Every plant is a member of a complex insect community that consists of tens to hundreds of species that belong to different trophic levels. The dynamics of this community are critically influenced by the plant, which mediates interactions between community members that can occur on the plant simultaneously or at different times. Herbivory results in changes in the plant's morphological or chemical phenotype that affect interactions with subsequently arriving herbivores. Changes in the plant's phenotype are mediated by molecular processes such as phytohormonal signaling networks and transcriptomic rearrangements that are initiated by oral secretions of the herbivore. Processes at different levels of biological complexity occur at timescales ranging from minutes to years. In this review, we address plant-mediated interactions with multiple species of the associated insect community and their effects on community dynamics, and link these to the mechanistic effects that multiple attacks have on plant phenotypes.


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Literature Cited

  1. Agrawal AA. 1.  2000. Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89:493–500 [Google Scholar]
  2. Agrawal AA. 2.  2005. Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evol. Ecol. Res. 7:651–67 [Google Scholar]
  3. Agrawal AA, Karban R, Colfer RG. 3.  2000. How leaf domatia and induced plant resistance affect herbivores, natural enemies and plant performance. Oikos 89:70–80 [Google Scholar]
  4. Ali JG, Agrawal AA. 4.  2012. Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci. 17:293–302 [Google Scholar]
  5. Andow DA. 5.  1991. Vegetational diversity and arthropod population response. Annu. Rev. Entomol. 36:561–86 [Google Scholar]
  6. Baldwin IT. 6.  2012. Training a new generation of biologists: the genome-enabled field biologists. Proc. Am. Philos. Soc. 156:205–14 [Google Scholar]
  7. Barbour RC, O'Reilly-Wapstra JM, De Little DW, Jordan GJ, Steane DA. 7.  et al. 2009. A geographic mosaic of genetic variation within a foundation tree species and its community-level consequences. Ecology 90:1762–72 [Google Scholar]
  8. Benrey B, Denno RF. 8.  1997. The slow growth high mortality hypothesis: a test using the cabbage butterfly. Ecology 78:987–99 [Google Scholar]
  9. Bidart-Bouzat MG, Kliebenstein D. 9.  2011. An ecological genomic approach challenging the paradigm of differential plant responses to specialist versus generalist insect herbivores. Oecologia 167:677–89Shows that plant transcriptional responses are strongly shaped by insect taxa (i.e., aphid as opposed to lepidopteran species). [Google Scholar]
  10. Bonaventure G, Van Doorn A, Baldwin IT. 10.  2011. Herbivore-associated elicitors: FAC signaling and metabolism. Trends Plant Sci. 16:294–99 [Google Scholar]
  11. Braasch J, Wimp GM, Kaplan I. 11.  2012. Testing for phytochemical synergism: arthropod community responses to induced plant volatile blends across crops. J. Chem. Ecol. 38:1264–75 [Google Scholar]
  12. Broekgaarden C, Poelman EH, Voorrips RE, Dicke M, Vosman B. 12.  2010. Intraspecific variation in herbivore community composition and transcriptional profiles in field-grown Brassica oleracea cultivars. J. Exp. Bot. 61:807–19 [Google Scholar]
  13. Bukovinszky T, Gols R, Kamp A, de Oliveira-Domingues F, Hambäck PA. 13.  et al. 2010. Combined effects of patch size and plant nutritional quality on local densities of insect herbivores. Basic Appl. Ecol. 11:396–405 [Google Scholar]
