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Improved Understanding of Weed Biological Control Safety and Impact with Chemical Ecology: A Review

Published online by Cambridge University Press:  20 January 2017

Gregory S. Wheeler*
Affiliation:
U.S. Department of Agriculture/Agricultural Research Service Invasive Plant Research Lab, 3225 College Ave., Fort Lauderdale, FL 33314
Urs Schaffner
Affiliation:
CABI, Rue des Grillons 1, 2800 Delémont, Switzerland
*
Corresponding author's E-mail: [email protected]
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Abstract

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We review chemical ecology literature as it relates to biological control of weeds and discuss how this means of controlling invasive plants could be enhanced by the consideration of several well-established research approaches. The interface between chemical ecology and biological control of weeds presents a rich opportunity to exploit potentially coevolved relationships between agents and plants where chemical factors mediating interactions are important. Five topics seem relevant, which if implemented could improve the predictability of host range determination, agent establishment, and impact on the target weed. (1) The host secondary plant chemistry and a potential biological control agent's response to that chemistry can be exploited to improve predictability of potential agent host range. (2) Evolutionary changes may occur in secondary plant chemistry of invasive weeds that have been introduced to novel environments and exposed to a new set of biotic and abiotic stressors. Further, such a scenario facilitates rapid evolutionary changes in phenotypic traits, which in turn may help explain one mechanism of invasiveness and affect the outcome of biological control and other management options. (3) Herbivores can induce production of secondary plant compounds. (4) Variability of weed secondary chemistry which, either constitutive or inducible, can be an important factor that potentially influences the performance of some biological control agents and their impact on the target weed. (5) Finally, sequestration of secondary plant chemistry may protect herbivores against generalist predators, which might improve establishment of a biological control agent introduced to a new range and eventually impact on the target weed. Recognition of these patterns and processes can help identify the factors that impart success to a biological control program.

Type
Reviews
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
Copyright © Weed Science Society of America

References

Literature Cited

Adler, L. S. and Kittelson, P. M. 2004. Variation in Lupinus arboreus alkaloid profiles and relationships with multiple herbivores. Biochem. Syst. Ecol. 32 :371390.Google Scholar
Agrawal, A. A. 2005. Future directions in the study of induced plant responses to herbivory. Entomol. Exp. Appl. 115 :97105.Google Scholar
Alborn, H. T., Turlings, T. C. J., Jones, T. H., Stenhagen, G., Loughrin, J. H., and Tumlinson, J. H. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276 :945949.Google Scholar
Bartelt, R. J., Cossé, A. A., Zilkowski, B. W., Weisleder, D., and Momany, F. A. 2001. Male-specific sesquiterpenes from Phyllotreta and Aphthona flea beetles. J. Chem. Ecol. 27 :23972423.Google Scholar
Becerra, J. X. and Venable, D. L. 1999. Macroevolution of insect–plant associations: the relevance of host biogeography to host affiliation. Proc. Natl. Acad. Sci. U. S. A. 96 :1262612631.Google Scholar
Beck, J. J., Smith, L., and Merrill, G. B. 2008. In situ volatile collection, analysis, and comparison of three Centaurea species and their relationship to biocontrol with herbivorous insects. J. Agric. Food Chem. 56 :27592764.Google Scholar
Berenbaum, M. R. 1990. Evolution of specialization in insect–umbellifer associations. Annu. Rev. Entomol. 35 :319343.Google Scholar
