Host plant defense signaling in response to a coevolved herbivore combats introduced herbivore attack

Abstract

Defense-free space resulting from coevolutionarily naïve host plants recently has been implicated as a factor facilitating invasion success of some insect species. Host plants, however, may not be entirely defenseless against novel herbivore threats. Volatile chemical-mediated defense signaling, which allows plants to mount specific, rapid, and intense responses, may play a role in systems experiencing novel threats. Here we investigate defense responses of host plants to a native and exotic herbivore and show that (1) host plants defend more effectively against the coevolved herbivore, (2) plants can be induced to defend against a newly-associated herbivore when in proximity to plants actively defending against the coevolved species, and (3) these defenses affect larval performance. These findings highlight the importance of coevolved herbivore-specific defenses and suggest that naïveté or defense limitations can be overcome via defense signaling. Determining how these findings apply across various host–herbivore systems is critical to understand mechanisms of successful herbivore invasion.

References Agrawal, A. A. 1998. Induced responses to herbivory and increased plant performance. Science 279:1201–1202. Alborn, H. T., T. C. J. Turlings, T. H. Jones, G. Stenhagen, J. H. Loughrin, and J. H. Tumlinson. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949. Arimura, G., K. Shiojiri, and R. Karban. 2010. Acquired immunity to herbivory and allelopathy caused by airborne plant emissions. Phytochemistry 71:1642–1649. Baker, A. J., and P. Stiling. 2009. Comparing the effects of the exotic cactus-feeding moth Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) and the native cactus-feeding moth Melitara prodenialis (Walker) (Lepidoptera: Pyralidae) on two species of Florida Opuntia. Biol. Invasions 11:619–624. Baldwin, I. T., and J. C. Schultz. 1983. Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science 221:277–279. Benrey, B., and R. F. Denne. 1997. The slow growth—high mortality hypothesis: a test using the cabbage butterfly. Ecology 78:987–999. Berger, D., R. Walters, and K. Gotthard. 2006. What keeps insects small? Size dependent predation on two species of butterfly larvae. Evol. Ecol. 20:575–589. Carlton, C. E., and T. J. Kring. 1994. Melitara prodenialis Walker on prickly pear in Arkansas. Southwest Entomol. 19:23–32. Chen, M.-S. 2008. Inducible direct plant defense against insect herbivores: a review. Insect. Sci. 15:101–114. Coley, P. D., L. M. Bateman, and T. A. Kursar. 2006. The effects of plant quality on caterpillar growth and defense against natural enemies. Oikos 115:219–228. Cornelissen, T., and P. Stiling. 2006. Does low nutritional quality act as a plant defense? An experimental test of the slow-growth, high-mortality hypothesis. Ecol. Entomol. 31:32–40. Desurmont, G. A., M. J. Donoghue, W. L. Clement, and A. A. Agrawal. 2011. Evolutionary history predicts plant defense against an invasive pest. Proc. Natl. Acad. Sci. U.S.A. 108:7070–7074. Dicke, M. 2009. Behavioral and community ecology of plants that cry for help. Plant Cell. Environ. 32:654–665. Dicke, M., and I. T. Baldwin. 2010. The evolutionary context for herbivore induced plant volatiles: beyond the “cry for help”. Trends Plant Sci. 15:167–175. Dodd, A. P. 1940. The biological campaign against prickly pear. Commonwealth Prickly Pear Board, Brisbane , pp. 177. Engelberth, J., H. T. Alborn, E. A. Schmelz, and J. H. Tumlinson. 2004. Airborne signals prime plants against insect herbivore attack. Proc. Natl. Acad. Sci. U.S.A. 101:1781–1785. Farmer, E. E. 2001. Surface-to-air signals. Nature 411:854–856. Felton, G. W., and J. H. Tumlinson. 2008. Plant–insect dialogs: complex interactions at the plant–insect interface. Curr. Opin. Plant Biol. 11:457–463. Frost, C. J., M. C. Mescher, J. E. Carlson, and C.M. De Moraes. 2008. Plant defense priming against herbivores: getting ready for a different battle. Plant Physiol. 146:818–824. Gandhi, K. J. K., and D. A. Herms. 2009. Direct and indirect effects of alien insect herbivores on ecological processes and interactions in forests of eastern North America. Biol. Invasions 12:389–405. Gurr, G. M., and O. L. Kvedaras. 2010. Synergizing biological control: scope for sterile insect technique, induced plant defenses and cultural techniques to enhance natural enemy impact. Biol. Control. 52:198–207. Habeck, D. H., and F. D. Bennett. 1990. Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae), a Phycitine new to Florida. Entomology Circular 333. Florida Department of Agriculture and Consumer Services Division of Plant Industry, Florida . Häggström, H., and S. Larsson. 1995. Slow larval growth on a suboptimal willow results in high predation mortality in the leaf beetle Galerucella lineola. Oceologia 104:308–315. Heil, M., and R. Karban. 2010. Explaining evolution of plant communication by airborne signals. Trends Ecol. Evol. 25:137–144. Heil, M., and J. C. Silva Bueno. 2007. Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc. Natl. Acad. Sci. U.S.A. 104:5467–5472. Honĕk, A. 1993. