Journal of Chemical Ecology

, Volume 33, Issue 11, pp 2044–2053 | Cite as

Interspecific Variation Within the Genus Asclepias in Response to Herbivory by a Phloem-feeding Insect Herbivore

  • Caralyn B. Zehnder
  • Mark D. Hunter


Induced plant responses to leaf-chewing insects have been well studied, but considerably less is known about the effects of phloem-feedings insects on induction. In a set of laboratory experiments, we examined density-dependent induction by the milkweed-oleander aphid, Aphis nerii, of putative defenses in four milkweed species (Asclepias incarnata, Asclepias syriaca, Asclepias tuberosa, and Asclepias viridis). We hypothesized that high aphid density would lead to increased cardenolide expression in species with low constitutive levels of cardenolides (e.g., A. tuberosa), but that there would be no induction in high constitutive cardenolide species (e.g., A. viridis). Based on previous studies, we did not expect cardenolide induction in A. incarnata. Contrary to our predictions, we observed feeding-induced declines of cardenolide concentrations in A. viridis. Cardenolide concentrations did not respond to aphid feeding in the other three milkweed species. Aphids also caused reductions in biomass accumulation by two of four Asclepias species, A. viridis and A. incarnata. High aphid density led to a decrease in A. viridis foliar nitrogen concentration. However, aphids had no effect on the defensive chemistry, growth, or nutritional quality of either A. syriaca or A. tuberosa. Our results highlight that congeneric plant species may respond differently to the same levels of herbivore damage.


Aphis nerii Asclepias Cardenolide Density-dependence Induction milkweeds Plant defense 



We thank J. Castings, P. Doty, M. Fleming, T. Maddox, and S. Scott for laboratory and field assistance. We thank B. Ball, W. Duncan, K. Wickings, and four anonymous reviewers for helpful suggestions concerning this manuscript.