Berenbaum, M. R., Zangerl, A. R., and Nitao, J. K. 1986. Constraints on chemical coevolution: wild parsnips and the parsnip webworm. Evolution 40 :12151228.Google Scholar
Bernays, E. A. and Chapman, R. F. 1994. Host–Plant Selection by Phytophagous Insects. New York : Chapman & Hall. 312 p.Google Scholar
Bernays, E. A., Hartmann, T., and Chapman, R. F. 2004. Gustatory responsiveness to pyrrolizidine alkaloids in the Senecio specialist, Tyria jacobaeae (Lepidoptera, Arctiidae). Physiol. Entomol. 29 :6772.Google Scholar
Binder, R. G., Turner, C. E., and Flath, R. A. 1990a. Comparison of yellow starthistle volatiles from different plant parts. J. Agric. Food Chem. 38 :764767.Google Scholar
Binder, R. G., Turner, C. E., and Flath, R. A. 1990b. Volatile components of purple starthistle. J. Agric. Food Chem. 38 :10531055.Google Scholar
Blackburn, T. M., Cassey, P., Duncan, R. P., Evans, K. L., and Gaston, K. J. 2004. Avian extinction and mammalian introductions on oceanic islands. Science 305 :19551958.Google Scholar
Blossey, B. and Nötzold, R. 1995. Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J. Ecol. 83 :887889.Google Scholar
Buttery, R. G., Maddox, D. M., Light, D. M., and Ling, L. C. 1986. Volatile components of yellow starthistle. J. Agric. Food Chem. 34 :786788.Google Scholar
Callaway, R. M. and Ridenour, W. M. 2004. Novel weapons: invasive success and the evolution of increased competitive ability. Front. Ecol. Environ 2 :436443.Google Scholar
Cao, W. H., Charlton, R. E., Nechols, J. R., and Horak, M. J. 2003. Sex pheromone of the noctuid moth, Tyta luctuosa (Lepidoptera: Noctuidae), a candidate biological control agent of field bindweed. Environ. Entomol. 32 :1722.Google Scholar
Cappuccino, N. and Arnason, J. T. 2006. Novel chemistry of invasive exotic plants. Biol. Lett. 2 :189193.Google Scholar
Carmona, D., Lajeunesse, M. J., and Johnson, M. T. J. 2011. Plant traits that predict resistance to herbivores. Funct. Ecol. 25 :358367.Google Scholar
Castells, E. and Berenbaum, M. R. 2006. Laboratory rearing of Agonopterix alstroemeriana, the defoliating poison hemlock (Conium maculatum L.) moth, and effects of piperidine alkaloids on preference and performance. Environ. Entomol. 35 :607615.Google Scholar
Castells, E. and Berenbaum, M. R. 2008. Host plant selection by a monophagous herbivore is not mediated by quantitative changes in unique plant chemistry: Agonopterix alstroemeriana and Conium maculatum . Arthropod Plant Interact. 2 :4351.Google Scholar
Center, T., Purcell, M., Pratt, P., Rayamajhi, M., Tipping, P., Wright, S., and Dray, F. 2011. Biological control of Melaleuca quinquenervia: an Everglades invader. Biocontrol 115.Google Scholar
Christensen, R. M., Pratt, P. D., Costello, S. L., Rayamajhi, M. B., and Center, T. D. 2011. Acquired natural enemies of the weed biological control agent Oxyops vitiosa (Coleoptera: Curculionidae). Fla. Entomol. 94 :18.Google Scholar
Cipollini, D., Purrington, C. B., and Bergelson, J. 2003. Costs of induced responses in plants. Basic Appl. Ecol. 4 :7989.Google Scholar
Cipollini, D., Mbagwu, J., Barto, K., Hillstrom, C., and Enright, S. 2005. Expression of constitutive and inducible chemical defenses in native and invasive populations of Alliaria petiolata . J. Chem. Ecol. 31 :12551267.Google Scholar
Cossé, A., Bartelt, R. J., Zilkowski, B. W., Bean, D. W., and Petroski, R. J. 2005. The aggregation pheromone of Diorhabda elongata, a biological control agent of saltcedar (Tamarix spp.): identification of two behaviorally active components. J. Chem. Ecol. 31 :657670.Google Scholar
Cossé, A. A., Robert, J. B., Bruce, W. Z., Daniel, W. B., and Earl, R. A. 2006. Behaviorally active green leaf volatiles for monitoring the leaf beetle, Diorhabda elongata, a biocontrol agent of saltcedar, Tamarix spp. J. Chem. Ecol. 32 :26952708.Google Scholar
