Skip to main content Accessibility help
×
Home
  • Get access
    Check if you have access via personal or institutional login
  • Cited by 32
  • Print publication year: 2007
  • Online publication date: August 2009

9 - Ecology meets plant physiology: herbivore-induced plant responses and their indirect effects on arthropod communities

Summary

Introduction

Herbivory by arthropods induces a wealth of changes in the primary and secondary chemistry of plants (Karban and Baldwin 1997, Constabel 1999, Agrawal et al. 1999, Kessler and Baldwin 2002). These chemical changes in turn do not only affect the inducer, but also other herbivore species attacking the induced plant (Denno et al. 1995, Denno and Kaplan Chapter 2 this volume). This effect of one herbivore species on other herbivores is called “indirect,” because it can only arise via the plant as an intermediate organism (Wootton 1994). Moreover, it is called trait-mediated, because the immediate effect of herbivory is an induced change in plant quality, not in plant quantity (Werner and Peacor 2003, Schmitz et al. 2004).

The herbivore-induced state of plants may influence the community of arthopods that live on them. When the induced plant allocates much of its energy in compensatory growth or defense specifically aimed at the inducer, other herbivore species may profit from the increased nutritional quality or weakened defense of the plant, thereby giving rise to interspecific aggregations of herbivores on individual plants (Denno et al. 1995). If, however, the induced plant mounts a sufficiently generalized defense, the plant becomes “vaccinated” against attack by other herbivores, leading to species-poor communities of herbivorous arthropods on the plant (Karban and Baldwin 1997). Much the same reasoning applies to herbivore genotypes within a single species.

References
Agrawal, A. A., and Colfer, R. G.. 2000. Consequences of thrips-infested plants for attraction of conspecifics and parasitoids. Ecological Entomology 25:493–496.
Agrawal, A. A., Tuzun, S., and Bent, E. (eds.) 1999. Induced Plant Defenses against Pathogens and Herbivores. St. Paul, MN: American Phytopathological Society Press.
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 276:945–949.
Alborn, H. T., Jones, T. H., Stenhagen, G. S., and Tumlinson, J. H.. 2000. Identification and synthesis of volicitin and related components from beet armyworm oral secretions. Journal of Chemical Ecology 26:203–220.
Ament, K., Kant, M. R., Sabelis, M. W., Haring, M. A., and Schuurink, R. C.. 2004. Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiology 135:1–13.
Aratchige, N. S., Lesna, I., and Sabelis, M. W.. 2004. Below-ground plant parts emit herbivore-induced volatiles: olfactory responses of a predatory mite to tulip bulbs infested by rust mite. Experimental and Applied Acarology 33:21–30.
Baldwin, I. T. 1998. Jasmonate-induced responses are costly but benefit plants under attack in natural populations. Proceedings of the National Academy of Sciences of the USA 95:8113–8118.
Baldwin, I. T. 2001. An ecologically motivated analysis of plant–herbivore interactions in native tobacco. Plant Physiology 127:1449–1458.
Belliure, B., Janssen, A., Maris, P. C., Peters, D., and Sabelis, M. W.. 2005. Herbivore arthropods benefit from vectoring plant viruses. Ecology Letters 8:70–79.
Bernasconi, M. L., Turlings, T. C. J., Ambrosetti, L., Bassetti, P., and Dorn, S.. 1998. Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis. Entomologia Experimentalis et Applicata 87:133–142.
Birkett, M. A., Campbell, C. A. M., Chamberlain, K., et al. 2000. New roles for cis-jasmone as an insect semiochemical and in plant defense. Proceedings of the National Academy of Sciences of the USA 97:9329–9334.
Birkett, M. A., Chamberlain, K., Guerrieri, E., et al. 2003. Volatiles from whitefly-infested plants elicit a host-locating response in the parasitoid, Encarsia formosa. Journal of Chemical Ecology 29:1589–1600.