  14. Bukovinszky T, Gols R, Smid HM, Bukovinskiné Kiss G, Dicke M, Harvey JA. 14.  2012. Consequences of constitutive and induced variation in the host's food plant quality for parasitoid larval development. J. Insect Physiol. 58:367–75 [Google Scholar]
  15. Bukovinszky T, Poelman EH, Gols R, Prekatsakis G, Vet LEM. 15.  et al. 2009. Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism. Oecologia 160:299–308 [Google Scholar]
  16. Bukovinszky T, van Veen FJF, Jongema Y, Dicke M. 16.  2008. Direct and indirect effects of resource quality on food web structure. Science 319:804–7Shows that plant genotype affects insect communities at the second, third, and fourth trophic levels through size- and density-mediated effects. [Google Scholar]
  17. Cerrudo I, Keller MM, Cargnel MD, Demkura PV, de Wit M. 17.  et al. 2012. Low red/far-red ratios reduce Arabidopsis resistance to Botrytis cinerea and jasmonate responses via a COI1-JAZ10-dependent, salicylic acid-independent mechanism. Plant Physiol. 158:2042–52 [Google Scholar]
  18. D'Alessandro M, Turlings TCJ. 18.  2006. Advances and challenges in the identification of volatiles that mediate interactions among plants and arthropods. Analyst 131:24–32 [Google Scholar]
  19. De Rijk M, Dicke M, Poelman EH. 19.  2013. Foraging behaviour by parasitoids in multiherbivore communities. Anim. Behav. 85:1517–28 [Google Scholar]
  20. De Vos M, Van Oosten VR, Van Poecke RMP, Van Pelt JA, Pozo MJ. 20.  et al. 2005. Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol. Plant-Microbe Interact. 18:923–37 [Google Scholar]
  21. De Vos M, Van Zaanen W, Koornneef A, Korzelius JP, Dicke M. 21.  et al. 2006. Herbivore-induced resistance against microbial pathogens in Arabidopsis. Plant Physiol. 142:352–63 [Google Scholar]
  22. Dempsey DA, Vlot AC, Wildermuth MC, Klessig DF. 22.  2011. Salicylic acid biosynthesis and metabolism. Arabidopsis Book 9:e0156 [Google Scholar]
  23. Denno RF, McClure MS, Ott JR. 23.  1995. Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Annu. Rev. Entomol. 40:297–331 [Google Scholar]
  24. Dicke M, Baldwin IT. 24.  2010. The evolutionary context for herbivore-induced plant volatiles: beyond the “cry for help.”. Trends Plant Sci. 15:167–75 [Google Scholar]
  25. Dicke M, van Loon JJA, Soler R. 25.  2009. Chemical complexity of volatiles from plants induced by multiple attack. Nat. Chem. Biol. 5:317–24 [Google Scholar]
  26. Diezel C, von Dahl CC, Gaquerel E, Baldwin IT. 26.  2009. Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol. 150:1576–86 [Google Scholar]
  27. Dombrecht B, Xue GP, Sprague SJ, Kirkegaard Ja, Ross JJ. 27.  et al. 2007. MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell 19:2225–45 [Google Scholar]
  28. Durrant WE, Dong X. 28.  2004. Systemic acquired resistance. Annu. Rev. Phytopathol. 42:185–209 [Google Scholar]
  29. Dussourd DE. 29.  1995. Entrapment of aphids and whiteflies in lettuce latex. Ann. Entomol. Soc. Am. 88:163–72 [Google Scholar]
  30. Ehlting J, Chowrira SG, Mattheus N, Aeschliman DS, Arimura G, Bohlmann J. 30.  2008. Comparative transcriptome analysis of Arabidopsis thaliana infested by diamond back moth (Plutella xylostella) larvae reveals signatures of stress response, secondary metabolism, and signalling. BMC Genomics 9:154 [Google Scholar]
  31. Erb M, Foresti N, Turlings TCJ. 31.  2010. A tritrophic signal that attracts parasitoids to host-damaged plants withstands disruption by non-host herbivores. BMC Plant Biol. 10:247 [Google Scholar]
  32. Erb M, Meldau S, Howe GA. 32.  2012. Role of phytohormones in insect-specific plant reactions. Trends Plant Sci. 17:250–59 [Google Scholar]