Costello, S. L., Pratt, P. D., Rayachhetry, M. B., and Center, T. D. Morphology and life history characteristics of Podisus mucronatus (Heteroptera: Pentatomidae). Fla. Entomol. 2002. 85 :344350.Google Scholar
Courtney, S. P. and Kibota, T. T. 1990. Mother doesn't know best: selection of hosts by ovipositing insects. Pages 161188 in Bernays, E. A., ed. Insect–Plant Interactions. Boca Raton, FL : CRC.Google Scholar
Crider, K. K. 2011. Predator interference with the cinnabar moth (Tyria jacobaeae) for the biological control of tansy ragwort (Senecio jacobaea). Invasive Plant Sci. Manag. 4 :332340.Google Scholar
Cripps, M. G., Hinz, H. L., McKenney, J. L., Price, W. J., and Schwarzlander, M. 2009. No evidence for an ‘evolution of increased competitive ability’ for the invasive Lepidium draba . Basic Appl. Ecol. 10 :103112.Google Scholar
Davis, M. A. 2003. Biotic globalization: does competition from introduced species threaten biodiversity? Bioscience 53 :481489.Google Scholar
de Vos, M., Kriksunov, K. L., and Jander, G. 2008. Indole-3-acetonitrile production from indole glucosinolates deters oviposition by Pieris rapae . Plant Physiol. 146 :916926.Google Scholar
Dicke, M. and Baldwin, I. T. 2010. The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci. 15 :167175.Google Scholar
Dicke, M. and Van Loon, J. J. A. 2000. Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomol. Exp. Appl. 97 :237249.Google Scholar
Diezel, C., von Dahl, C. C., Gaquerel, E., and Baldwin, I. T. 2009. Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol. 150 :15761586.Google Scholar
Dobler, S., Haberer, W., Witte, L., and Hartmann, T. 2000. Selective sequestration of pyrrolizidine alkaloids from diverse host plants by Longitarsus flea beetles. J. Chem. Ecol. 26 :12811298.Google Scholar
Doorduin, L. J. and Vrieling, K. 2011. A review of the phytochemical support for the shifting defence hypothesis. Phytochem. Rev. 10 :99106.Google Scholar
Doss, R. P., Oliver, J. E., Proebsting, W. M., Potter, S. W., Kuy, S., Clement, S. L., Williamson, R. T., Carney, J. R., and DeVilbiss, E. D. 2000. Bruchins: insect-derived plant regulators that stimulate neoplasm formation. Proc. Natl. Acad. Sci. U. S. A. 97 :62186223.Google Scholar
Duffey, S. S. 1980. Sequestration of plant natural products by insects. Annu. Rev. Entomol. 25 :447477.Google Scholar
Duffey, S. S. and Stout, M. J. 1996. Antinutritive and toxic components of plant defense against insects. Arch. Insect Biochem. Physiol. 32 :337.Google Scholar
Ehrlich, P. R. and Raven, P. H. 1964. Butterflies and plants: a study in coevolution. Evolution 18 :586608.Google Scholar
Eigenbrode, S., Andreas, J., Cripps, M., Ding, H., Biggam, R., and Schwärzlander, M. 2008. Induced chemical defenses in invasive plants: a case study with Cynoglossum officinale L. Biol. Invasions 10 :13731379.Google Scholar
Engelberth, J., Alborn, H. T., Schmelz, E. A., and Tumlinson, J. H. 2004. Airborne signals prime plants against insect herbivore attack. Proc. Natl. Acad. Sci. U. S. A. 101 :17811785.Google Scholar
Franks, S. J., Pratt, P. D., Dray, F. A., and Simms, E. L. 2008a. No evolution of increased competitive ability or decreased allocation to defense in Melaleuca quinquenervia since release from natural enemies. Biol. Invasions 10 :455466.Google Scholar
Franks, S. J., Pratt, P. D., Dray, F. A., and Simms, E. L. 2008b. Selection on herbivory resistance and growth rate in an invasive plant. Am. Nat. 171 :678691.Google Scholar
Franks, S. J., Wheeler, G. S., and Goodnight, C. 2012. Genetic variation and evolution of secondary compounds in native and introduced populations of the invasive plant Melaleuca quinquenervia . Evolution 66 :13981412.Google Scholar
Frost, C. J., Appel, H. M., Carlson, J. E., de Moraes, C. M., Mescher, M. C., and Schultz, J. C. 2007. Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol. Let. 10 :490498.Google Scholar