Bouwmeester, H. J., Verstappen, F. W. A., Posthumus, M. A., and Dicke, M.. 1999. Spider mite-induced (3S)-(E)-nerolidol synthase activity in cucumber and lima bean: the first dedicated step in acyclic C11-homoterpene biosynthesis. Plant Physiology 121:173–180.
Campbell, C. A. M., Pettersson, J., Pickett, J. A., Wadhams, L. J., and Woodcock, C. M.. 1993. Spring migration of damson-hop aphid, Phorodon humuli (Homoptera, Aphididae), and summer host plant-derived semiochemicals released on feeding. Journal of Chemical Ecology 81:1569–1576.
Constabel, C. P. 1999. A survey of herbivore-inducible defensive proteins and phytochemicals, pp. 137–166 in Agrawal, A. A., Tuzun, S., and Bent, E. (eds.) Induced Plant Defenses against Pathogens and Herbivores. St. Paul, MN: American Phytopathological Society Press.
Cui, J., Bahrami, A. K., Pringle, E. G., et al. 2005. Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proceedings of the National Academy of Sciences of the USA 102:1791–1796.
Boer, J. G. 2004. Bugs in odour space: how predatory mites respond to variation in herbivore-induced plant volatiles. Ph.D. dissertation, Wageningen University, the Netherlands.
Boer, J. G., and Dicke, M.. 2004. Experience with methyl salicylate affects behavioural responses of a predatory mite to blends of herbivore-induced plant volatiles. Entomologia Experimentalis et Applicata 110:181–189.
Boer, J. G., Posthumus, M. A., and Dicke, M.. 2004. Identification of volatiles that are used in discrimination between plants infested with prey or nonprey herbivores by a predatory mite. Journal of Chemical Ecology 30:2215–2230.
Boer, J. G., Snoeren, T. A. L., and Dicke, M.. 2005. Predatory mites learn to discriminate between plant volatiles induced by prey and nonprey herbivores. Animal Behaviour 69:869–879.
Moraes, C. M., Lewis, W. J., Paré, P. W., Alborn, H. T., and Tumlinson, J. H.. 1998. Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573.
Denno, R. F., McClure, M. S., and Ott, J. R.. 1995. Interspecific interactions in phytophagous insects: competition revisited and resurrected. Annual Review of Entomology 40:297–331.
Dicke, M. 1994. Local and systemic production of volatile herbivore-induced terpenoids: their role in plant–carnivore mutualism. Journal of Plant Physiology 143:465–472.
Dicke, M. 1999. Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods?Entomologia Experimentalis et Applicata 91:131–142.
Dicke, M., and Sabelis, M. W.. 1988. How plants obtain predatory mites as bodyguards. Netherlands Journal of Zoology 38:148–165.
Dicke, M., Beek, T. A., Posthumus, M. A., et al. 1990a. Isolation and identification of volatile kairomone that affects acarine predator–prey interactions: involvement of host plant in its production. Journal of Chemical Ecology 16:381–396.
Dicke, M., Sabelis, M. W., Takabayashi, J., Bruin, J., and Posthumus, M. A.. 1990b. Plant strategies of manipulating predator–prey interactions through allelochemicals: prospects for application in pest control. Journal of Chemical Ecology 16:3091–3118.
Dicke, M., Takabayashi, J., Posthumus, M. A., Schütte, C., and Krips, O. E.. 1998. Plant–phytoseiid interactions mediated by herbivore-induced plant volatiles: variation in production of cues and in responses of predatory mites. Experimental and Applied Acarology 22:311–333.
Dicke, M., Boer, J. G., Hofte, M., and Rocha-Granados, M. C.. 2003. Mixed blends of herbivore-induced plant volatiles and foraging success of carnivorous arthropods. Oikos 101:38–48.
Doares, S. H., Syrovets, T., Weiler, E. W., and Ryan, C. A.. 1995. Oligogalacturonides and chitosan activate plant defensive genes through the octadecanoid pathway. Proceedings of the NationalAcademy of Sciences of the USA 92:4095–4098.
Drukker, B., Scutareanu, P., and Sabelis, M. W.. 1995. Do anthocorid predators respond to synomones from Psylla-infested pear trees under field conditions?Entomologia Experimentalis et Applicata 77:193–203.