  33. Erb M, Robert CAM, Hibbard BE, Turlings TCJ. 33.  2011. Sequence of arrival determines plant-mediated interactions between herbivores. J. Ecol. 99:7–15 [Google Scholar]
  34. Felton GW, Tumlinson JH. 34.  2008. Plant-insect dialogs: complex interactions at the plant-insect interface. Curr. Opin. Plant Biol. 11:457–63 [Google Scholar]
  35. Fritz RS, McDonough SE, Rhoads AG. 35.  1997. Effects of plant hybridization on herbivore-parasitoid interactions. Oecologia 110:360–67 [Google Scholar]
  36. Giron D, Frago E, Glevarec G, Pieterse CMJ, Dicke M. 36.  2013. Cytokinins as key regulators in plant-microbe-insect interactions: connecting plant growth and defence. Funct. Ecol. 27:599–609 [Google Scholar]
  37. Glazebrook J. 37.  2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43:205–27 [Google Scholar]
  38. Gols R, Bukovinszky T, van Dam NM, Dicke M, Bullock JM, Harvey JA. 38.  2008. Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations. J. Chem. Ecol. 34:132–43 [Google Scholar]
  39. Gols R, Harvey JA. 39.  2009. Plant-mediated effects in the Brassicaceae on the performance and behaviour of parasitoids. Phytochem. Rev. 8:187–206 [Google Scholar]
  40. Gols R, Wagenaar R, Bukovinszky T, van Dam NM, Dicke M. 40.  et al. 2008. Genetic variation in defense chemistry in wild cabbages affects herbivores and their endoparasitoids. Ecology 89:1616–26 [Google Scholar]
  41. Hartley SE, Gange AC. 41.  2009. Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu. Rev. Entomol. 54:323–42 [Google Scholar]
  42. Harvey JA, van Dam NM, Raaijmakers CE, Bullock JM, Gols R. 42.  2011. Tri-trophic effects of inter- and intra-population variation in defence chemistry of wild cabbage (Brassica oleracea). Oecologia 166:421–31 [Google Scholar]
  43. Harvey JA, Wagenaar R, Bezemer TM. 43.  2009. Interactions to the fifth trophic level: secondary and tertiary parasitoid wasps show extraordinary efficiency in utilizing host resources. J. Anim. Ecol. 78:686–92 [Google Scholar]
  44. Haukioja E. 44.  1980. On the role of plant defences in the fluctuation of herbivore populations. Oikos 35:202–13 [Google Scholar]
  45. Heidel AJ, Baldwin IT. 45.  2004. Microarray analysis of salicylic acid- and jasmonic acid-signalling in responses of Nicotiana attenuata to attack by insects from multiple feeding guilds. Plant Cell Environ. 27:1362–73 [Google Scholar]
  46. Heil M. 46.  2008. Indirect defence via tritrophic interactions. New Phytol. 178:41–61 [Google Scholar]
  47. Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE. 47.  2001. Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proc. Natl. Acad. Sci. USA 98:1083–88 [Google Scholar]
  48. Hilker M, Meiners T. 48.  2010. How do plants “notice” attack by herbivorous arthropods?. Biol. Rev. 85:267–80 [Google Scholar]
  49. Hopkins RJ, van Dam NM, van Loon JJA. 49.  2009. Role of glucosinolates in insect-plant relationships and multitrophic interactions. Annu. Rev. Entomol. 54:57–83 [Google Scholar]
  50. Howe GA, Jander G. 50.  2008. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59:41–66 [Google Scholar]
  51. Hunter MD, Price PW. 51.  1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–32 [Google Scholar]
  52. Johnson MTJ. 52.  2008. Bottom-up effects of plant genotype on aphids, ants, and predators. Ecology 89:145–54 [Google Scholar]
  53. Johnson MTJ, Agrawal AA. 53.  2005. Plant genotype and environment interact to shape a diverse arthropod community on evening primrose (Oenothera biennis). Ecology 86:874–85 [Google Scholar]
  54. Johnson MTJ, Agrawal AA. 54.  2007. Covariation and composition of arthropod species across plant genotypes of evening primrose (Oenothera biennis). Oikos 116:941–56 [Google Scholar]