Futuyma, D. J. 2000. Potential evolution of host range in herbivorous insects. Pages 4253 in Van Driesche, R. G., Heard, T. A., McClay, A., and Reardon, R., eds. Proceedings: Host Specificity Testing of Exotic Arthropod Biological Control Agents: The Biological Basis for Improvement in Safety. Morgantown, WV : USDA Forest Service.Google Scholar
Garcia-Rossi, D., Rank, N., and Strong, D. R. 2003. Potential for self-defeating biological control? Variation in herbivore vulnerability among invasive Spartina genotypes. Ecol. Appl. 13 :16401649.Google Scholar
Goeden, R. D. and Louda, S. M. 1976. Biotic interference with insects imported for weed control. Annu. Rev. Entomol. 21 :325342.Google Scholar
Grayer, R. J., Chase, M. W., and Simmonds, M. S. J. 1999. A comparison between chemical and molecular characters for the determination of phylogenetic relationships among plant families: an appreciation of Hegnauer's “Chemotaxonomie der Pflanzen.”. Biochem. Syst. Ecol. 27 :369393.Google Scholar
Harris, P. and Zwölfer, H. 1968. Screening of phytophagous insects for biological control of weeds. Can. Entomol. 100 :295303.Google Scholar
Hartmann, T. and Dierich, B. 1998. Chemical diversity and variation of pyrrolizidine alkaloids of the senecionine type: biological need or coincidence? Planta 206 :443451.Google Scholar
Heard, T. A. 2000. Concepts in insect host-plant selection behavior and their application to host specificity testing. Pages 110 in Van Driesche, R. G., Heard, T. A., McClay, A., and Reardon, R., eds. Proceedings: Host Specificity Testing of Exotic Arthropod Biological Control Agents: The Biological Basis for Improvement in Safety. Morgantown, WV : USDA Forest Service.Google Scholar
Hegnauer, R. 1962–1996. Chemotaxomie der Pflanzen. Vols. 1-XI. Basel : Birkäuser.Google Scholar
Hinz, H. L., Schwarzlander, M., and Gaskin, J. F. 2008. Does phylogeny explain the host-choice behaviour of potential biological control agents for Brassicaceae weeds? Pages 418425 in Julien, M. H., Sforza, R., Bon, M-C., Evans, H. C., Hatcher, P. E., Hinz, H. L., and Rector, B. G., eds. International Symposium on Biological Control of Weeds. Cambridge, MA : CABI North American Office.Google Scholar
Holden, A. N. G. and Mahlberg, P. G. 1992. Application of chemotaxonomy of leafy spurges (Euphorbia spp.) in biological control. Can. J. Bot. 70 :15291536.Google Scholar
Holt, R. D. and Hochberg, M. E. 1997. When is biological control evolutionarily stable (or is it)? Ecology 78 :16731683.Google Scholar
Huang, W., Siemann, E., Wheeler, G. S., Zhou, J., Carrillo, J., and Ding, J. 2010. Resource allocation to defense and growth are driven by different responses to generalist and specialist herbivory in an invasive plant. J. Ecol. 98 :11571167.Google Scholar
Inderjit, , Callaway, R. M., and Vivanco, J. M. 2006. Can plant biochemistry contribute to understanding of invasion ecology? Trends Plant Sci. 11 :574580.Google Scholar
Inderjit, , Wardle, D. A., Karban, R., and Callaway, R. M. 2011. The ecosystem and evolutionary contexts of allelopathy. Trends Ecol. Evol. 26 :655662.Google Scholar
Ireland, B. F., Hibbert, D. B., Goldsack, R. J., Doran, J. C., and Brophy, J. J. 2002. Chemical variation in the leaf essential oil of Melaleuca quinquenervia (Cav.) S.T. Blake. Biochem. Syst. Ecol. 30 :457470.Google Scholar
Jamieson, M. A. and Bowers, M. D. 2010. Iridoid glycoside variation in the invasive plant dalmatian toadflax, Linaria dalmatica (Plantaginaceae), and sequestration by the biological control agent, Calophasia lunula . J. Chem. Ecol. 36 :7079.Google Scholar
Joshi, J. and Vrieling, K. 2005. The enemy release and EICA hypothesis revisited: incorporating the fundamental difference between specialist and generalist herbivores. Ecol. Lett. 8 :704714.Google Scholar
Karban, R. and Agrawal, A. A. 2002. Herbivore offense. Annu. Rev. Ecol. Syst. 33 :641664.Google Scholar
Karban, R. and Baldwin, I. T. 1997. Induced Responses to Herbivory. Chicago : University of Chicago Press. 319 p.Google Scholar