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos 66:483–492. Kant, M. R., and I. T. Baldwin. 2007. The ecogenetics and ecogenomics of plant herbivore interactions: rapid progress on a slippery road. Curr. Opin. Genet. Dev. 17:519–524. Karban, R. 2011. The ecology and evolution of induced resistance against herbivores. Funct. Ecol. 25:339–347. Karban, R., and I. T. Baldwin. 1997. Induced responses to herbivory. The University of Chicago Press, Chicago , pp. 330. Karban, R., K. Shiojiri, and S. Ishizaki. 2010. An air transfer experiment confirms the role of volatile cues in communication between plants. Am. Nat. 176:381–384. Kessler, A., and I. T. Baldwin. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144. Khan, Z. R., D. G. James, C. A. O. Midega, and J. A. Pickett. 2008. Chemical ecology and conservation biological control. Biol. Control. 45:210–224. Legaspi, J. C., and B. C. Legaspi. 2007. Life table analysis for Cactoblastis cactorum immature and female adults under five constant temperatures: implications for pest management. Ann. Entomol. Soc. Am. 100:497–505. Legaspi, B. C., and J. C. Legaspi. 2010. Field level validation of a CLIMEX model for Cactoblastis cactorum (Lepidoptera: Pyralidae) using estimated larval growth rates. Environ. Entomol. 39:368–377. Madsen, J. D. 2011. Cactus Moth Detection & Monitoring Network. Available at: http://www.gri.msstate.edu/research/cmdmn, GeoResources Institute. Accessed 8 September 2011. Mafokoane, L. D., H. G. Zimmermann, and M. P. Hill. 2007. Development of Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) on six North American Opuntia species. Afr. Entomol. 15:295–299. Marti, O. G., R. E. Myers, and J. E. Carpenter. 2008. Rearing Cactoblastis cactorum (Lepidoptera: Pyralidae) on artificial diet and Opuntia cladodes. J. Entomol. Sci. 43:95–106. Musser, R. O., S. M. Hum-Musser, H. Eichenseer, M. Peiffer, G. Ervin, J. B. Murphy, and G. W. Felton. 2002. Herbivory: caterpillar saliva beats plant defenses. Nature 416:599–600. Neunzig, H. H., and E. G. Munroe. 1997. Pyraloidea. Pyralidae (part), Phycitinae (part). Pp. 157 in R. B. Dominick, D. C. Ferguson, J. G. Franclemont, R. W. Hodges, eds. The moths of America north of Mexico, fascicle 15.4. The Wedge Entomological Research Foundation, Washington , D.C. Orre, G. U. S., S. D. Wratten, M. Jonsson, and R. J. Hale. 2010. Effects of an herbivore-induced plant volatile on arthropods from three trophic levels in brassicas. Biol. Control 53:62–67. Paré, P. W., H. T. Alborn, and J. H. Tumlinson. 1998. Concerted biosynthesis of an insect elicitor of plant volatiles. Proc. Natl. Acad. Sci. U.S.A. 95:13971–13975. Parker, J. D., D. E. Burkepile, and M. E. Hay. 2006. Response to comment on “Opposing effects of native and exotic herbivores on plant invasion”. Science 313:298b. Peng, J. Y., Z. H. Li, H. Xian, J. H. Huang, S. H. Jia, X. X. Miao, and Y. P. Huang. 2005. Preliminary studies on differential defense responses induced during plant communication. Cell. Res. 15:187–192. Pimentel, D. 1963. Introducing parasites and predators to control native pests. Can. Entomol. 95:785–792. Prime-A-Plant Group:  U. Conrath, G. J. M. Beckers, V. Flors, P. García-Agustín, G. Jakab, F. Mauch, M. A. Newman, C. M. Pierterse, B. Poinssot, M. J. Pozo, et al. 2006. Priming: getting ready for battle. Mol. Plant Microbe Interact. 19:1062–1071. Raupp, M. J., P. M. Shrewsbury, and D. A. Herms. 2010. Ecology of herbivorous arthropods in urban landscapes. Annu. Rev. Entomol. 55:19–38. Sauby, K. E. 2009. The ecology of Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) in Florida. Master's thesis, Mississippi State University , Mississippi . Simonson, S. E., T. J. Stohlgren, L. Tyler, W. P. Gregg, R. Muir, and L. J. Garrett. 2005. Preliminary assessment of the potential impacts and risks of the invasive cactus moth Cactoblastis cactorum Berg., in the U.S. and Mexico. Pp. 1–32 in Final Report of the Inter. Atomic Energy Agency. Simpson, M., G. M. Gurr, A. T. Simmons, S. D. Wratten, D. G. James, G. Leeson, and H. I. Nicol. 2011. Insect attraction to synthetic herbivore-induced plant volatile-treated field crops. Agr. Forest Entomol. 13:45–57. Solis, M. A., S. D. Hight, and D. R. Gordon. 2004. Tracking the cactus moth, Cactoblastis cactorum Berg., as it flies and eats its way westward in the U.S. News of the Lepidopterist's Society 46:3–7. Tammaru, T., T. Esperk, and I. Castellanos. 2002. No evidence for costs of being large in females of Orgyia spp. (Lepidoptera, Lymantriidae): larger is always better. Oecologia 133:430–438. Thaler, J. S. 1999. Jasmonate-inducible plant defenses cause increased parasitism of herbivores. Nature 399:686–688. van Hulten, M., M. Pelser, L. C. van Loon, C. M. J. Pieterse, and J. Ton. 2006. Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 103:5602–5607. Weinhold, A., and I. T. Baldwin. 2011. Trichome-derived O-acyl sugars are a first meal for caterpillars that tags them for predation. Proc. Natl. Acad. Sci. U.S.A. 108:7855–7859. Wu, J., and I. T. Baldwin. 2009. Herbivory induced signaling in plants: perception and action. Plant Cell. Environ. 32:1161–1174. Wu, J., and I. T. Baldwin. 2010. New insights into plant responses to the attack from insect herbivores. Annu. Rev. Genet. 44:1–24.