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Impacts of Induction of Plant Volatiles by Individual and Multiple Stresses Across Trophic Levels

  • Martín ParejaEmail author
  • Delia M. Pinto-Zevallos
Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM)

Abstract

Plants are constantly challenged by many different stresses, ranging from abiotic factors, such as ultraviolet light and ozone, to herbivores and pathogens. To defend themselves against these challenges, plants activate defences that are specific to each stressor. One such defence is the emission of induced volatile organic compounds (VOCs) that can directly reduce the intensity of the stress or, in the case of herbivores, attract predators and parasitoids, in what is known as indirect defence. In nature, however, plants are rarely subject to stress by a single agent. In this chapter, we review what is known about the ecological effects of induced plant VOCs against individual and multiple stresses. First, we describe the biochemical responses against individual stressors that result in the emission of VOCs and how they can be modified by multiple stresses. We then discuss how plant VOCs can have an impact on herbivores, herbivore natural enemies and plant mutualists. We finish by discussing how future research should begin to investigate the importance of induced responses to multiple stresses in structuring plant-based communities.

Keywords

Natural Enemy Multiple Stress Lima Bean Induce Plant Defence Aboveground Herbivore 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We are grateful to James Blande and Robert Glinwood for the invitation to write this chapter and comments on previous versions. The ideas presented in this chapter greatly benefited from conversations with Gabriela Gomes, James Blande, João Oliveira, Luiz Henrique Rezende, Mônica Kersch-Becker, Rodolfo Faria Silva and Thiago Marinho Alvarenga. During writing, MP was supported by a FAEPEX-PAPDIC grant from UNICAMP and CNPq project 474449/2012-2. DMP-Z was funded by the Fundação de Apoio a Pesquisa e Inovação Tecnológica de Sergipe—FAPITEC.

References

  1. Abrams PA (1995) Implications of dynamically variable traits for identifying, classifying, and measuring direct and indirect effects in ecological communities. Am Nat 146:112–134CrossRefGoogle Scholar
  2. Agbogba BC, Powell W (2007) Effect of the presence of a nonhost herbivore on the response of the aphid parasitoid Diaeretiella rapae to host-infested cabbage plants. J Chem Ecol 33:2229–2235PubMedCrossRefGoogle Scholar
  3. Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302PubMedCrossRefGoogle Scholar
  4. Ali JG, Agrawal AA, Fox C (2014) Asymmetry of plant-mediated interactions between specialist aphids and caterpillars on two milkweeds. Funct Ecol 28:1404–1412CrossRefGoogle Scholar
  5. Ament K, Kant MR, Sabelis MW, Haring MA, Schuurink RC (2004) Jasmonic acid is a key regulator of spider mite-induced volatile terpenoid and methyl salicylate emission in tomato. Plant Physiol 135:2025–2037PubMedPubMedCentralCrossRefGoogle Scholar
  6. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedCrossRefGoogle Scholar
  7. Arimura G, Matsui K, Takabayashi J (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant Cell Physiol 50:911–923PubMedCrossRefGoogle Scholar
  8. Arimura GI, Ozawa R, Maffei ME (2011) Recent advances in plant early signaling in response to herbivory. Int J Mol Sci 12:3723–3739PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bari R, Jones JDG (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488PubMedCrossRefGoogle Scholar
  10. Bede JC, Musser RO, Felton GW, Korth KL (2006) Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzymes in terpenoid biosynthesis. Plant Mol Biol 60:519–531PubMedCrossRefGoogle Scholar
  11. Berenbaum MR, Zangerl AR (2006) Parsnip webworms and host plants at home and abroad: trophic complexity in a geographic mosaic. Ecology 87:3070–3081PubMedCrossRefGoogle Scholar
  12. Beyaert I, Hilker M (2014) Plant odour plumes as mediators of plant-insect interactions. Biol Rev 89:68–81PubMedCrossRefGoogle Scholar
  13. Biere A, Elzinga JA, Honders SC, Harvey JA (2002) A plant pathogen reduces the enemy-free space of an insect herbivore on a shared plant. Proc R Soc Lond B 269:2197–2204CrossRefGoogle Scholar
  14. Blande JD, Tiiva P, Oksanen E, Holopainen JK (2007) Emission of herbivore-induced volatile terpenoids from two hybrid aspen (Populus tremula × tremuloides) clones under ambient and elevated ozone concentrations in the field. Glob Chang Biol 13:2538–2550CrossRefGoogle Scholar