Karban, R., English-Loeb, G., and Hougen-Eitzman, D. 1997. Mite vaccinations for sustainable management of spider mites in vineyards. Ecol. Appl. 7 :183193.Google Scholar
Kessler, A. and Baldwin, I. T. 2002. Plant responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Biol. 53 :299328.Google Scholar
Kirk, H., Choi, Y. H., Kim, H. K., Verpoorte, R., and van der Meijden, E. 2005. Comparing metabolomes: the chemical consequences of hybridization in plants. New Phytol. 167 :613622.Google Scholar
Kirk, H., Vrieling, K., Pelser, P., and Schaffner, U. 2012. Can plant resistance to specialist herbivores be explained by plant chemistry or resource use strategy? Oecologia 168 :10431055.Google Scholar
Koricheva, J. 2002. Meta-analysis of sources of variation in fitness costs of plant antiherbivore defenses. Ecology 83 :176190.Google Scholar
Koricheva, J., Nykanen, H., and Gianoli, E. 2004. Meta-analysis of tradeoffs among plant antiherbivore defenses: are plants jacks of all trades, masters of all? Am. Nat. 163 :E64E75.Google Scholar
Landau, I., Müller-Schärer, H., and Ward, P. I. 1994. Influence of cnicin, a sesquiterpene lactone of Centaurea maculosa (Asteraceae), on specialist and generalist insect herbivores. J. Chem. Ecol. 20 :929942.Google Scholar
Lindroth, R. L., Scriber, J. M., and Hsia, M. T. S. 1988. Chemical ecology of the tiger swallowtail: mediation of host use by phenolic glycosides. Ecology 69 :814822.Google Scholar
Macel, M., Klinkhamer, P. G. L., Vrieling, K., and van der Meijden, E. 2002. Diversity of pyrrolizidine alkaloids in Senecio species does not affect the specialist herbivore Tyria jacobaeae . Oecologia 133 :541550.Google Scholar
Macel, M. and Vrieling, K. 2003. Pyrrolizidine alkaloids as oviposition stimulants for the cinnabar moth, Tyria jacobaeae . J. Chem. Ecol. 29 :14351446.Google Scholar
Madeira, P. T., Pemberton, R. W., and Center, T. D. 2008. A molecular phylogeny of the genus Lygodium (Schizaeaceae) with special reference to the biological control and host range testing of Lygodium microphyllum . Biol. Control 45 :308318.Google Scholar
Maron, J. L., Vilà, M., and Arnason, J. 2004. Loss of enemy resistance among introduced populations of St. John's wort (Hypericum perforatum). Ecology 85 :32433253.Google Scholar
McNaughton, S. J. 1983. Compensatory plant growth as a response to herbivory. Oikos 40 :329336.Google Scholar
Montgomery, B. R. and Wheeler, G. S. 2000. Antipredatory activity of the weevil Oxyops vitiosa: a biological control agent of Melaleuca quinquenervia . J. Insect Behav. 13 :915926.Google Scholar
Mooney, H. A. and Drake, J. A. 1986. Ecology of Biological Invasions of North American and Hawaii. New York : Springer-Verlag. 457 p.Google Scholar
Morgan, E. C. and Overholt, W. A. 2005. Potential allelopathic effects of Brazilian pepper (Schinus terebinthifolius Raddi, Anacardiaceae) aqueous extract on germination and growth of selected Florida native plants. Bull. Torrey Bot. Club 132 :1115.Google Scholar
Morin, L., Reid, A. M., Sims-Chilton, N. M., Buckley, Y. M., Dhileepan, K., Hastwell, G. T., Nordblom, T. L., and Raghu, S. 2009. Review of approaches to evaluate the effectiveness of weed biological control agents. Biol. Control 51 :115.Google Scholar
Moyes, C. L., Collin, H. A., Britton, G., and Raybould, A. F. 2000. Glucosinolates and differential herbivory in wild populations of Brassica oleracea . J. Chem. Ecol. 26 :26252641.Google Scholar
Müller, C. and Martens, N. 2005. Testing predictions of the ’‘evolution of increased competitive ability’ hypothesis for an invasive crucifer. Evol. Ecol. 19 :533550.Google Scholar
Muller, R., de Vos, M., Sun, J., Sonderby, I., Halkier, B., Wittstock, U., and Jander, G. 2010. Differential effects of indole and aliphatic glucosinolates on Lepidopteran herbivores. J. Chem. Ecol. 36 :905913.Google Scholar
Müller-Schärer, H., Schaffner, U., and Steinger, T. 2004. Evolution in invasive plants: implications for biological control. Trends Ecol. Evol. 19 :417422.Google Scholar