Drukker, B., Bruin, J., Jacobs, G., Kroon, A., and Sabelis, M. W.. 2000a. How predatory mites learn to cope with variability in volatile plant signals in the environment of their herbivorous prey. Experimental and Applied Acarology 24:881–895.
Drukker, B., Bruin, J., and Sabelis, M. W.. 2000b. Anthocorid predators learn to associate herbivore-induced plant volatiles with presence or absence of prey. Physiological Entomology 25:260–265.
Du, Y. J., Poppy, G. M., Powell, W., et al. 1998. Identification of semiochemicals released during aphid feeding that attract parasitoid Aphidius ervi. Journal of Chemical Ecology 24:1355–1368.
Farmer, E. E., and Ryan, C. A.. 1992. Octadecanoid precursors of jasmonic acid activate the synthesis of wound-inducible proteinase inhibitors. Plant Cell 4:129–134.
Felton, G., and Korth, K.. 2000. Trade-offs between pathogen and herbivore resistance. Current Opinion in Plant Biology 3:309–314.
Felton, G. W., Korth, K. I., Bi, J. L., et al. 1999. Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory. Current Biology 9:317–320.
Fritzsche-Hoballah, M. E., and Turlings, T. C. J.. 2001. Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids. Evolutionary Ecology Research 3:533–565.
Geervliet, J. B. F., Vreugdenhil, A. I., Dicke, M., and Vet, L. E. M.. 1998a. Learning to discriminate between infochemicals from different plant-host complexes by the parasitoids Cotesia glomerata and C. rubecula. Entomologia Experimentalis et Applicata 86:241–252.
Geervliet, J. B. F., Ariens, S., Dicke, M., and Vet, L. E. M.. 1998b. Long-distance assessment of patch profitability through volatile infochemicals by the parasitoids Cotesia glomerata and C. rubecula (Hymenoptera: Braconidae). Biological Control 11:113–121.
Gols, R., Roosjen, M., Dijkman, H., and Dicke, M.. 2003. Induction of direct and indirect plant responses by jasmonic acid, low spider mite densities, or a combination of jasmonic acid treatment and spider mite infestation. Journal of Chemical Ecology 29:2651–2666.
Gu, H., and Dorn, S.. 2000. Genetic variation in behavioral response to herbivore-infested plants in the parasitic wasp Cotesia glomerata (L.) (Hymenoptera: Braconidae). Journal of Insect Behavior 13:141–156.
Guerrieri, E., Poppy, G. M., Powell, W., Tremblay, E., and Pennacchio, F.. 1999. Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi. Journal of Chemical Ecology 25:1247–1261.
Hassell, M. P. 1978. The Dynamics of Arthropod Predator–Prey Systems. Princeton, NJ: Princeton University Press.
Havill, N. P., and Raffa, K. F.. 2000. Compound effects of induced plant responses on insect herbivores and parasitoids: implications for tritrophic interactions. Ecological Entomology 25:171–179.
Heil, M., Koch, T., Hilpert, A., et al. 2001. Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proceedings of the National Academy of Sciences of the USA 98:1083–1088.
Heil, M., Greiner, S., Meimberg, H., et al. 2004. Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430:205–208.
Holopainen, J. K. 2004. Multiple functions of inducible plant volatiles. Trends in Plant Science 9:529–533.
Hopke, J., Donath, J., Blechert, S., and Boland, W.. 1994. Herbivore-induced volatiles: the emission of acyclic homoterpenes from leaves of Phaseolus lunatus and Zea mays can be triggered by a beta-glucosidase and jasmonic acid. FEBS Letters 352:146–150.
Hountondji, F. C. C., Sabelis, M. W., Hanna, R., and Janssen, A.. 2005. Do herbivore-induced plant volatiles trigger sporulation in an entomopathogenic fungus? A study on cassava green mite and Neozygites tanajoae. Journal of Chemical Ecology 31:1003–1021.