  15. Blande JD, Turunen K, Holopainen JK (2009) Pine weevil feeding on Norway spruce bark has a stronger impact on needle VOC emissions than enhanced ultraviolet-B radiation. Environ Pollut 157:174–180PubMedCrossRefGoogle Scholar
  16. Bleeker PM, Diergaarde PJ, Ament K, Guerra J, Weidner M, Schutz S, de Both MT, Haring MA, Schuurink RC (2009) The role of specific tomato volatiles in tomato-whitefly interaction. Plant Physiol 151:925–935PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bos JIB, Prince D, Pitino M, Maffei ME, Win J, Hogenhout SA (2010) A functional genomics approach identifies candidate effectors from the aphid species Myzus persicae (green peach aphid). PLoS Genet 6:e1001216PubMedPubMedCentralCrossRefGoogle Scholar
  18. Bostock RM (2005) Signal crosstalk and induced resistance: straddling the line between cost and benefit. Annu Rev Phytopathol 43:545–580PubMedCrossRefGoogle Scholar
  19. Braasch J, Wimp GM, Kaplan I (2012) Testing for phytochemical synergism: arthropod community responses to induced plant volatile blends across crops. J Chem Ecol 38:1264–1275PubMedCrossRefGoogle Scholar
  20. Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects—finding the right mix. Phytochemistry 72:1605–1611PubMedCrossRefGoogle Scholar
  21. Bruce TJA, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274PubMedCrossRefGoogle Scholar
  22. Bruce TJA, Matthes MC, Napier JA, Pickett JA (2007) Stressful “memories” of plants: evidence and possible mechanisms. Plant Sci 173:603–608CrossRefGoogle Scholar
  23. Bruessow F, Gouhier-Darimont C, Buchala A, Metraux J-P, Reymond P (2010) Insect eggs suppress plant defence against chewing herbivores. Plant J 62:876–885PubMedCrossRefGoogle Scholar
  24. Bruinsma M, Lucas-Barbosa D, ten Broeke CJM, van Dam NM, van Beek TA, Dicke M, van Loon JJA (2014) Folivory affects composition of nectar, floral odor and modifies pollinator behavior. J Chem Ecol 40:39–49PubMedCrossRefGoogle Scholar
  25. Bukovinszky T, Poelman EH, Kamp A, Hemerik L, Prekatsakis G, Dicke M (2012) Plants under multiple herbivory: consequences for parasitoid search behaviour and foraging efficiency. Anim Behav 83:501–509CrossRefGoogle Scholar
  26. Cardoza YJ, Alborn HT, Tumlinson JH (2002) In vivo volatile emissions from peanut plants induced by simultaneous fungal infection and insect damage. J Chem Ecol 28:161–174PubMedCrossRefGoogle Scholar
  27. Cardoza YJ, Teal PEA, Tumlinson JH (2003a) Effect of peanut plant fungal infection on oviposition preference by Spodoptera exigua and on host-searching behavior by Cotesia marginiventris. Environ Entomol 32:970–976CrossRefGoogle Scholar
  28. Cardoza YJ, Lait CG, Schmelz EA, Huang J, Tumlinson JH (2003b) Fungus-induced biochemical changes in peanut plants and their effect on development of beet armyworm, Spodoptera exigua Hubner (Lepidoptera: Noctuidae) larvae. Environ Entomol 32:220–228CrossRefGoogle Scholar
  29. Chen YH, Gols R, Benrey B (2015) Crop domestication and its impact on naturally selected trophic interactions. Annu Rev Entomol 60:35–58PubMedCrossRefGoogle Scholar
  30. Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF, Hoover K, Luthe DS, Felton GW (2013) Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc Natl Acad Sci USA 110:15728–15733PubMedPubMedCentralCrossRefGoogle Scholar
  31. Colazza S, McElfresh JS, Millar JG (2004a) Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis. J Chem Ecol 30:945–964PubMedCrossRefGoogle Scholar
  32. Colazza S, Fucarino A, Peri E, Salerno G, Conti E, Bin F (2004b) Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. J Exp Biol 207:47–53PubMedCrossRefGoogle Scholar
  33. Cook SM, Khan ZR, Pickett JA (2007) The use of push-pull strategies in integrated pest management. Annu Rev Entomol 52:375–400PubMedCrossRefGoogle Scholar
  34. Cozzolino S, Fineschi S, Litto M, Scopece G, Trunschke J, Schiestl FP (2015) Herbivory increases fruit set in Silene latifolia: a consequence of induced pollinator-attracting floral volatiles? J Chem Ecol 41:622–630PubMedCrossRefGoogle Scholar
  35. Cui HY, Su JW, Wei JN, Hu YJ, Ge F (2014) Elevated O-3 enhances the attraction of whitefly-infested tomato plants to Encarsia formosa. Sci Rep 4:5350PubMedPubMedCentralGoogle Scholar
  36. Danner H, Brown P, Cator EA, Harren FJ, van Dam NM, Cristescu SM (2015) Aboveground and belowground herbivores synergistically induce volatile organic sulfur compound emissions from shoots but not from roots. J Chem Ecol 41:631–640PubMedPubMedCentralCrossRefGoogle Scholar
  37. de Boer JG, Dicke M (2004) The role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. J Chem Ecol 30:255–271PubMedCrossRefGoogle Scholar