  55. Johnson MTJ, Lajeunesse MJ, Agrawal AA. 55.  2006. Additive and interactive effects of plant genotypic diversity on arthropod communities and plant fitness. Ecol. Lett. 9:24–34 [Google Scholar]
  56. Kahl J, Siemens DH, Aerts RJ, Gabler R, Kuhnemann F. 56.  et al. 2000. Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210:336–42 [Google Scholar]
  57. Kant MR, Sabelis MW, Haring MA, Schuurink RC. 57.  2008. Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences. Proc. R. Soc. B 275:443–52 [Google Scholar]
  58. Kaplan I, Denno RF. 58.  2007. Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol. Lett. 10:977–94Provides extensive quantitative analysis of plant-mediated effects among herbivorous insects. [Google Scholar]
  59. Karban R, Agrawal AA. 59.  2002. Herbivore offense. Annu. Rev. Ecol. Syst. 33:641–64 [Google Scholar]
  60. Karban R, Agrawal AA, Mangel M. 60.  1997. The benefits of induced defenses against herbivores. Ecology 78:1351–55 [Google Scholar]
  61. Karban R, Baldwin IT. 61.  1997. Induced Responses to Herbivory Chicago: Chicago Univ. Press [Google Scholar]
  62. Kareiva P, Sahakian R. 62.  1990. Tritrophic effects of a simple architectural mutation in pea plants. Nature 345:433–34 [Google Scholar]
  63. Kawazu K, Mochizuki A, Sato Y, Sugeno W, Murata M. 63.  et al. 2012. Different expression profiles of jasmonic acid and salicylic acid inducible genes in the tomato plant against herbivores with various feeding modes. Arthropod-Plant Interact. 6:221–30 [Google Scholar]
  64. Kazana E, Pope TW, Tibbles L, Bridges M, Pickett JA. 64.  et al. 2007. The cabbage aphid: a walking mustard oil bomb. Proc. R. Soc. B 274:2271–77 [Google Scholar]
  65. Keith AR, Bailey JK, Whitham TG. 65.  2010. A genetic basis to community repeatability and stability. Ecology 91:3398–406 [Google Scholar]
  66. Kessler A, Baldwin IT. 66.  2002. Plant responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Biol. 53:299–328 [Google Scholar]
  67. Kessler A, Baldwin IT. 67.  2004. Herbivore-induced plant vaccination. Part I. The orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata. Plant J. 38:639–49 [Google Scholar]
  68. Kessler A, Halitschke R, Baldwin IT. 68.  2004. Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305:665–68Demonstrates that lipoxygenase-silencing of tobacco plants results in major effects on interactions with herbivores in the field. [Google Scholar]
  69. Kessler A, Halitschke R, Poveda K. 69.  2011. Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions. Ecology 92:1769–80 [Google Scholar]
  70. Keurentjes JJB, Angenent GC, Dicke M, Dos Santos V, Molenaar J. 70.  et al. 2011. Redefining plant systems biology: from cell to ecosystem. Trends Plant Sci. 16:183–90 [Google Scholar]
  71. Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC. 71.  et al. 2008. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 147:1358–68 [Google Scholar]
  72. Kos M, Broekgaarden C, Kabouw P, Lenferink KO, Poelman EH. 72.  et al. 2011. Relative importance of plant-mediated bottom-up and top-down forces on herbivore abundance on Brassica oleracea. Funct. Ecol. 25:1113–24 [Google Scholar]
  73. Kuśnierczyk A, Winge P, Jørstad TS, Troczyńska J, Rossiter JT, Bones AM. 73.  2008. Towards global understanding of plant defence against aphids—timing and dynamics of early Arabidopsis defence responses to cabbage aphid (Brevicoryne brassicae) attack. Plant Cell Environ. 31:1097–115 [Google Scholar]