Inbar, M., Doostdar, H., Sonoda, R. M., Leibee, G. L., and Mayer, R. T.. 1998. Elicitors of plant defensive systems reduce insect densities and disease incidence. Journal of Chemical Ecology 24:135–149.
Janssen, A., Pallini, A., Venzon, M., and Sabelis, M. W.. 1998. Behaviour and food web interactions among plant inhabiting mites and thrips. Experimental and Applied Acarology 22:497–521.
Janssen, A., Sabelis, M. W., and Bruin, J.. 2002. Evolution of herbivore-induced plant volatiles. Oikos 97:134–138.
Jia, F., Margolies, D. C., Boyer, J. E., and Charlton, R. E.. 2002. Genetic variation in foraging traits among inbred lines of a predatory mite. Heredity 89:371–379.
Kahl, J., Siemens, D. H., Aerts, R. J., et al. 2000. Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210:336–342.
Kant, M. R., Ament, K., Sabelis, M. W., Haring, M., and Schuurink, R.. 2004. Differential timing of spider mite-induced direct and indirect-defenses in tomato plants. Plant Physiology 135:483–495.
Karban, R., and Baldwin, I. T.. 1997. Induced Responses to Herbivory. Chicago, IL: University of Chicago Press.
Kessler, A., and Baldwin, I. T.. 2001. Defensive function of herbivore-induced volatiles in nature. Science 291:2141–2144.
Kessler, A., and Baldwin, I. T.. 2002. Plant responses to insect herbivory: the emerging molecular analysis. Annual Review of Plant Biology 53:299–328.
Kessler, A., Halitschke, R., and Baldwin, I. T.. 2004. Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305:665–668.
Kloek, A. P., Verbsky, M. L., Sharma, S. B., et al. 2001. Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant Journal 26:509–522.
Krips, O. E., Willems, P. E. L., Gols, R., Posthumus, M. A., and Dicke, M.. 1999. The response of Phytoseiulus persimilis to spider mite-induced volatiles from Gerbera: influence of starvation and experience. Journal of Chemical Ecology 25:2623–2641.
Kunkel, B. N., and Brooks, D. M.. 2002. Cross-talk between signaling pathways in pathogen defense. Current Opinion in Plant Biology 5:325–331.
Lesna, I., Conijn, C. G. M., and Sabelis, M. W.. 2004. From biological control to biological insight: rust-mite induced change in bulb morphology, a new mode of indirect plant defence?Phytophaga 14:1–7.
Li, C. Y., Williams, M. M., Loh, Y. T., Lee, G. I., and Howe, G. A.. 2002. Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway. Plant Physiology 130:494–503.
Li, L., Zhao, Y. F., McCaig, B. C., et al. 2004. The tomato homolog of CORONATINE-INSENSITIVE1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16:126–143.
Maeda, T., Takabayashi, J., Yano, S., and Takafuji, A.. 1999. Response of the predatory mite, Amblyseius womersleyi (Acari: Phytoseiidae), toward herbivore-induced plant volatiles: variation in response between two local populations. Applied Entomology and Zoology 34:449–454.
Maeda, T., Takabayashi, J., Yano, S., and Takafuji, A.. 2001. Variation in the olfactory response of predatory mite, Amblyseius womersleyi (Acari: Phytoseiidae), of 13 populations to herbivore-induced plant volatiles. Experimental and Applied Acarology 25:55–64.
Mantyla, E., Klemola, T., and Haukioja, E.. 2004. Attraction of willow warblers to sawfly-damaged mountain birches: novel function of inducible plant defences?Ecology Letters 7:915–918.
Margolies, D. C., Sabelis, M. W., and Boyer, J. E.. 1997. Response of a phytoseiid predator to herbivore-induced plant volatiles: selection on attraction and effect of prey exploitation. Journal of Insect Behavior 10:695–709.
Mattiacci, L., Dicke, M., and Posthumus, M. A.. 1995. β-Glucosidase: an elicitor of herbivore-induced plant odor that attracts hostsearching parasitic wasps. Proceedings of the National Academy of Sciences of the USA 92:2036–2040.