  38. de Boer JG, Hordijk CA, Posthumus MA, Dicke M (2008) Prey and non-prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction. J Chem Ecol 34:281–290PubMedPubMedCentralCrossRefGoogle Scholar
  39. De Moraes CM, Mescher MC, Tumlinson JH (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–580PubMedCrossRefGoogle Scholar
  40. de Rijk M, Dicke M, Poelman EH (2013) Foraging behaviour by parasitoids in multiherbivore communities. Anim Behav 85:1517–1528CrossRefGoogle Scholar
  41. Delphia CM, Mescher MC, Felton G, Moraes CMD (2006) The role of insect-derived cues in eliciting indirect plant defenses in tobacco, Nicotiana tabacum. Plant Signal Behav 1:243–250PubMedPubMedCentralCrossRefGoogle Scholar
  42. Delphia CM, Mescher MC, De Moraes CM (2007) Induction of plant volatiles by herbivores with different feeding habits and the effects of induced defenses on host-plant selection by thrips. J Chem Ecol 33:997–1012PubMedCrossRefGoogle Scholar
  43. Denno RF, Kaplan I (2007) Plant-mediated interactions in herbivorous insects: mechanisms, symmetry, and challenging the paradigms of competition past. In: Ohgushi T, Craig TP, Price PW (eds) Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, Cambridge, pp 19–50CrossRefGoogle Scholar
  44. Denno RF, McClure MS, Ott JR (1995) Interspecific interactions in phytophagous insects—competition reexamined and resurrected. Annu Rev Entomol 40:297–331CrossRefGoogle Scholar
  45. Dicke M (2006) Chemical ecology from genes to communities—integrating ‘omics’ with community ecology. In: Dicke M, Takken W (eds) Chemical ecology: from gene to ecosystem. Springer, Dordrecht, pp 175–189CrossRefGoogle Scholar
  46. Dicke M (2009) Behavioural and community ecology of plants that cry for help. Plant Cell Environ 32:654–665PubMedCrossRefGoogle Scholar
  47. Dicke M, Gols R, Poelman EH (2012) Dynamics of plant secondary metabolites and consequences for food chains and community dynamics. In: Iason G, Dicke M, Hartley SE (eds) The ecology of plant secondary metabolites: form genes to global processes. Cambridge University Press, Cambridge, pp 308–328CrossRefGoogle Scholar
  48. Diezel C, von Dahl CC, Gaquerel E, Baldwin IT (2009) Different lepidopteran elicitors account for cross-talk in herbivory-induced phytohormone signaling. Plant Physiol 150:1576–1586PubMedPubMedCentralCrossRefGoogle Scholar
  49. Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. Crit Rev Plant Sci 25:417–440CrossRefGoogle Scholar
  50. Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32PubMedCrossRefGoogle Scholar
  51. Effmert U, Dinse C, Piechulla B (2008) Influence of green leaf herbivory by Manduca sexta on floral volatile emission by Nicotiana suaveolens. Plant Physiol 146:1996–2007PubMedPubMedCentralCrossRefGoogle Scholar
  52. Eichenseer H, Mathews MC, Powell JS, Felton GW (2010) Survey of a salivary effector in caterpillars: glucose oxidase variation and correlation with host range. J Chem Ecol 36:885–897PubMedCrossRefGoogle Scholar
  53. Erb M, Foresti N, Turlings TCJ (2010) A tritrophic signal that attracts parasitoids to host-damaged plants withstands disruption by non-host herbivores. BMC Plant Biol 10:247PubMedPubMedCentralCrossRefGoogle Scholar
  54. Fatouros NE, Dicke M, Mumm R, Meiners T, Hilker M (2008a) Foraging behavior of egg parasitoids exploiting chemical information. Behav Ecol 19:677–689CrossRefGoogle Scholar
  55. Fatouros NE, Broekgaarden C, Bukovinszkine’Kiss G, van Loon JJA, Mumm R, Huigens ME, Dicke M, Hilker M (2008b) Male-derived butterfly anti-aphrodisiac mediates induced indirect plant defense. Proc Natl Acad Sci USA 105:10033–10038PubMedPubMedCentralCrossRefGoogle Scholar
  56. Fontana A, Reichelt M, Hempel S, Gershenzon J, Unsicker SB (2009) The effects of Arbuscular Mycorrhizal Fungi on direct and indirect defense metabolites of Plantago lanceolata L. J Chem Ecol 35:833–843PubMedPubMedCentralCrossRefGoogle Scholar
  57. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442PubMedCrossRefGoogle Scholar
  58. Glinwood RT, Pettersson J (2000) Change in response of Rhopalosiphum padi spring migrants to the repellent winter host component methyl salicylate. Entomol Exp Appl 94:325–330CrossRefGoogle Scholar
  59. Gomez JM, Gonzalez-Megias A (2002) Asymmetrical interactions between ungulates and phytophagous insects: being different matters. Ecology 83:203–211CrossRefGoogle Scholar
  60. Gomez JM, Gonzalez-Megias A (2007) Long-term effects of ungulates on phytophagous insects. Ecol Entomol 32:229–234Google Scholar