  74. Leimu R, Koricheva J. 74.  2006. A meta-analysis of genetic correlations between plant resistances to multiple enemies. Am. Nat. 168:E15–37 [Google Scholar]
  75. Leon-Reyes A, Spoel SH, De Lange ES, Abe H, Kobayashi M. 75.  et al. 2009. Ethylene modulates the role of NONEXPRESSOR OF PATHOGENESIS-RELATED GENES1 in cross talk between salicylate and jasmonate signaling. Plant Physiol. 149:1797–809Shows that ET modulates the NPR1 dependency of JA-SA antagonistic crosstalk. [Google Scholar]
  76. Lorenzo O, Chico JM, Sa JJ. 76.  2004. JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–50 [Google Scholar]
  77. Lucas-Barbosa D, van Loon JJA, Dicke M. 77.  2011. The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects. Phytochemistry 72:1647–54 [Google Scholar]
  78. Maffei ME, Arimura G, Mithöfer A. 78.  2012. Natural elicitors, effectors and modulators of plant responses. Nat. Prod. Rep. 29:1288–303 [Google Scholar]
  79. Maffei ME, Mithöfer A, Boland W. 79.  2007. Before gene expression: early events in plant-insect interaction. Trends Plant Sci. 12:310–16 [Google Scholar]
  80. McCormick AC, Unsicker SB, Gershenzon J. 80.  2012. The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci. 17:303–10 [Google Scholar]
  81. Memelink J. 81.  2009. Regulation of gene expression by jasmonate hormones. Phytochemistry 70:1560–70 [Google Scholar]
  82. Mendes R, Kruijt M, De Bruijn I, Dekkers E, Van der Voort M. 82.  et al. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–100 [Google Scholar]
  83. Miller-Pierce MR, Preisser EL. 83.  2012. Asymmetric priority effects influence the success of invasive forest insects. Ecol. Entomol. 37:350–58 [Google Scholar]
  84. Mithöfer A, Boland W. 84.  2012. Plant defense against herbivores: chemical aspects. Annu. Rev. Plant Biol. 63:431–50 [Google Scholar]
  85. Moran PJ, Cheng Y, Cassell JL, Thompson GA. 85.  2002. Gene expression profiling of Arabidopsis thaliana in compatible plant-aphid interactions. Arch. Insect Biochem. Physiol. 51:182–203 [Google Scholar]
  86. Müller C. 86.  2009. Interactions between glucosinolate-and myrosinase-containing plants and the sawfly Athalia rosae. Phytochem. Rev. 8:121–34 [Google Scholar]
  87. Newton EL, Bullock JM, Hodgson DJ. 87.  2009. Bottom-up effects of glucosinolate variation on aphid colony dynamics in wild cabbage populations. Ecol. Entomol. 34:614–23 [Google Scholar]
  88. Newton EL, Bullock JM, Hodgson DJ. 88.  2009. Glucosinolate polymorphism in wild cabbage (Brassica oleracea) influences the structure of herbivore communities. Oecologia 160:63–76 [Google Scholar]
  89. Ode PJ. 89.  2006. Plant chemistry and natural enemy fitness: effects on herbivore and natural enemy interactions. Annu. Rev. Entomol. 51:163–85 [Google Scholar]
  90. Ohgushi T. 90.  2005. Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu. Rev. Ecol. Evol. Syst. 36:81–105 [Google Scholar]
  91. Ohgushi T. 91.  2008. Herbivore-induced indirect interaction webs on terrestrial plants: the importance of non-trophic, indirect, and facilitative interactions. Entomol. Exp. Appl. 128:217–29 [Google Scholar]
  92. Pieterse CMJ, Dicke M. 92.  2007. Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci. 12:564–69 [Google Scholar]
  93. Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SC. 93.  2009. Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5:308–16 [Google Scholar]
  94. Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC. 94.  2012. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28:489–521 [Google Scholar]
  95. Pineda A, Zheng SJ, van Loon JJA, Pieterse CMJ, Dicke M. 95.  2010. Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci. 15:507–14 [Google Scholar]