McConn, M., Creellman, R. A., Bell, E., Mullet, J. E., and Browse, J.. 1997. Jasmonate is essential for insect defense in Arabidopsis. Proceedings of the National Academy of Sciences of the USA 93:5473–5477.
Mercke, P., Kappers, I. F., Verstappen, F. W. A., et al. 2004. Combined transcript and metabolite analysis reveals genes involved in spider mite induced volatile formation in cucumber plants. Plant Physiology 135:2012–2024.
Mori, N., Alborn, H. T., Teal, P. E. A., and Tumlinson, J. H.. 2001. Enzymatic decomposition of elicitors of plant volatiles in Heliothis virescens and Helicoverpa zea. Journal of Insect Physiology 47:749–757.
Musser, R. O., Cipollini, D. F., Hum-Musser, S. M., et al. 2005a. Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in solanaceous plants. Archives of Insect Biochemistry and Physiology 58:128–137.
Musser, R. O., Kwon, H. S., Williams, S. A., et al. 2005b. Evidence that caterpillar labial saliva suppresses infectivity of potential bacterial pathogens. Archives of Insect Biochemistry and Physiology 58:138–144.
O'Dowd, D. J., Brew, C. F. R., Christophel, D. C., and Norton, R. A.. 1991. Mite–plant associations from the Eocene of Southern Australia. Science 252:99–101.
Ozawa, R., Arimura, G., Takabayashi, J., Shimoda, T., and Nishioka, T.. 2000. Involvement of jasmonate- and salicylate-related signaling pathway for the production of specific herbivore-induced volatiles in plants. Plant Cell Physiology 41:391–398.
Ozawa, R., Shiojiri, K., Sabelis, M. W., et al. 2004. Corn plants treated with jasmonic acid attract more specialist parasitoids, thereby increasing parasitization of the common armyworm. Journal of Chemical Ecology 30:1797–1808.
Pallini, A., Janssen, A., and Sabelis, M. W.. 1997. Odour-mediated responses of phytophagous mites to conspecific and heterospecific competitors. Oecologia 110:179–185.
Pallini, A., Janssen, A., and Sabelis, M. W.. 1998. Predators induce interspecific herbivore competition for food in refuge space. Ecology Letters 1:171–176.
Pallini, A., A. Janssen, and M. W. Sabelis. 1999. Do western flower thrips avoid plants infested with spider mites? Interactions between potential competitors, pp. 375–380 in Bruin, J., Geest, L. P. S., and Sabelis, M. W. (eds.) Ecology and Evolution of the Acari. Dordrecht, The Netherlands: Kluwer Academic Publishers.
Papaj, D. R., and Lewis, A. C.. 1993. Insect Learning: Ecology and Evolutionary Perspectives. New York: Chapman and Hall.
Papaj, D. R., Snellen, H., Swaans, K., and Vet, L. E. M.. 1994. Unrewarding experiences and their effect on foraging in the parasitic wasp Leptopilina heterotoma (Hymenoptera, Eucoilidae). Journal of Insect Behavior 7:465–481.
Paré, P. W., Lewis, W. J., and Tumlinson, J. H.. 1999. Induced plant volatiles: biochemistry and effects on parasitoids, pp. 167–180 in Agrawal, A. A., Tuzun, S., and Bent, E. (eds.) Induced Defenses against Pathogens and Herbivores. St. Paul, MN: American Phytopathological Society Press.
Paul, N. D., Hatcher, P. E., and Taylor, J. E.. 2000. Coping with multiple enemies: an integration of molecular and ecological perspectives. Trends in Plant Science 5:221–225.
Pieterse, C. M. J., and Loon, L. C.. 1999. Salicylic acid-independent plant defence pathways. Trends in Plant Science 4:52–58.
Pieterse, C. M. J., and Loon, L. C.. 2004. NPR1: the spider in the web of induced resistance signaling pathways. Current Opinion in Plant Biology 7:456–464.
