Advertisement

Journal of Chemical Ecology

, Volume 38, Issue 7, pp 893–901 | Cite as

Attenuation of the Jasmonate Burst, Plant Defensive Traits, and Resistance to Specialist Monarch Caterpillars on Shaded Common Milkweed (Asclepias syriaca)

  • Anurag A. Agrawal
  • Emily E. Kearney
  • Amy P. Hastings
  • Trey E. Ramsey
Article

Abstract

Plant responses to herbivory and light competition are often in opposing directions, posing a potential conflict for plants experiencing both stresses. For sun-adapted species, growing in shade typically makes plants more constitutively susceptible to herbivores via reduced structural and chemical resistance traits. Nonetheless, the impact of light environment on induced resistance has been less well-studied, especially in field experiments that link physiological mechanisms to ecological outcomes. Accordingly, we studied induced resistance of common milkweed (Asclepias syriaca, a sun-adapted plant), and linked hormonal responses, resistance traits, and performance of specialist monarch caterpillars (Danaus plexippus) in varying light environments. In natural populations, plants growing under forest-edge shade showed reduced levels of resistance traits (lower leaf toughness, cardenolides, and trichomes) and enhanced light-capture traits (higher specific leaf area, larger leaves, and lower carbon-to-nitrogen ratio) compared to paired plants in full sun. In a field experiment repeated over two years, only milkweeds growing in full sun exhibited induced resistance to monarchs, whereas plants growing in shade were constitutively more susceptible and did not induce resistance. In a more controlled field experiment, plant hormones were higher in the sun (jasmonic acid, salicylic acid, abscisic acid, indole acidic acid) and were induced by herbivory (jasmonic acid and abscisic acid). In particular, the jasmonate burst following herbivory was halved in plants raised in shaded habitats, and this correspondingly reduced latex induction (but not cardenolide induction). Thus, we provide a mechanistic basis for the attenuation of induced plant resistance in low resource environments. Additionally, there appears to be specificity in these interactions, with light-mediated impacts on jasmonate-induction being stronger for latex exudation than cardenolides.

Keywords

Cardenolide Herbivory Latex Monarch butterfly Plant defense Plant-insect interactions Shade-avoidance response Signal cross-talk Specialist herbivore 

Notes

Acknowledgements

We thank Gaylord Desurmont, Daisy Johnson, and Julia Kerr for help with field and lab work, Sergio Rasmann and Rayko Halitschke for critical guidance with chemical analyses, and Jared Ali, Alexis Erwin, Monica Kersch-Becker, Jennifer Thaler, and anonymous reviewers for helpful comments and discussion. All chemical analyses were conducted in the Cornell Chemical Ecology Group’s Core Facility and field work was conducted at Cornell Plantation's Durland Bird Preserve as well as other Cornell Natural Areas. Our lab (http://www.herbivory.com) and this research was supported by NSF DEB-1118783, NSF REU supplements that supported E.E.K. and T.E.R., and Cornell University Agricultural Experiment Station federal formula funds (Hatch project NYC-102400).