  96. Poelman EH, Broekgaarden C, van Loon JJA, Dicke M. 96.  2008. Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol. Ecol. 17:3352–65Links insect behavior and gene expression to effects of early-season herbivory on insect community development. [Google Scholar]
  97. Poelman EH, Bruinsma M, Zhu F, Weldegergis BT, Boursault AE. 97.  et al. 2012. Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host. PLoS Biol. 10:e1001435 [Google Scholar]
  98. Poelman EH, van Dam NM, van Loon JJA, Vet LEM, Dicke M. 98.  2009. Chemical diversity in Brassica oleracea affects biodiversity of insect herbivores. Ecology 90:1863–77 [Google Scholar]
  99. Poelman EH, van Loon JJA, Dicke M. 99.  2008. Consequences of variation in plant defense for biodiversity at higher trophic levels. Trends Plant Sci. 13:534–41 [Google Scholar]
  100. Poelman EH, van Loon JJA, van Dam NM, Vet LEM, Dicke M. 100.  2010. Herbivore-induced plant responses in Brassica oleracea prevail over effects of constitutive resistance and result in enhanced herbivore attack. Ecol. Entomol. 35:240–47 [Google Scholar]
  101. Poelman EH, Zheng SJ, Zhang Z, Heemskerk NM, Cortesero AM, Dicke M. 101.  2011. Parasitoid-specific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores. Proc. Natl. Acad. Sci. USA 108:19647–52 [Google Scholar]
  102. Ponzio C, Gols R, Pieterse CMJ, Dicke M. 102.  2013. Ecological and phytohormonal aspects of plant volatile emission in response to single and dual infestations with herbivores and phytopathogens. Funct. Ecol. 27:587–98 [Google Scholar]
  103. Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE. 103.  1980. Interactions among three trophic levels: influence of plant on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11:41–65 [Google Scholar]
  104. Reymond P. 104.  2013. Perception, signaling and molecular basis of oviposition-mediated plant responses. Planta 238:247–58 [Google Scholar]
  105. Reymond P, Bodenhausen N, Van Poecke RMP, Krishnamurthy V, Dicke M, Farmer EE. 105.  2004. A conserved transcript pattern in response to a specialist and a generalist herbivore. Plant Cell 16:3132–47 [Google Scholar]
  106. Rodriguez-Saona CR, Musser RO, Vogel H, Hum-Musser SM, Thaler JS. 106.  2010. Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J. Chem. Ecol. 361043–57 [Google Scholar]
  107. Romero GQ, Benson WW. 107.  2005. Biotic interactions of mites, plants and leaf domatia. Curr. Opin. Plant Biol. 8:436–40 [Google Scholar]
  108. Sanders D, Sutter L, van Veen FJF. 108.  2013. The loss of indirect interactions leads to cascading extinctions of carnivores. Ecol. Lett. 16:664–69 [Google Scholar]
  109. Schoonhoven LM, van Loon JJA, Dicke M. 109.  2005. Insect-Plant Biology Oxford, UK: Oxford Univ. Press [Google Scholar]
  110. Schweitzer JA, Madritch MD, Bailey JK, LeRoy CJ, Fischer DG. 110.  et al. 2008. From genes to ecosystems: the genetic basis of condensed tannins and their role in nutrient regulation in a Populus model system. Ecosystems 11:1005–20 [Google Scholar]
  111. Scriber JM, Slansky F. 111.  1981. The nutritional ecology of immature insects. Annu. Rev. Entomol. 26:183–211 [Google Scholar]
  112. Shiojiri K, Takabayashi J, Yano S, Takafuji A. 112.  2001. Infochemically mediated tritrophic interaction webs on cabbage plants. Popul. Ecol. 43:23–29 [Google Scholar]
  113. Smith DS, Bailey JK, Shuster SM, Whitham TG. 113.  2011. A geographic mosaic of trophic interactions and selection: trees, aphids and birds. J. Evol. Biol. 24:422–29 [Google Scholar]