  61. Gouinguené SP, Turlings TCJ (2002) The effects of abiotic factors on induced volatile emissions in corn plants. Plant Physiol 129:1296–1307PubMedPubMedCentralCrossRefGoogle Scholar
  62. Hare JD (2011) Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annu Rev Entomol 56:161–180PubMedCrossRefGoogle Scholar
  63. Hartley SE, Gange AC (2009) Impacts of plant symbiotic fungi on insect herbivores: mutualism in a multitrophic context. Annu Rev Entomol 54:323–342PubMedCrossRefGoogle Scholar
  64. Harvey JA, van Dam NM, Gols R (2003) Interactions over four trophic levels: foodplant quality affects development of a hyperparasitoid as mediated through a herbivore and its primary parasitoid. J Anim Ecol 72:520–531CrossRefGoogle Scholar
  65. Heiden AC, Hoffmann T, Kahl J, Kley D, Klockow D, Langebartels C, Mehlhorn H, Sandermann H, Schraudner M, Schuh G, Wildt J (1999) Emission of volatile organic compounds from ozone-exposed plants. Ecol Appl 9:1160–1167CrossRefGoogle Scholar
  66. Heil M (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61PubMedCrossRefGoogle Scholar
  67. Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272PubMedCrossRefGoogle Scholar
  68. Hilker M, Fatouros NE (2015) Plant responses to insect egg deposition. Annu Rev Entomol 60:493–515PubMedCrossRefGoogle Scholar
  69. Hilker M, Meiners T (2010) How do plants “notice” attack by herbivorous arthropods? Biol Rev 85:267–280PubMedCrossRefGoogle Scholar
  70. Himanen SJ, Nerg A-M, Nissinen A, Pinto DM, Stewart CN Jr, Poppy GM, Holopainen JK (2009) Effects of elevated carbon dioxide and ozone on volatile terpenoid emissions and multitrophic communication of transgenic insecticidal oilseed rape (Brassica napus). New Phytol 181:174–186PubMedCrossRefGoogle Scholar
  71. Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184PubMedCrossRefGoogle Scholar
  72. Huberty AF, Denno RF (2004) Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology 85:1383–1398CrossRefGoogle Scholar
  73. Huntzinger M, Karban R, Young TP, Palmer TM (2004) Relaxation of induced indirect defenses of acacias following exclusion of mammalian herbivores. Ecology 85:609–614CrossRefGoogle Scholar
  74. Inbar M, Gerling D (2008) Plant-mediated interactions between whiteflies, herbivores, and natural enemies. Annu Rev Entomol 53:431–448PubMedCrossRefGoogle Scholar
  75. Inbar M, Doostdar H, Leibee GL, Mayer RT (1999) The role of plant rapidly induced responses in asymmetric interspecific interactions among insect herbivores. J Chem Ecol 25:1961–1979CrossRefGoogle Scholar
  76. Ingwell LL, Eigenbrode SD, Bosque-Perez NA (2012) Plant viruses alter insect behavior to enhance their spread. Sci Rep 2:578PubMedPubMedCentralCrossRefGoogle Scholar
  77. Kaplan I (2012) Attracting carnivorous arthropods with plant volatiles: the future of biocontrol or playing with fire? Biol Control 60:77–89CrossRefGoogle Scholar
  78. Karban R (2011) The ecology and evolution of induced resistance against herbivores. Funct Ecol 25:339–347CrossRefGoogle Scholar
  79. Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  80. Kessler A, Baldwin IT (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 38:639–649PubMedCrossRefGoogle Scholar
  81. Kessler D, Diezel C, Baldwin IT (2010) Changing pollinators as a means of escaping herbivores. Curr Biol 20:237–242PubMedCrossRefGoogle Scholar
  82. Kessler A, Halitschke R, Poveda K (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant-pollinator interactions. Ecology 92:1769–1780PubMedCrossRefGoogle Scholar
  83. Khan ZR, Midega CAO, Pittchar JO, Murage AW, Birkett MA, Bruce TJA, Pickett JA (2014) Achieving food security for one million sub-Saharan African poor through push-pull innovation by 2020. Philos Trans R Soc B Biol Sci 369:20120284CrossRefGoogle Scholar
  84. Koornneef A, Pieterse CMJ (2008) Cross talk in defense signaling. Plant Physiol 146:839–844PubMedPubMedCentralCrossRefGoogle Scholar
  85. Kopper BJ, Lindroth RL (2003) Effects of elevated carbon dioxide and ozone on the phytochemistry of aspen and performance of an herbivore. Oecologia 134:95–103PubMedCrossRefGoogle Scholar
  86. Landolt PJ, Tumlinson JH, Alborn DH (1999) Attraction of Colorado potato beetle (Coleoptera: Chrysomelidae) to damaged and chemically induced potato plants. Environ Entomol 28:973–978CrossRefGoogle Scholar
  87. Lehtilä K, Strauss SY (1997) Leaf damage by herbivores affects attractiveness to pollinators in wild radish, Raphanus raphanistrum. Oecologia 111:396–403CrossRefGoogle Scholar
  88. Li T, Blande JD, Gundel PE, Helander M, Saikkonen K (2014) Epichloë endophytes alter inducible indirect defences in host grasses. PLoS One 9:e101331PubMedPubMedCentralCrossRefGoogle Scholar