Narberhaus, I., Theuring, C., Hartmann, T., and Dobler, S. 2003. Uptake and metabolism of pyrrolizidine alkaloids in Longitarsus flea beetles (Coleoptera: Chrysomelidae) adapted and non-adapted to alkaloid-containing host plants. J. Comp. Physiol. B 173 :483491.Google Scholar
Nimmo, K. R. and Tipping, P. W. 2009. An introduced insect biological control agent preys on an introduced weed biological control agent. Fla. Entomol. 92 :179180.Google Scholar
Oelrichs, P. B., MacLeod, J. K., Seawright, A. A., and Grace, P. B. 2001. Isolation and identification of the toxic peptides from Lophyrotoma zonalis (Pergidae) sawfly larvae. Toxicon 39 :19331936.Google Scholar
Opitz, S. and Muller, C. 2009. Plant chemistry and insect sequestration. Chemoecology 19 :117154.Google Scholar
Paige, K. N. and Whitham, T. G. 1987. Overcompensation in response to mammalian herbivory. Am. Nat. 129 :407416.Google Scholar
Pearson, D. E. and Callaway, R. M. 2003. Indirect effects of host-specific biological control agents. Trends Ecol. Evol. 18 :456461.Google Scholar
Pedigo, L. P., Hutchins, S. H., and Higley, L. G. 1986. Economic injury levels in theory and practice. Annu. Rev. Entomol. 31 :341368.Google Scholar
Pelser, P. B., de, V. H., Theuring, C., Beuerle, T., Vrieling, K., and Hartmann, T. 2005. Frequent gain and loss of pyrrolizidine alkaloids in the evolution of Senecio section Jacobaea (Asteraceae). Phytochemistry 66 :12851295.Google Scholar
Pemberton, R. W. 2000. Predictable risk to native plants in weed biological control. Oecologia 125 :489494.Google Scholar
Poelman, E. H., Galiart, R. J. F. H., Raaijmakers, C. E., van Loon, J. J. A., and van Dam, N. M. 2008. Performance of specialist and generalist herbivores feeding on cabbage cultivars is not explained by glucosinolate profiles. Entomol. Exp. Appl. 127 :218228.Google Scholar
Pratt, P. D., Rayamajhi, M. B., Center, T. D., Tipping, P. W., and Wheeler, G. S. 2009. The ecological host range of an intentionally introduced herbivore: a comparison of predicted versus actual host use. Biol. Control 49 :146153.Google Scholar
Prince, E. and Pohnert, G. 2010. Searching for signals in the noise: metabolomics in chemical ecology. Anal. Bioanal. Chem. 396 :193197.Google Scholar
Raghu, S. and Van Klinken, R. D. 2006. Refining the ecological basis for agent selection in weed biological control. Aust. J. Entomol. 45 :251252.Google Scholar
Randrianalijaona, J. A., Ramanoelina, P. A. R., Rasoarahona, J. R. E., and Gaydou, E. M. 2005. Seasonal and chemotype influences on the chemical composition of Lantana camara L.: essential oils from Madagascar. Anal. Chim. Acta 545 :4652.Google Scholar
Rapo, C., Muller-Scharer, H., Vrieling, K., and Schaffner, U. 2010. Is there rapid evolutionary response in introduced populations of tansy ragwort, Jacobaea vulgaris when exposed to biological control? Evol. Ecol. 24 :10811099.Google Scholar
Rasmann, S. and Agrawal, A. A. 2011. Evolution of specialization: a phylogenetic study of host range in the red milkweed beetle (Tetraopes tetraophthalmus). Am. Nat. 177 :728737.Google Scholar
Ratzka, A., Vogel, H., Kliebenstein, D. J., Mitchell-Olds, T., and Kroymann, J. 2002. Disarming the mustard oil bomb. Proc. Natl. Acad. Sci. U. S. A. 99 :1122311228.Google Scholar
Reimer, N. J. 1988. Predation on Liothrips urichi Karny (Thysanoptera: Phlaeothripidae): a case of biotic interference. Environ. Entomol. 17 :132134.Google Scholar
Renwick, J. A. A., Haribal, M., Gouinguene, S., and Stadler, E. 2006. Isothiocyanates stimulating oviposition by the diamondback moth, Plutella xylostella . J. Chem. Ecol. 32 :755766.Google Scholar
Ridenour, W. M., Vivanco, J. M., Feng, Y., Horiuchi, J. I., and Callaway, R. M. 2008. No evidence for trade-offs: Centaurea plants from America are better competitors and defenders. Ecol. Monogr. 78 :369386.Google Scholar
