pyrrolizidine alkaloid to eggs in the danaine butterfly, Danaus gilippusExperientia45896898PubMedCrossRefGoogle Scholar
  9. Fordyce, J. A. 2000A model without a mimic: Aristolochic acids from the California pipevine swallowtail, Battus philenor hirsuta, and its host plant, Aristolochia californicaJ. Chem. Ecol.2625672578Google Scholar
  10. Fordyce, J. A. 2001The lethal plant defense paradox remains: inducible host-plant aristolochic acids and the growth and defense of the pipevine swallowtailEntomol. Exp. Appl.100339346CrossRefGoogle Scholar
  11. Fordyce, J. A. 2003Aggregative feeding of pipevine swallowtail larvae enhances host-plant suitabilityOecologia135250257PubMedGoogle Scholar
  12. Fordyce, J. A., Nice, C. C. 2003Contemporary patterns in a historical context: Phylogeographic history of the pipevine swallowtail, Battus philenor (Papilionidae)Evolution5710891099PubMedGoogle Scholar
  13. Gonzalez, A., Rossini, C., Eisner, M., Eisner, T. 1999Sexually transmitted chemical defense in a moth (Utetheisa ornatrix)Proc. Natl. Acad. Sci. USA9655705574PubMedGoogle Scholar
  14. Jeffords, M. R., Sternburg, J. G., Waldbauer, G. P. 1979Batesian mimicry: field demonstration of the survival value of pipevine swallowtail and monarch color patternsEvolution33275286Google Scholar
  15. Kassarov, L. 1999Are birds able to taste and reject butterflies based on ‘beak mark tasting’? Adifferent point of viewBehaviour136965981CrossRefGoogle Scholar
  16. Malcolm, S. B., Brower, L. P. 1989Evolutionary and ecological implications of cardenolide sequestration in the monarch butterflyExperientia45284295CrossRefGoogle Scholar
  17. Malcolm, S. B., Cockrell, B. J., Brower, L. P. 1989Cardenolide fingerprint of monarch butterflies reared on common milkweed, Asclepias syriaca LJ. Chem. Ecol.15819854Google Scholar
  18. Moranz, R., Brower, L. P. 1998Geographic and temporal variation of cardenolide-based chemical defenses of queen butterfly (Danaus gilippus) in northern FloridaJ. Chem. Ecol.24905932CrossRefGoogle Scholar
  19. Nelson, C. J., Seiber, J. N., Brower, L. P. 1981Seasonal and intraplant variation of cardenolide content in the California milkweed, Asclepias eriocarpa, and implications for plant defenseJ. Chem. Ecol.79811010CrossRefGoogle Scholar
  20. Nishida, R. 2002Sequestration of defensive substances from plants by LepidopteraAnnu. Rev. Entomol.475792PubMedCrossRefGoogle Scholar
  21. Nishida, R., Fukami, H. 1989Ecological adaptation of an Aristolochiaceae-feeding swallowtail butterfly, Atrophaneura alcinous, to aristolochic acidsJ. Chem. Ecol.1525492564Google Scholar
  22. Platt, A. P., Coppinger, R. P., Brower, L. P. 1971Demonstration of the selective advantage of mimetic Limenitis butterflies presented to caged avian predatorsEvolution5692701Google Scholar
  23. Racheli, T., Pariset, L. 1992II genere Battus tassonomia e storia naturaleFragm. Entomol. (Roma) (Suppl.)231163Google Scholar
  24. Ritland, D. B. 1994Variation in palatability of Queen butterflies (Danaus gilippus) and implications regarding mimicryEcology75732746Google Scholar
  25. Rothschild, M., Keutmann, H., Lane, N. J., Parsons, J., Prince, W., Swales, L. S. 1979Study on the mode of action and composition of a toxin from the female abdomen and eggs of Arctia caja (L.) (Lep Arctiidae)—electro-physiological, ultrastructural and biochemical analysisToxicon17285306PubMedCrossRefGoogle Scholar
  26. Sime, K. R., Feeny, P. P., Haribal, M. M. 2000Sequestration of aristolochic acids by the pipevine swallowtail, Battus philenor (L.): evidence and ecological implicationsChemoecology10169178Google Scholar
  27. Stamp, N. E. 1980Egg deposition patterns in butterflies: Why do some species cluster their eggs rather than deposit them singly?Am. Nat.115367380CrossRefGoogle Scholar
  28. Uesugi, K. 1996The adaptive significance of Batesian mimicry in the swallowtail butterfly, Papilio polytes (Insecta, Papilionidae): Associative learning in a predatorEthology102762775Google Scholar
  29. Urzua, A., Priestap, H. 1985Aristolochic acids from Battus polydamasBiochem. Syst. Ecol.13169170Google Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • James A. Fordyce
    • 1
  • Zachary H. Marion
    • 1
  • Arthur M. Shapiro
    • 2
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of TennesseeKnoxvilleUSA
  2. 2.Section of Evolution and Ecology and Center for Population BiologyUniversity of CaliforniaDavisUSA

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