  89. Lins JC Jr, van Loon JJA, Bueno VHP, Lucas-Barbosa D, Dicke M, van Lenteren JC (2014) Response of the zoophytophagous predators Macrolophus pygmaeus and Nesidiocoris tenuis to volatiles of uninfested plants and to plants infested by prey or conspecifics. BioControl 59:707–718CrossRefGoogle Scholar
  90. Loreto F, Delfine S (2000) Emission of isoprene from salt-stressed Eucalyptus globulus leaves. Plant Physiol 123:1605–1610PubMedPubMedCentralCrossRefGoogle Scholar
  91. Loreto F, Schnitzler J-P (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166PubMedCrossRefGoogle Scholar
  92. Loreto F, Forster A, Durr M, Csiky O, Seufert G (1998) On the monoterpene emission under heat stress and on the increased thermotolerance of leaves of Quercus ilex L. fumigated with selected monoterpenes. Plant Cell Environ 21:101–107CrossRefGoogle Scholar
  93. Loreto F, Pinelli P, Manes F, Kollist H (2004) Impact of ozone on monoterpene emissions and evidence for an isoprene-like antioxidant action of monoterpenes emitted by Quercus ilex leaves. Tree Physiol 24:361–367PubMedCrossRefGoogle Scholar
  94. Loreto F, Barta C, Brilli F, Nogues I (2006) On the induction of volatile organic compound emissions by plants as consequence of wounding or fluctuations of light and temperature. Plant Cell Environ 29:1820–1828PubMedCrossRefGoogle Scholar
  95. Lucas-Barbosa D, van Loon JJA, Dicke M (2011) The effects of herbivore-induced plant volatiles on interactions between plants and flower-visiting insects. Phytochemistry 72:1647–1654PubMedCrossRefGoogle Scholar
  96. Lucas-Barbosa D, Sun P, Hakman A, van Beek TA, van Loon JJA, Dicke M, Koricheva J (2015) Visual and odour cues: plant responses to pollination and herbivory affect the behaviour of flower visitors. Funct Ecol 30:431–441CrossRefGoogle Scholar
  97. Maffei ME, Arimura G, Mithofer A (2012) Natural elicitors, effectors and modulators of plant responses. Nat Prod Rep 29:1288–1303PubMedCrossRefGoogle Scholar
  98. Mann RS, Ali JG, Hermann SL, Tiwari S, Pelz-Stelinski KS, Alborn HT, Stelinski LL (2012) Induced release of a plant-defense volatile ‘deceptively’ attracts insect vectors to plants infected with a bacterial pathogen. Plos Pathog 8:e1002610PubMedPubMedCentralCrossRefGoogle Scholar
  99. Martinsen GD, Driebe EM, Whitham TG (1998) Indirect interactions mediated by changing plant chemistry: beaver browsing benefits beetles. Ecology 79:192–200CrossRefGoogle Scholar
  100. McCormick AC, Unsicker SB, Gershenzon J (2012) The specificity of herbivore-induced plant volatiles in attracting herbivore enemies. Trends Plant Sci 17:303–310CrossRefGoogle Scholar
  101. Menzel TR, Huang TY, Weldegergis BT, Gols R, van Loon JJA, Dicke M (2014) Effect of sequential induction by Mamestra brassicae L. and Tetranychus urticae Koch on lima bean plant indirect defense. J Chem Ecol 40:977–985PubMedCrossRefGoogle Scholar
  102. Michereff MFF, Laumann RA, Borges M, Michereff-Filho M, Diniz IR, Neto ALF, Moraes MCB (2011) Volatiles mediating a plant-herbivore-natural enemy interaction in resistant and susceptible soybean cultivars. J Chem Ecol 37:273–285PubMedCrossRefGoogle Scholar
  103. Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19PubMedCrossRefGoogle Scholar
  104. Moayeri HRS, Ashouri A, Poll L, Enkegaard A (2007) Olfactory response of a predatory mirid to herbivore induced plant volatiles: multiple herbivory vs. single herbivory. J Appl Entomol 131:326–332CrossRefGoogle Scholar
  105. Moraes MCB, Pareja M, Laumann RA, Hoffmann-Campo CB, Borges M (2008) Response of the parasitoid Telenomus podisi to induced volatiles from soybean damaged by stink bug herbivory and oviposition. J Plant Interact 3:111–118CrossRefGoogle Scholar
  106. Mothershead K, Marquis RJ (2000) Fitness impacts of herbivory through indirect effects on plant-pollinator interactions in Oenothera macrocarpa. Ecology 81:30–40Google Scholar
  107. Musser RO, Mum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Caterpillar saliva beats plant defences. Nature 416:599–600PubMedCrossRefGoogle Scholar
  108. Musser RO, Cipollini DF, Hum-Musser SM, Williams SA, Brown JK, Felton GW (2005) Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in solanaceous plants. Arch Insect Biochem Physiol 58:128–137PubMedCrossRefGoogle Scholar
  109. Ohgushi T (2005) Indirect interaction webs: herbivore-induced effects through trait change in plants. Annu Rev Ecol Syst 36:81–105CrossRefGoogle Scholar
  110. Ohgushi T (2008) Herbivore-induced indirect interaction webs on terrestrial plants: the importance of non-trophic, indirect, and facilitative interactions. Entomol Exp Appl 128:217–229CrossRefGoogle Scholar