  114. Snoeren TAL, Mumm R, Poelman EH, Yang Y, Pichersky E, Dicke M. 114.  2010. The herbivore-induced plant volatile methyl salicylate negatively affects attraction of the parasitoid Diadegma semiclausum. J. Chem. Ecol. 36:479–89 [Google Scholar]
  115. Soler R, Erb M, Kaplan I. 115.  2013. Long distance root-shoot signalling in plant-insect community interactions. Trends Plant Sci. 18:149–56 [Google Scholar]
  116. Soler R, Badenes-Pérez FR, Broekgaarden C, Zheng S-J, David A. 116.  et al. 2012. Plant-mediated facilitation between a leaf-feeding and a phloem-feeding insect in a brassicaceous plant: from insect performance to gene transcription. Funct. Ecol. 26:156–66 [Google Scholar]
  117. Staswick PE, Tiryaki I. 117.  2004. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16:2117–27 [Google Scholar]
  118. Stireman JO, Nason JD, Heard SB, Seehawer JM. 118.  2006. Cascading host-associated genetic differentiation in parasitoids of phytophagous insects. Proc. R. Soc. Lond. B 273:523–30 [Google Scholar]
  119. Tack AJM, Dicke M. 119.  2013. Plant pathogens structure arthropod communities across multiple spatial and temporal scales. Funct. Ecol. 27:633–45 [Google Scholar]
  120. Thaler JS. 120.  1999. Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686–88 [Google Scholar]
  121. Thaler JS. 121.  2002. Effect of jasmonate-induced plant responses on the natural enemies of herbivores. J. Anim. Ecol. 71:141–50 [Google Scholar]
  122. Thaler JS, Fidantsef AL, Bostock RM. 122.  2002. Antagonism between jasmonate- and salicylate-mediated induced plant resistance: effects of concentration and timing of elicitation on defense-related proteins, herbivore, and pathogen performance in tomato. J. Chem. Ecol. 28:1131–59 [Google Scholar]
  123. Thaler JS, Humphrey PT, Whiteman NK. 123.  2012. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci. 17:260–70 [Google Scholar]
  124. Thaler JS, McArt SH, Kaplan I. 124.  2012. Compensatory mechanisms for ameliorating the fundamental trade-off between predator avoidance and foraging. Proc. Natl. Acad. Sci. USA 109:12075–80 [Google Scholar]
  125. Thaler JS, Stout MJ, Karban R, Duffey SS. 125.  2001. Jasmonate-mediated induced plant resistance affects a community of herbivores. Ecol. Entomol. 26:312–24 [Google Scholar]
  126. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A. 126.  et al. 2007. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–65 [Google Scholar]
  127. Tooker JF, De Moraes CM. 127.  2008. Gall insects and indirect plant defenses: a case of active manipulation?. Plant Signal. Behav. 3:503–4 [Google Scholar]
  128. Underwood N. 128.  2012. When herbivores come back: effects of repeated damage on induced resistance. Funct. Ecol. 26:1441–49 [Google Scholar]
  129. Utsumi S, Ando Y, Miki T. 129.  2010. Linkages among trait-mediated indirect effects: a new framework for the indirect interaction web. Popul. Ecol. 52:485–97Reviews trait-mediated indirect effects in plant-associated arthropod communities and explores the mechanisms of linkages among TMIUs. [Google Scholar]
  130. Utsumi S, Ohgushi T. 130.  2008. Host plant variation in plant-mediated indirect effects: moth boring-induced susceptibility of willows to a specialist leaf beetle. Ecol. Entomol. 33:250–60 [Google Scholar]
  131. van Veen FJF, Morris RJ, Godfray HCJ. 131.  2006. Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annu. Rev. Entomol. 51:187–208 [Google Scholar]
  132. van Veen FJF, van Holland PD, Godfray HCJ. 132.  2005. Stable coexistence in insect communities due to density- and trait-mediated indirect effects. Ecology 86:3182–89 [Google Scholar]