  1. Agrawal, A. A. 2000. Benefits and costs of induced plant defense for Lepidium virginicum (Brassicaceae). Ecology 81:1804–1813.Google Scholar
  2. Agrawal, A. A. 2004. Plant defense and density-dependence in the population growth of herbivores. Am. Nat. 164:113–120.PubMedCrossRefGoogle Scholar
  3. Agrawal, A. A., and Malcolm, S. B. 2002. Once upon a milkweed—In this complex community, one insects poison may be another’s meal. Nat. Hist. 111:48–53.Google Scholar
  4. Agrawal, A. A., and Fishbein, M. 2006. Plant defense syndromes. Ecology 87:S132–S149.PubMedCrossRefGoogle Scholar
  5. Boege, K., and Marquis, R. J. 2005. Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol. Evol. 20:441–448.PubMedCrossRefGoogle Scholar
  6. Brower, L. P., Seiber, J. N., Nelson, C. J., Lynch, S. P., and Holland, M. M. 1984. Plant-determined variation in the cardenolide content, thin-layer chromatography profiles, and emetic potency of monarch butterflies, Danaus-plexippus L (Lepidoptera, Danaidae) reared on milkweed plants in California .2. Asclepias speciosa (Apocynales, Asclepiadaceae). J. Chem. Ecol. 10:601–639.CrossRefGoogle Scholar
  7. Cardoza, Y. J., Reidy-Crofts, J., and Edwards, O. R. 2005. Differential inter- and intra-specific defense induction in Lupinus by Myzus persicae feeding. Entomol. Exp. Appl. 117:155–163.CrossRefGoogle Scholar
  8. Carroll, C. R., and Hoffman, C. A. 1980. Chemical feeding deterrent mobilized in response to insect herbivory and counteradaptation by Epilachna tredecimnotata. Science 209:414–416.PubMedCrossRefGoogle Scholar
  9. De Moraes, C. M., Lewis, W. J., Pare, P. W., Alborn, H. T., and Tumlinson, J. H. 1998. Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573.CrossRefGoogle Scholar
  10. Fordyce, J. A. 2001. The lethal plant defense paradox remains: Inducible host-plant aristolochic acids and the growth and defense of the pipevine swallowtail. Entomol. Exp. Appl. 100:339–346.CrossRefGoogle Scholar
  11. Gianoli, E. 2002. A phenotypic trade-off between constitutive defenses and induced responses in wheat seedlings. Ecoscience 9:482–488.Google Scholar
  12. Gianoli, E., and Niemeyer, H. M. 1997. Characteristics of hydroxamic acid induction in wheat triggered by aphid infestation. J. Chem. Ecol. 23:2695–2705.CrossRefGoogle Scholar
  13. Green, T. R., and Ryan, C. A. 1972. Wound induced proteinase inhibitor in plant leaves—Possible defense mechanism against insects. Science 175:776–777.PubMedCrossRefGoogle Scholar
  14. Groeters, F. R. 1993. Tests for host-associated fitness trade-offs in the milkweed-oleander aphid. Oecologia 93:406–411.CrossRefGoogle Scholar
  15. Helms, S. E., Connelly, S. J., and Hunter, M. D. 2004. Effects of variation among plant species on the interaction between a herbivore and its parasitoid. Ecol. Entomol. 29:44–51.CrossRefGoogle Scholar
  16. Karban, R., and Baldwin, I. T. 1997. Induced Responses to Herbivory. Chicago University Press, Chicago.Google Scholar
  17. Koricheva, J., Nykanen, H., and Gianoli, E. 2004. Meta-analysis of trade-offs among plant antiherbivore defenses: Are plants jacks-of-all-trades, masters of all? Am. Nat. 163:E64–E75.PubMedCrossRefGoogle Scholar
  18. Malcolm, S. B. 1989. Disruption of web structure and predatory behavior of a spider by plant-derived chemical defenses of an aposematic aphid. J. Chem. Ecol. 15:1699–1716.CrossRefGoogle Scholar
  19. Malcolm, S. B. 1991. Cardenolide-mediated interactions between plants and herbivores, in G. A. Rosenthal, M. R. Berenbaum, (eds.). Herbivores: Their Interactions with Secondary Plant Metabolites. Academic, San DiegoGoogle Scholar
  20. Malcolm, S. B., and Brower, L. P. 1989. Evolutionary and ecological implications of cardenolide sequestration in the monarch butterfly. Experientia 45:284–294.CrossRefGoogle Scholar
  21. Malcolm, S. B., and Zalucki, M. P. 1996. Milkweed latex and cardenolide induction may resolve the lethal plant defence paradox. Entomol. Exp. Appl. 80:193–196.CrossRefGoogle Scholar
  22. Martel, J. W., and Malcolm, S. B. 2004. Density-dependent reduction and induction of milkweed cardenolides by a sucking insect herbivore. J. Chem. Ecol. 30:545–561.PubMedCrossRefGoogle Scholar
  23. Malcolm, S. B., Cockrell, B. J., and Brower, L. P. 1989. Cardenolide fingerprint of monarch butterflies reared on common milkweed, Asclepias syriaca. J. Chem. Ecol. 15:819–853.CrossRefGoogle Scholar
  24. Nelson, C. J., Seiber, J. N., and Brower, L. P. 1981. Seasonal and intraplant variation of cardenolide content in the California milkweed, Asclepias eriocarpa, and implications for plant defense. J. Chem. Ecol. 7:981–1010.CrossRefGoogle Scholar
  25. Sauge, M. H., Mus, F., Lacroze, J. P., Pascal, T., Kervella, J., and Poessel, J. L. 2006. Genotypic variation in induced resistance and induced susceptibility in the peach—Myzus persicae aphid system. Oikos 113:305–313.CrossRefGoogle Scholar
  26. Sokal, R. R., and Rohlf, F. J. 1995. Biometry: The Principles and Practice of Statistics in Biological Research. W.H. Freeman & Company, New York.Google Scholar
  27. Strauss, S. Y., Rudgers, J. A., Lau, J. A., and Irwin, R. E. 2002. Direct and ecological costs of resistance to herbivory. Trends Ecol. Evol. 17:278–285.CrossRefGoogle Scholar
  28. Takada, H., and Miyazaki, M. 1993. Bisexual reproduction of a form of Aphis nerii B–De–F (Homoptera, Aphididae) from Hokkaido. Appl. Entomol. Zool. 28:199–205.Google Scholar
  29. Thaler, J. S., and Karban, R. 1997. A phylogenetic reconstruction of constitutive and induced resistance in Gossypium. Am. Nat. 149:1139–1146.CrossRefPubMedGoogle Scholar
  30. Vilarino, M. D., Mareggiani, G., Grass, M. Y., Leicach, S. R., and Ravetta, D. A. 2005. Post-damage alkaloid concentration in sweet and bitter lupin varieties and its effect on subsequent herbivory. J. Appl. Entomol. 129:233–238.CrossRefGoogle Scholar
  31. Warashina, T., and Noro, T. 2000. Cardenolide and oxypregnane glycosides from the root of Asclepias incarnata L. Chem. Pharm. Bull. 48:516–524.PubMedGoogle Scholar
  32. Woodson, R. E. 1954. The North American species of Asclepias L. Ann. Mo. Bot. Gard. 41:1–211.CrossRefGoogle Scholar
  33. Zalucki, M. P., Brower, L. P., and Alonso, A. 2001a. Detrimental effects of latex and cardiac glycosides on survival and growth of first-instar monarch butterfly larvae Danaus plexippus feeding on the sandhill milkweed Asclepias humistrata. Ecol. Entomol. 26:212–224.CrossRefGoogle Scholar
  34. Zalucki, M. P., Malcolm, S. B., Paine, T. D., Hanlon, C. C., Brower, L. P., and Clarke, A. R. 2001b. It’s the first bites that count: Survival of first-instar monarchs on milkweeds. Austral Ecol. 26:547–555.CrossRefGoogle Scholar
  35. Zehnder, C. B., and Hunter, M. D. 2007. A comparison of maternal effects and current environment on vital rates of Aphis nerii, the milkweed–oleander aphid. Ecol. Entomol. 32:172–180.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  1. 1.Institute of EcologyUniversity of GeorgiaAthensUSA
  2. 2.Department of Ecology and Evolutionary Biology and School of Natural Resources and EnvironmentUniversity of MichiganAnn ArborUSA

Personalised recommendations