References

  1. Agrawal, A. A. 1998. Induced responses to herbivory and increased plant performance. Science 279:1201–1202.PubMedCrossRefGoogle Scholar
  2. Agrawal, A. A. 2004. Resistance and susceptibility of milkweed: competition, root herbivory, and plant genetic variation. Ecology 85:2118–2133.CrossRefGoogle Scholar
  3. Agrawal, A. A. 2005. Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evolutionary Ecology Research 7:651–667.Google Scholar
  4. Agrawal, A. A. 2011. Current trends in the evolutionary ecology of plant defence. Funct. Ecol. 25:420–432.CrossRefGoogle Scholar
  5. Agrawal, A. A. and FISHBEIN, M. 2006. Plant defense syndromes. Ecology 87:S132–S149.PubMedCrossRefGoogle Scholar
  6. Agrawal, A. A., Conner, J. K. and Rasmann, S. 2010. Tradeoffs and adaptive negative correlations in evolutionary ecology, pp. 243–268 in M. Bell, W. Eanes, D. Futuyma and J. Levinton (eds.), Evolution After Darwin: the First 150 Years. Sinauer Associates, Sunderland, MA.Google Scholar
  7. AGRAWAL, A. A., PETSCHENKA, G., BINGHAM, R. A., WEBER, M. G., and RASMANN, S. 2012. Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions. New Phytol 194:28–45.PubMedCrossRefGoogle Scholar
  8. Agrawal, A. A. and VAN ZANDT, P. A. 2003. Ecological play in the coevolutionary theatre: genetic and environmental determinants of attack by a specialist weevil on milkweed. J. Ecol. 91:1049–1059.CrossRefGoogle Scholar
  9. Auld, J. R., Agrawal, A. A., and Relyea, R. A. 2010. Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc. Royal Soc. B-Biological Sciences 277:503–511.CrossRefGoogle Scholar
  10. Bingham, R. A. and AGRAWAL, A. A. 2010. Specificity and trade-offs in the induced plant defence of common milkweed Asclepias syriaca to two lepidopteran herbivores. J. Ecol. 98:1014–1022.CrossRefGoogle Scholar
  11. Boege, K. 2010. Induced responses to competition and herbivory: natural selection on multi-trait phenotypic plasticity. Ecology 91:2628–2637.PubMedCrossRefGoogle Scholar
  12. Callaway, R. M., Pennings, S. C., and Richards, C. L. 2003. Phenotypic plasticity and interactions among plants. Ecology 84:1115–1128.CrossRefGoogle Scholar
  13. Cipollini, D. 2004. Stretching the limits of plasticity: Can a plant defend against both competitors and herbivores? Ecology 85:28–37.CrossRefGoogle Scholar
  14. Dudley, S. A. and Schmitt, J. 1996. Testing the adaptive plasticity hypothesis: Density-dependent selection on manipulated stem length in Impatiens capensis. Am. Nat. 147:445–465.CrossRefGoogle Scholar
  15. Dudt, J. F. and Shure, D. J. 1994. The influence of light and nutrients on foliar phenolics and insect herbivory. Ecology 75:86–98.CrossRefGoogle Scholar
  16. Guerra, P. C., Becerra, J., and Gianoli, E. 2010. Explaining differential herbivory in sun and shade: the case of Aristotelia chilensis saplings. Arthropod-Plant Interact. 4:229–235.CrossRefGoogle Scholar
  17. Herms, D. A. and MATTSON, W. J. 1992. The dilemma of plants: to grow or defend. Quart. Rev. Biol. 67:283–335.CrossRefGoogle Scholar
  18. Izaguirre, M. M., Mazza Cabiondini, M., Baldwin, I. T., and Ballare, C. L. 2006. Remote sensing of future competitors: Impacts on plant defenses. Proc. Natl. Acad. Sci. USA 103:7170–7174.PubMedCrossRefGoogle Scholar
  19. Jansen, M. P. T. and STAMP, N. E. 1997. Effects of light availability on host plant chemistry and the consequences for behavior and growth of an insect herbivore. Entomol. Exper. Appl. 82:319–333.CrossRefGoogle Scholar
  20. Kephart, S. R. 1981. Breeding systems in Asclepias incarnata L Asclepias syriaca L and Asclepias verticillata L. Am. J. Bot. 68:226–232.CrossRefGoogle Scholar
  21. Koricheva, J. 1999. Interpreting phenotypic variation in plant allelochemistry: Problems with the use of concentrations. Oecologia 119:467–473.CrossRefGoogle Scholar