Preston, C. A., Lewandowski, C., Enyedi, A. J., and Baldwin, I. T.. 1999. Tobacco mosaic virus inoculation inhibits wound-induced jasmonic acid-mediated responses within but not between plants. Planta 209:87–95.
Price, P. W., Bouton, C. E., Gross, P., et al. 1980. Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual Review of Ecology and Systematics 11:41–65.
Reymond, P., Bodenhausen, N., Poecke, R. M. P., et al. 2004. A conserved transcriptional pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–3147.
Rojo, E., Solano, R., and Sanchez-Serrano, J. J.. 2003. Interactions between signaling compounds involved in plant defense. Journal of Plant Growth Regulation 22:82–98.
Roitberg, B., M. L. Reid, and C. Li. 1993. Choosing hosts and mates: the value of learning, pp. 174–194 in Papaj, D. R. and Lewis, A. C. (eds.) Insect Learning: Ecology and Evolutionary Perspectives. New York: Chapman and Hall.
Sabelis, M. W., and Bakker, F. M.. 1992. How predatory mites cope with the web of their tetranychid prey: a functional view on dorsal chaetotaxy in the Phytoseiidae. Experimental and Applied Acarology 16:203–225.
Sabelis, M. W., and Jong, M. C. M.. 1988. Should all plants recruit bodyguards? Conditions for a polymorphic ESS of synomone production in plants. Oikos 53:247–252.
Sabelis, M. W., and M. Dicke. 1985. Long-range dispersal and searching behaviour, pp. 141–160 in Helle, W. and Sabelis, M. W. (eds.) Spider Mites: Their Biology, Natural Enemies and Control. Amsterdam, The Netherlands: Elsevier.
Sabelis, M. W., and Baan, H. E.. 1983. Location of distant spider mite colonies by phytoseiid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi. Entomologia Experimentalis et Applicata 33:303–314.
Sabelis, M. W., B. P. Afman, and P. J. Slim. 1984. Location of distant spider-mite colonies by Phytoseiulus persimilis: localization and extraction of a kairomone, pp. 431–440 in Griffiths, D. A. and Bowman, C. E. (eds.) Acarology VI, vol. 1. New York: Halsted Press.
Sabelis, M. W., Janssen, A., Pallini, A., et al. 1999a. Behavioural responses of predatory and herbivorous arthropods to induced plant volatiles: from evolutionary ecology to agricultural applications, pp. 269–296 in Agrawal, A. A., Tuzun, S., and Bent, E. (eds.) Induced Plant Defenses against Pathogens and Herbivores. St. Paul, MN: American Phytopathological Society Press.
Sabelis, M. W., Baalen, M., Bakker, F. M., et al. 1999b. The evolution of direct and indirect plant defence against herbivorous arthropods, pp. 109–166 in Olff, H., Brown, V. K., and Drent, R. H. (eds.) Herbivores: Between Plants and Predators. Oxford, UK: Blackwell Science.
Sabelis, M. W., Janssen, A., Bruin, J., et al. 1999c. Interactions between arthropod predators and plants: a conspiracy against herbivorous arthropods? pp. 207–230 in Bruin, J., Geest, L. P. S., and Sabelis, M. W. (eds.) Ecology and Evolution of the Acari. Dordrecht, The Netherlands: Kluwer Academic Publishers.
Sabelis, M. W., M. van Baalen, B. Pels, M. Egas, and A. Janssen. 2002. Evolution of exploitation and defence in plant–herbivore–predator interactions, pp. 297–321 in Dieckmann, U., Metz, J. A. J., Sabelis, M. W., and Sigmund, K. (eds.) The Adaptive Dynamics of Infectious Diseases: In Pursuit of Virulence Management. Cambridge, UK: Cambridge University Press.
Sabelis, M. W., P. C. J. van Rijn, and A. Janssen. 2005. Fitness consequences of food-for-protection strategies in plants, pp. 109–134 in Wäckers, F. L., Rijn, P. C. J., and Bruin, J. (eds.) Plant-Provided Food and Herbivore–Carnivore Interactions. Cambridge, UK: Cambridge University Press.