Sankaran, M. and McNaughton, S. J. 1999. Determinants of biodiversity regulate compositional stability of communities. Nature 401 :691693.Google Scholar
Schaffner, U. 2001. Host range testing of insects for biological weed control: how can it be better interpreted? Bioscience 51 :951959.Google Scholar
Schoonhoven, L. M., Jermy, T., and Van Loon, J. J. A. 1998. Insect–Plant Biology. London : Chapman & Hall. 409 p.Google Scholar
Shinoda, T., Nagao, T., Nakayama, M., Serizawa, H., Koshioka, M., Okabe, H., and Kawai, A. 2002. Identification of a triterpenoid saponin from a crucifer, Barbarea vulgaris, as a feeding deterrent to the diamondback moth, Plutella xylostella . J. Chem. Ecol. 28 :587599.Google Scholar
Shiojiri, K., Kishimoto, K., Ozawa, R., Kugimiya, S., Urashimo, S., Arimura, G., Horiuchi, J., Nishioka, T., Matsui, K., and Takabayashi, J. 2006. Changing green leaf volatile biosynthesis in plants: an approach for improving plant resistance against both herbivores and pathogens. Proc. Natl. Acad. Sci. U. S. A. 103 :1667216676.Google Scholar
Siemann, E. and Rogers, W. E. 2001. Genetic differences in growth of an invasive tree species. Ecol. Lett. 4 :514518.Google Scholar
Sirvent, T. and Gibson, D. 2002. Induction of hypericins and hyperforin in Hypericum perforatum L. in response to biotic and chemical elicitors. Physiol. Mol. Plant Pathol. 60 :311320.Google Scholar
Sirvent, T. M., Krasnoff, S. B., and Gibson, D. M. 2003. Induction of hypericins and hyperforins in Hypericum perforatum in response to damage by herbivores. J. Chem. Ecol. 29 :26672681.Google Scholar
Sirvent, T. M., Walker, L., Vance, N., and Gibson, D. M. 2002. Variation in hypericins from wild populations of Hypericum perforatum L. in the Pacific Northwest of the USA. Econ. Bot. 56 :4148.Google Scholar
Southwell, I. A. and Bourke, C. A. 2001. Seasonal variation in hypericin content of Hypericum perforatum L. (St. John's wort). Phytochemistry 56 :437441.Google Scholar
Stastny, M., Schaffner, U., and Elle, E. 2005. Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J. Ecol. 93 :2737.Google Scholar
Sumner, L. W., Mendes, P., and Dixon, R. A. 2003. Plant metabolomics: large-scale phytochemistry in the functional genomics era. Phytochemistry 62 :817836.Google Scholar
Sun, J., Sonderby, I., Halkier, B., Jander, G., and de Vos, M. 2009. Non-volatile intact indole glucosinolates are host recognition cues for ovipositing Plutella xylostella . J. Chem. Ecol. 35 :14271436.Google Scholar
Thompson, J. N. 2005. Coevolution: the geographic mosaic of coevolutionary arms races. Curr. Biol. 15 :R992R994.Google Scholar
Tilman, D., Knops, J., Wedin, D., Reich, P., Ritchie, M., and Siemann, E. 1997. The influence of functional diversity and composition on ecosystem processes. Science 277 :13001302.Google Scholar
Tipping, P. W., Martin, M. R., Nimmo, K. R., Pierce, R. M., Smart, M. D., White, E., Madeira, P. T., and Center, T. D. 2009. Invasion of a West Everglades wetland by Melaleuca quinquenervia countered by classical biological control. Biol. Control 48 :7378.Google Scholar
Trilles, B. L., Bombarda, I., Bouraima-Madjebi, S., Raharivelomanana, P., Bianchini, J. P., and Gaydou, E. M. 2006. Occurrence of various chemotypes in niaouli (Melaleuca quinquenervia (Cav.) S. T. Blake) essential oil from New Caledonia. Flavour Fragr. J. 21 :677682.Google Scholar
Turlings, T. C. and Ton, J. 2006. Exploiting scents of distress: the prospect of manipulating herbivore-induced plant odours to enhance the control of agricultural pests. Curr. Opin. Plant Biol. 9 :421427.Google Scholar
Unsicker, S. B., Kunert, G., and Gershenzon, J. 2009. Protective perfumes: the role of vegetative volatiles in plant defense against herbivores. Curr. Opin. Plant Biol. 12 :479485.Google Scholar
van Dam, N., Vuister, L., Bergshoeff, C., de Vos, H., and van der Meijden, E. D. 1995. The “raison d' etre” of pyrrolizidine alkaloids Cynoglossum officinale: deterrent effects against generalist herbivores. J. Chem. Ecol. 21 :507523.Google Scholar