  111. Ohgushi T, Craig TP, Price PW (eds) (2007) Ecological communities: plant mediation in indirect interaction webs. Cambridge University Press, CambridgeGoogle Scholar
  112. Ohgushi T, Schmitz OJ, Holt RD (eds) (2012) Trait-mediated indirect interactions: ecological and evolutionary perspectives. Cambridge University Press, CambridgeGoogle Scholar
  113. Oliveira MS, Pareja M (2014) Attraction of a ladybird to sweet pepper damaged by two aphid species simultaneously or sequentially. Arthropod Plant Interact 8:547–555CrossRefGoogle Scholar
  114. Pallini A, Janssen A, Sabelis MW (1997) Odour-mediated responses of phytophagous mites to conspecific and heterospecific competitors. Oecologia 110:179–185CrossRefGoogle Scholar
  115. Pareja M, Mohib A, Birkett MA, Dufour S, Glinwood RT (2009) Multivariate statistics coupled to generalized linear models reveal complex use of chemical cues by a parasitoid. Anim Behav 77:901–909CrossRefGoogle Scholar
  116. Pareja M, Qvarfordt E, Webster B, Mayon P, Pickett J, Birkett M, Glinwood R (2012) Herbivory by a phloem-feeding insect inhibits floral volatile production. PLoS One 7:e31971PubMedPubMedCentralCrossRefGoogle Scholar
  117. Peñaflor MF, Erb M, Robert CA, Miranda LA, Werneburg AG, Dossi FC, Turlings TC, Bento JM (2011) Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize. Planta 234:207–215PubMedCrossRefGoogle Scholar
  118. Peñuelas J, Llusià J (2004) Plant VOC emissions: making use of the unavoidable. Trends Ecol Evol 19:402–404PubMedCrossRefGoogle Scholar
  119. Perfecto I, Vandermeer J (2010) The agroecological matrix as alternative to the land-sparing/agriculture intensification model. Proc Natl Acad Sci USA 107:5786–5791PubMedPubMedCentralCrossRefGoogle Scholar
  120. Perfecto I, Vandermeer J (2015) Coffee agroecology: a new approach to understanding agricultural biodiversity, ecosystem services and sustainable development. Routledge, Abingdon, OxonGoogle Scholar
  121. Petrov V, Hille J, Mueller-Roeber B, Gechev TS (2015) ROS-mediated abiotic stress-induced programmed cell death in plants. Front Plant Sci 6:69PubMedPubMedCentralCrossRefGoogle Scholar
  122. Pierik R, Ballare CL, Dicke M (2014) Ecology of plant volatiles: taking a plant community perspective. Plant Cell Environ 37:1845–1853PubMedCrossRefGoogle Scholar
  123. Pierre PS, Dugravot S, Ferry A, Soler R, van Dam NM, Cortesero AM (2011a) Aboveground herbivory affects indirect defences of brassicaceous plants against the root feeder Delia radicum Linnaeus: laboratory and field evidence. Ecol Entomol 36:326–334CrossRefGoogle Scholar
  124. Pierre PS, Jansen JJ, Hordijk CA, van Dam NM, Cortesero AM, Dugravot S (2011b) Differences in volatile profiles of turnip plants subjected to single and dual herbivory above- and belowground. J Chem Ecol 37:368–377PubMedPubMedCentralCrossRefGoogle Scholar
  125. Poelman EH, Broekgaarden C, Van Loon JJA, Dicke M (2008) Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol Ecol 17:3352–3365PubMedCrossRefGoogle Scholar
  126. Ponzio C, Gols R, Weldegergis BT, Dicke M (2014) Caterpillar-induced plant volatiles remain a reliable signal for foraging wasps during dual attack with a plant pathogen or non-host insect herbivore. Plant Cell Environ 37:1924–1935PubMedCrossRefGoogle Scholar
  127. Poveda K, Steffan-Dewenter I, Scheu S, Tscharntke T (2003) Effects of below- and above-ground herbivores on plant growth, flower visitation and seed set. Oecologia 135:601–605PubMedCrossRefGoogle Scholar
  128. Poveda K, Steffan-Dewenter I, Scheu S, Tscharntke T (2005) Effects of decomposers and herbivores on plant performance and aboveground plant-insect interactions. Oikos 108:503–510CrossRefGoogle Scholar
  129. Raguso RA (2004) Why do flowers smell? The chemical ecology of fragrance-driven pollination. In: Cardé RT, Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, Cambridge, pp 151–178CrossRefGoogle Scholar
  130. Raguso RA (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annu Rev Ecol Syst 39:549–569CrossRefGoogle Scholar
  131. Raguso RA (2009) Floral scent in a whole-plant context: moving beyond pollinator attraction. Funct Ecol 23:837–840CrossRefGoogle Scholar
  132. Rasmann S, Turlings TCJ (2007) Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecol Lett 10:926–936PubMedCrossRefGoogle Scholar
  133. Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737PubMedCrossRefGoogle Scholar
  134. Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant-plant interactions. The University of Chicago Press, ChicagoCrossRefGoogle Scholar