Schmitz, O. J., Krivan, V., and Ovadia, O.. 2004. Trophic cascades: the primacy of trait-mediated indirect interactions. Ecology Letters 7:153–163.
Schneider, M., Schweitzer, P., Meuwly, P., and Metraux, J. P.. 1996. Systemic acquired resistance in plants. International Review of Cytology 168:303–339.
Scutareanu, P., Drukker, B., Bruin, J., Posthumus, M. A., and Sabelis, M. W.. 1997. Isolation and identification of volatile synomones involved in the interaction between Psylla-infested pear trees and two anthocorid predators. Journal of Chemical Ecology 23:2241–2260.
Scutareanu, P., Lingeman, R., Drukker, B., and Sabelis, M. W.. 1999. Cross-correlation analysis of fluctuations in local populations of pear psyllids and anthocorid bugs. Ecological Entomology 24:1–9.
Shimoda, T., and Dicke, M.. 2000. Attraction of a predator to chemical information related to nonprey: when can it be adaptive?Behavioral Ecology 11:606–613.
Shiojiri, K., Takabayashi, J., Yano, S., and Takafuji, A.. 2002. Oviposition preferences of herbivores are affected by tritrophic interaction webs. Ecology Letters 5:186–192.
Spoel, S. H., Koornneef, A., Claessens, S. M. C., et al. 2003. NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770.
Storeck, A., Poppy, G. M., Emden, H. F., and Powell, W.. 2000. The role of plant chemical cues in determining host preference in the generalist aphid parasitoid Aphidius colemani. Entomologia Experimentalis et Applicata 97:41–46.
Takabayashi, J., and Dicke, M.. 1992. Response of predatory mites with different rearing histories to volatiles of uninfested plants. Entomologia Experimentalis et Applicata 64:187–193.
Takabayashi, J., and Dicke, M., 1996. Plant–carnivore mutualism through herbivore-induced carnivore attractants. Trends in Plant Science 1:109–113.
Takabayashi, J., Dicke, M., and Posthumus, M. A.. 1991. Variation in composition of predator-attracting allelochemicals emitted by herbivore-infested plants: relative influence of plant and herbivore. Chemoecology 2:1–6.
Takabayashi, J., Sabelis, M. W., Janssen, A., Shiojiri, K., and Wijk, M.. 2006. Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical networks. Ecological Research 21:3–8.
Thaler, J. S. 1999a. Jasmonic acid mediated interactions between plants, herbivores, parasitoids, and pathogens: a review of field experiments in tomato, pp. 319–334 in Agrawal, A. A., Tuzun, S., and Bent, E. (eds.) Induced Plant Defenses against Pathogens and Herbivores. St. Paul, MN: American Phytopathological Society Press.
Thaler, J. S. 1999b. Jasmonate-inducible plant defenses cause increased parasitism of herbivores. Nature 399:686–688.
Thaler, J. S., 2002. Effect of jasmonate-induced plant responses on the natural enemies of herbivores. Journal of Animal Ecology 71:141–150.
Thaler, J. S., Fidantsef, A. L., Duffey, S. S., and Bostock, R. M.. 1999. Trade-offs in plant defense against pathogens and herbivores: a field demonstration of chemical elicitors of induced resistance. Journal of Chemical Ecology 25:1597–1609.
Thaler, J. S., Stout, M. J., Karban, R., and Duffey, S. S.. 2001. Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecological Entomology 26:312–324.
Thaler, J. S., Farag, M. A., Paré, P. W., and Dicke, M.. 2002a. Jasmonate-deficient plants have reduced direct and indirect defenses against herbivores. Ecology Letters 5:764–774.
Thaler, J. S., Karban, R., Ullman, D. E., Boege, K., and Bostock, R. M.. 2002b. Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131:227–235.
Turlings, T. C. J., and Tumlinson, J. H.. 1992. Systemic release of chemical signals by herbivore-injured corn. Proceedings of the National Academy of Sciences of the USA 89:8399–8402.