  133. Van Zandt PA, Agrawal AA. 133.  2004. Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616–29Shows species-specific effects of initial herbivory on communities associated with plants. [Google Scholar]
  134. Van Zandt PA, Agrawal AA. 134.  2004. Specificity of induced plant responses to specialist herbivores of the common milkweed Asclepias syriaca. Oikos 104:401–9 [Google Scholar]
  135. Viswanathan DV, Lifchits OA, Thaler JS. 135.  2007. Consequences of sequential attack for resistance to herbivores when plants have specific induced responses. Oikos 116:1389–99 [Google Scholar]
  136. Viswanathan DV, Narwani AJT, Thaler JS. 136.  2005. Specificity in induced plant responses shapes patterns of herbivore occurrence on Solanum dulcamara. Ecology 86:886–96 [Google Scholar]
  137. Voelckel C, Baldwin IT. 137.  2004. Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations. Plant J. 38:650–63Shows that the transcriptomic response to multiple herbivore attacks differs significantly from the response to single attacks. [Google Scholar]
  138. Vrieling K, Smit W, van der Meijden E. 138.  1991. Tritrophic interactions between aphids (Aphis jacobaeae Schrank), ant species, Tyria jacobaeae L., and Senecio jacobaea L. lead to maintenance of genetic variation in pyrrolizidine alkaloid concentration. Oecologia 86:177–82 [Google Scholar]
  139. Wang D, Amornsiripanitch N, Dong X. 139.  2006. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathol. 2:e123 [Google Scholar]
  140. Wang X, Hu L, Zhou G, Cheng J, Lou Y. 140.  2011. Salicylic acid and ethylene signaling pathways are involved in production of rice trypsin proteinase inhibitors induced by the leaf folder Cnaphalocrocis medinalis (Guenée). Chin. Sci. Bull. 56:2351–58 [Google Scholar]
  141. Webster B, Bruce T, Pickett J, Hardie J. 141.  2010. Volatiles functioning as host cues in a blend become nonhost cues when presented alone to the black bean aphid. Anim. Behav. 79:451–57 [Google Scholar]
  142. Whitham TG, Bailey JK, Schweitzer JA, Shuster SM, Bangert RK. 142.  et al. 2006. A framework for community and ecosystem genetics: from genes to ecosystems. Nat. Rev. Genet. 7:510–23 [Google Scholar]
  143. Whitham TG, Gehring CA, Lamit LJ, Wojtowicz T, Evans LM. 143.  et al. 2012. Community specificity: life and afterlife effects of genes. Trends Plant Sci. 17:271–81 [Google Scholar]
  144. Wildermuth MC, Dewdney J, Wu G, Ausubel FM. 144.  2001. Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414:562–65 [Google Scholar]
  145. Wu JQ, Baldwin IT. 145.  2010. New insights into plant responses to the attack from insect herbivores. Annu. Rev. Genet. 44:1–24 [Google Scholar]
  146. Xiao Y, Wang Q, Erb M, Turlings TCJ, Ge L. 146.  et al. 2012. Specific herbivore-induced volatiles defend plants and determine insect community composition in the field. Ecol. Lett. 15:1130–39 [Google Scholar]
  147. Zarate SI, Kempema LA, Walling LL. 147.  2007. Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol. 143:866–75 [Google Scholar]
  148. Zhang PJ, Broekgaarden C, Zheng SJ, Snoeren TAL, van Loon JJA. 148.  et al. 2013. Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana. New Phytol. 197:1291–99 [Google Scholar]
  149. Zhang PJ, Zheng SJ, van Loon JJA, Boland W, David A. 149.  et al. 2009. Whiteflies interfere with indirect plant defense against spider mites in Lima bean. Proc. Natl. Acad. Sci. USA 106:21202–7Uses transcriptional, chemical, and behavioral data to elucidate whitefly feeding interference with spider-mite-induced emission of predator-attracting volatile. [Google Scholar]

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