  135. Rodríguez-Saona C, Crafts-Brandner SJ, Canas LA (2003) Volatile emissions triggered by multiple herbivore damage: beet armyworm and whitefly feeding on cotton plants. J Chem Ecol 29:2539–2550PubMedCrossRefGoogle Scholar
  136. Rodríguez-Saona C, Chalmers JA, Raj S, Thaler JS (2005) Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoid. Oecologia 143:566–577PubMedCrossRefGoogle Scholar
  137. Rodriguez-Saona CR, Musser RO, Vogel H, Hum-Musser SM, Thaler JS (2010) Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J Chem Ecol 36:1043–1057PubMedCrossRefGoogle Scholar
  138. Rostás M, Simon M, Hilker M (2003) Ecological cross-effects of induced plant responses towards herbivores and phytopathogenic fungi. Basic Appl Ecol 4:43–62CrossRefGoogle Scholar
  139. Rostás M, Ton J, Mauch-Mani B, Turlings TCJ (2006) Fungal infection reduces herbivore-induced plant volatiles of maize but does not affect naïve parasitoids. J Chem Ecol 32:1897–1909PubMedCrossRefGoogle Scholar
  140. Rostás M, Maag D, Ikegami M, Inbar M (2013) Gall volatiles defend aphids against a browsing mammal. BMC Evol Biol 13:193PubMedPubMedCentralCrossRefGoogle Scholar
  141. Saikkonen K, Gundel PE, Helander M (2013) Chemical ecology mediated by fungal endophytes in grasses. J Chem Ecol 39:962–968PubMedCrossRefGoogle Scholar
  142. Salamanca J, Pareja M, Rodriguez-Saona C, Resende ALS, Souza B (2015) Behavioral responses of adult lacewings, Chrysoperla externa, to a rose–aphid–coriander complex. Biol Control 80:103–112CrossRefGoogle Scholar
  143. Sarmento RA, Lemos F, Bleeker PM, Schuurink RC, Pallini A, Oliveira MGA, Lima ER, Kant MR, Sabelis MW, Janssen A (2011) A herbivore that manipulates plant defence. Ecol Lett 14:229–236PubMedPubMedCentralCrossRefGoogle Scholar
  144. Schoener TW, Spiller DA (2012) Perspective: kinds of trait-mediated indirect effects in ecological communities. A synthesis. In: Ohgushi T, Schmitz OJ, Holt RD (eds) Trait-mediated indirect interactions: ecological and evolutionary perspectives. Cambridge University Press, Cambridge, pp 9–27CrossRefGoogle Scholar
  145. Schoonhoven LM, Van Loon JJA, Dicke M (2005) Insect-plant biology. Oxford University Press, OxfordGoogle Scholar
  146. Schwartzberg EG, Boroczky K, Tumlinson JH (2011) Pea aphids, Acyrthosiphon pisum, suppress induced plant volatiles in broad bean, Vicia faba. J Chem Ecol 37:1055–1062PubMedCrossRefGoogle Scholar
  147. Shiojiri K, Takabayashi J, Yano S, Takafuji A (2000) Flight response of parasitoids toward plant-herbivore complexes: a comparative study of two parasitoid-herbivore systems on cabbage plants. Appl Entomol Zool 35:87–92CrossRefGoogle Scholar
  148. Shiojiri K, Takabayashi J, Yano S, Takafuji A (2001) Infochemically mediated tritrophic interaction webs on cabbage plants. Popul Ecol 43:23–29CrossRefGoogle Scholar
  149. Shiojiri K, Takabayashi J, Yano S, Takafuji A (2002) Oviposition preferences of herbivores are affected by tritrophic interaction webs. Ecol Lett 5:186–182CrossRefGoogle Scholar
  150. da Silva SEB, França JF, Pareja M (2016) Olfactory response of four aphidophagous insects to aphid- and caterpillar-induced plant volatiles. Arthropod Plant Interact. doi: 10.1007/s11829-016-9436-x Google Scholar
  151. Soler R, Harvey JA, Kamp AFD, Vet LEM, van der Putten WH, van Dam NM, Stuefer JF, Gols R, Hordijk CA, Bezemer TM (2007) Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals. Oikos 116:367–376CrossRefGoogle Scholar
  152. Soler R, Badenes-Perez FR, Broekgaarden C, Zheng SJ, David A, Boland W, Dicke M (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 26:156–166CrossRefGoogle Scholar
  153. Stam JM, Kroes A, Li YH, Gols R, van Loon JJA, Poelman EH, Dicke M (2014) Plant interactions with multiple insect herbivores: from community to genes. Annu Rev Plant Biol 65:689–713PubMedCrossRefGoogle Scholar
  154. Steidle JLM, van Loon JJA (2003) Dietary specialization and infochemical use in carnivorous arthropods: testing a concept. Entomol Exp Appl 108:133–148CrossRefGoogle Scholar
  155. Tack AJM, Dicke M, Bennett A (2013) Plant pathogens structure arthropod communities across multiple spatial and temporal scales. Funct Ecol 27:633–645CrossRefGoogle Scholar
  156. Teuber M, Zimmer I, Kreuzwieser J, Ache P, Polle A, Rennenberg H, Schnitzler JP (2008) VOC emissions of Grey poplar leaves as affected by salt stress and different N sources. Plant Biol 10:86–96PubMedCrossRefGoogle Scholar
  157. Thaler JS, Owen B, Higgins VJ (2004) The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiol 135:530–538PubMedPubMedCentralCrossRefGoogle Scholar