Turlings, T. C. J., Tumlinson, J. H., and Lewis, W. J.. 1990. Exploitation of herbivore-induced plant odors by host seeking parasitic wasps. Science 250:1251–1253.
Turlings, T. C. J., F. Wäckers, L. E. M. Vet, W. J. Lewis, and J. H. Tumlinson. 1993a. Learning of host-finding cues by hymenopterous parasitoids, pp. 51–78 in Papaj, D. R. and Lewis, A. C. (eds.) Insect Learning: Ecology and Evolutionary Perspectives. New York: Chapman and Hall.
Turlings, T. C. J., McCall, P. J., Alborn, H. T., and Tumlinson, J. H.. 1993b. An elicitor in caterpillar oral secretions that induces corn seedlings to emit chemical signals attractive to parasitic wasps. Journal of Chemical Ecology 19:411–425.
Turlings, T. C. J., Loughrin, J. H., McCall, P. J., et al. 1995. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proceedings of the National Academy of Sciences of the USA 92:4169–4174.
Baalen, M., and Jansen, V. A. A.. 2003. Common language or Tower of Babel? On the evolutionary dynamics of signals and their meanings. Proceedings of the Royal Society of London Series B 270:69–76.
Dam, N. M., Hadwich, K., and Baldwin, I. T.. 2000. Induced responses in Nicotiana attenuata affect behavior and growth of the specialist herbivore Manduca sexta. Oecologia 122:371–379.
Meijden, E., and Klinkhamer, P. G. L.. 2000. Conflicting interests of plants and the natural enemies of herbivores. Oikos 89:202–208.
Loon, J. J. A., Boer, J. G., and Dicke, M.. 2000. Parasitoid–plant mutualism: parasitoid attack of herbivore increases plant reproduction. Entomologia Experimentalis et Applicata 97:219–227.
Poecke, R. M. P., and Dicke, M.. 2002. Induced parasitoid attraction by Arabidopsis thaliana: involvement of the octadecanoid and the salicylic acid pathway. Journal of Experimental Botany 53:1793–1799.
Poecke, R. M. P., and Dicke, M.. 2003. Signal transduction downstream of salicylic and jasmonic acid in herbivory-induced parasitoid attraction by Arabidopsis is independent of JAR1 and NPR1. Plant Cell and Environment 26:1541–1548.
Rijn, P. C. J., Houten, Y. M., and Sabelis, M. W.. 2002. How plants benefit from providing food to predators when it is also edible to herbivores. Ecology 83:2664–2679.
Tol, R. W. H. M., Sommen, A. T. C., Boff, M. I. C., et al. 2001. Plants protect their roots by alerting the enemies of grubs. Ecology Letters 4:292–294.
Zandt, P. A., and Agrawal, A. A.. 2004. Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616–2629.
Vet, L. E. M., and Dicke, M., , M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Ecology and Systematics 37:141–172.
Vet, L. E. M., Lewis, W. J., and Cardé, R. T.. 1995. Parasitoid foraging and learning, pp. 65–101 in Cardé, R. T. and Bell, W. J. (eds.) Chemical Ecology of Insects, vol. 2. New York: Chapman and Hall.
Vos, M., Berrocal, S. M., Karamaouna, F., Hemerik, L., and Vet, L. E. M.. 2001. Plant-mediated indirect effects and the persistence of parasitoid–herbivore communities. Ecology Letters 4:38–45.
Wang, Q., and Dorn, S.. 2003. Selection on olfactory response to semiochemicals from a host-plant complex in a parasitic wasp. Heredity 91:430–435.
Wang, Q., Gu, H., and Dorn, S.. 2004. Genetic relationship between olfactory response and fitness in the Cotesia glomerata (L.). Heredity 92:579–584.
Werner, E. E., and Peacor, S. D.. 2003. A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100.
Wootton, J. T. 1994. The nature and consequences of indirect effects in ecological communities. Annual Review of Ecology and Systematics 25:443–466.
Zhao, Y. F., Thilmony, R., Bender, C. L., et al. 2003. Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant Journal 36:485–499.