  22. Kurashige, N. S. and AGRAWAL, A. A. 2005. Phenotypic plasticity to light competition and herbivory in Chenopodium album. Am. J. Bot. 92:21–26.PubMedCrossRefGoogle Scholar
  23. Mooney, E. H., Tiedeken, E. J., Muth, N. Z., and Niesenbaum, R. A. 2009. Differential induced response to generalist and specialist herbivores by Lindera benzoin (Lauraceae) in sun and shade. Oikos 118:1181–1189.CrossRefGoogle Scholar
  24. Mooney, K. A., Jones, P., and Agrawal, A. A. 2008. Coexisting congeners: Demography, competition, and interactions with cardenolides for two milkweed-feeding aphids. Oikos 117:450–458.CrossRefGoogle Scholar
  25. Moreno, J. E., Tao, Y., Chory, J., and Ballare, C. L. 2009. Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proc. Natl. Acad. Sci. USA 106:4935–4940.PubMedCrossRefGoogle Scholar
  26. MORGAN, D. C. and SMITH, H. 1981. Non-photosynthetic responses to light quality, pp. 109–134, in O. L. Lange, P. S. Nobel, C. B. Osmond, and H. Ziegler (eds.), Encylcopedia of Plant Physiology New Series. Springer, Berlin.Google Scholar
  27. MUTH, N. Z., KLUGER, E. C., LEVY, J. H., EDWARDS, M. J., and NIESENBAUM, R. A. 2008. Increased per capita herbivory in the shade: Necessity, feedback, or luxury consumption? Ecoscience 15:182–188.CrossRefGoogle Scholar
  28. Radhika, V., Kost, C., Mithofer, A., and Boland, W. 2010. Regulation of extrafloral nectar secretion by jasmonates in lima bean is light dependent. Proc. Natl. Acad. Sci. USA 107:17228–17233.PubMedCrossRefGoogle Scholar
  29. Rasmann, S., Johnson, M. D., and AGRAWAL, A. A. 2009. Induced responses to herbivory and jasmonate in three milkweed species. J. Chem. Ecol. 35:1326–1334.PubMedCrossRefGoogle Scholar
  30. Roberts, M. R. and PAUL, N. D. 2006. Seduced by the dark side: integrating molecular and ecological perspectives on the inflence of light on plant defence against pests and pathogens. New Phytol. 170:677–699.PubMedCrossRefGoogle Scholar
  31. ROZENDAAL, D. M. A., HURTADO, V. H., and POORTER, L. 2006. Plasticity in leaf traits of 38 tropical tree species in response to light: relationships with light demand and adult stature. Funct. Ecol. 20:207–216.CrossRefGoogle Scholar
  32. Salgado-Luarte, C. and Gianoli, E. 2010. Herbivory on temperate rainforest seedlings in sun and shade: Resistance, tolerance and habitat distribution. Plos One 5:e11460.PubMedCrossRefGoogle Scholar
  33. Salgado-Luarte, C. and Gianoli, E. 2011. Herbivory may modify functional responses to shade in seedlings of a light-demanding tree species. Funct. Ecol. 25:492–499.CrossRefGoogle Scholar
  34. Sipura, M. and Tahvanainen, J. 2000. Shading enhances the quality of willow leaves to leaf beetles - but does it matter? Oikos 91:550–558.CrossRefGoogle Scholar
  35. Thaler, J. S., Agrawal, A. A., and Halitschke, R. 2010. Salicylate-mediated interactions between pathogens and herbivores. Ecology 91:1075–1082.PubMedCrossRefGoogle Scholar
  36. Van Dam, N. M. and BALDWIN, I. T. 2001. Competition mediates costs of jasmonate-induced defences, nitrogen acquisition and transgenerational plasticity in Nicotiana attenuata. Funct. Ecol. 15:406–415.CrossRefGoogle Scholar
  37. Van Zandt P. A. and AGRAWAL, A. A. 2004. Specificity of induced plant responses to specialist herbivores of the common milkweed, Asclepias syriaca. Oikos 104:401–409.CrossRefGoogle Scholar
  38. Zalucki, M. P., Brower, L. P., and Alonso, A. 2001. 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. Ecolog. Entomol. 26:212–224.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Anurag A. Agrawal
    • 1
  • Emily E. Kearney
    • 1
  • Amy P. Hastings
    • 1
  • Trey E. Ramsey
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyCornell UniversityIthacaUSA

Personalised recommendations