van der Meijden, E. 1996. Plant defence, an evolutionary dilemma: contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomol. Exp. Appl. 80 :307310.Google Scholar
Vitousek, P. M. 1990. Biological invasions and ecosystem processes: toward an integration of population biology and ecosystem studies. Oikos 57 :713.Google Scholar
Vrieling, K. and de Boer, N. J. 1999. Host-plant choice and larval growth in the cinnabar moth: do pyrrolizidine alkaloids play a role? Entomol. Exp. Appl. 91 :251257.Google Scholar
Wahlberg, N. 2001. The phylogenetics and biochemistry of host-plant specialization in melitaeine butterflies (Lepidoptera: Nymphalidae). Evolution 55 :522537.Google Scholar
Walker, L., Sirvent, T., Gibson, D., and Vance, N. 2001. Regional differences in hypericin and pseudohypericin concentrations and five morphological traits among Hypericum perforatum plants in the northwestern United States. Can. J. Bot. 79 :12481255.Google Scholar
Wang, Y., Huang, W., Siemann, E., Zou, J., Wheeler, G. S., Carrillo, J., and Ding, J. 2011. Lower resistance and higher tolerance of invasive host plants: biocontrol agents reach high densities but exert weak control. Ecol. Appl. 21 :729738.Google Scholar
Wang, Y., Siemann, E., Wheeler, G. S., Gu, X., Zhu, L., and Ding, J. 2012. Genetic variation in anti-herbivore chemical defences in an invasive plant. J. Ecol. 100 :894904.Google Scholar
Wapshere, A. J. 1974. A strategy for evaluating the safety of organisms for biological weed control. Ann. Appl. Biol. 77 :201211.Google Scholar
Wheeler, G. S. 2005. Maintenance of a narrow host range by Oxyops vitiosa; a biological control agent of Melaleuca quinquenervia . Biochem. Syst. Ecol. 33 :365383.Google Scholar
Wheeler, G. S. 2006. Chemotype variation of the weed Melaleuca quinquenervia influences the biomass and fecundity of the biological control agent Oxyops vitiosa . Biol. Control 36 :121128.Google Scholar
Wheeler, G. S., Massey, L. M., and Southwell, I. A. 2002. Antipredator defense of biological control agent Oxyops vitiosa is mediated by plant volatiles sequestered from the host plant Melaleuca quinquenervia . J. Chem. Ecol. 28 :297315.Google Scholar
Wheeler, G. S., Massey, L. M., and Southwell, I. A. 2003. Dietary influences on terpenoids sequestered by the biological control agent Oxyops vitiosa: effect of plant volatiles from different Melaleuca quinquenervia chemotypes and laboratory host species. J. Chem. Ecol. 29 :188207.Google Scholar
Wheeler, G. S. and Ordung, K. M. 2005. Secondary metabolite variation affects the oviposition preference but has little effect on the performance of Boreioglycaspis melaleucae: a biological control agent of Melaleuca quinquenervia . Biol. Control 35 :115123.Google Scholar
Wheeler, G. S. and Ordung, K. M. 2006. Lack of an induced response following fire and herbivory of two chemotypes of Melaleuca quinquenervia and its effect on two biological control agents. Biol. Control 39 :154161.Google Scholar
Wheeler, G. S., Pratt, P. D., Giblin-Davis, R. M., and Ordung, K. M. 2007. Intraspecific variation in leaf oils of Melaleuca quinquenervia in its naturalized range in Florida, the Caribbean, and Hawaii. Biochem. Syst. Ecol. 35 :489500.Google Scholar
Willis, A. J., Thomas, M. B., and Lawton, J. H. 1999. Is the increased vigour of invasive weeds explained by a trade-off between growth and herbivore resistance? Oecologia 120 :632640.Google Scholar
Wink, M. 2003. Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64 :319.Google Scholar
Witte, L., Ernst, L., Adam, H., and Hartmann, T. 1992. Chemotypes of two pyrrolizidine alkaloid-containing Senecio species. Phytochemistry 31 :559565.Google Scholar
Zalucki, M. P., Brower, L. P., and Malcolm, S. B. 1990. Oviposition by Danaus plexippus in relation to cardenolide content of three Asclepias species in the southeasthern U.S.A. Ecol. Entomol. 15 :231240.Google Scholar