  158. Thaler JS, Agrawal AA, Halitschke R (2010) Salicylate-mediated interactions between pathogens and herbivores. Ecology 91:1075–1082PubMedCrossRefGoogle Scholar
  159. Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270PubMedCrossRefGoogle Scholar
  160. Theis N, Kesler K, Adler LS (2009) Leaf herbivory increases floral fragrance in male but not female Cucurbita pepp subsp. texana (Cucurbitaceae) flowers. Am J Bot 96:897–903PubMedCrossRefGoogle Scholar
  161. Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, ChicagoGoogle Scholar
  162. Ton J, D’Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TCJ (2006) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26PubMedCrossRefGoogle Scholar
  163. Valkama E, Koricheva J, Oksanen E (2007) Effects of elevated O3, alone and in combination with elevated CO2, on tree leaf chemistry and insect herbivore performance: a meta-analysis. Glob Chang Biol 13:184–201CrossRefGoogle Scholar
  164. Van Emden HF, Kifle AT (2002) Performance of the parasitoid Aphidius colemani when reared on Myzus persicae on a fully defined artificial diet. BioControl 47:607–616CrossRefGoogle Scholar
  165. Van Zandt PA, Agrawal AA (2004a) Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616–2629CrossRefGoogle Scholar
  166. Van Zandt PA, Agrawal AA (2004b) Specificity of induced plant responses to specialist herbivores of the common milkweed Asclepias syriaca. Oikos 104:401–409CrossRefGoogle Scholar
  167. Velikova V, Loreto F (2005) On the relationship between isoprene emission and thermotolerance in Phragmites australis leaves exposed to high temperatures and during the recovery from a heat stress. Plant Cell Environ 28:318–327CrossRefGoogle Scholar
  168. Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritophic context. Annu Rev Entomol 37:141–172CrossRefGoogle Scholar
  169. Vickers CE, Possell M, Cojocariu CI, Velikova VB, Laothawornkitkul J, Ryan A, Mullineaux PM, Nicholas Hewitt C (2009) Isoprene synthesis protects transgenic tobacco plants from oxidative stress. Plant Cell Environ 32:520–531PubMedCrossRefGoogle Scholar
  170. Viswanathan DV, Narwani AJT, Thaler JS (2005) Specificity in induced plant responses shapes patterns of herbivore occurrence on Solanum dulcamara. Ecology 86:886–896CrossRefGoogle Scholar
  171. Viswanathan DV, Lifchits OA, Thaler JS (2007) Consequences of sequential attack for resistance to herbivores when plants have specific induced responses. Oikos 116:1389–1399CrossRefGoogle Scholar
  172. Viswanathan DV, McNickle G, Thaler JS (2008) Heterogeneity of plant phenotypes caused by herbivore-specific induced responses influences the spatial distribution of herbivores. Ecol Entomol 33:86–94CrossRefGoogle Scholar
  173. Vuorinen T, Nerg A-M, Holopainen JK (2004) Ozone exposure triggers the emission of herbivore-induced plant volatiles, but does not disturb tritrophic signalling. Environ Pollut 131:305–311PubMedCrossRefGoogle Scholar
  174. Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216PubMedGoogle Scholar
  175. Walling LL (2008) Avoiding effective defenses: strategies employed by phloem-feeding insects. Plant Physiol 146:859–866PubMedPubMedCentralCrossRefGoogle Scholar
  176. Wäschke N, Meiners T, Rostás M (2013) Foraging strategies of parasitoids in complex chemical environments. In: Wajnberg E, Colazza S (eds) Chemical ecology of insect parasitoids. Wiley-Blackwell, Chichester, pp 37–63CrossRefGoogle Scholar
  177. Weech MH, Chapleau M, Pan L, Ide C, Bede JC (2008) Caterpillar saliva interferes with induced Arabidopsis thaliana defence responses via the systemic acquired resistance pathway. J Exp Bot 59:2437–2448PubMedPubMedCentralCrossRefGoogle Scholar
  178. Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84:1083–1100CrossRefGoogle Scholar
  179. Winkel-Shirley B (2002) Biosynthesis of flavonoids and effects of stress. Curr Opin Plant Biol 5:218–223PubMedCrossRefGoogle Scholar
  180. Winter TR, Rostás M (2008) Ambient ultraviolet radiation induces protective responses in soybean but does not attenuate indirect defense. Environ Pollut 155:290–297PubMedCrossRefGoogle Scholar
  181. Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annu Rev Ecol Syst 25:443–466CrossRefGoogle Scholar
  182. Wu J, Baldwin IT (2009) Herbivory-induced signalling in plants: perception and action. Plant Cell Environ 32:1161–1174PubMedCrossRefGoogle Scholar
  183. Yamamoto M, Shiojiri K, Uefune M, Takabayashi J (2011) Preferences of parasitic wasps for cabbage plants infested by plural herbivore species. J Plant Interact 6:167–168CrossRefGoogle Scholar
  184. Yuan S, Lin HH (2008) Role of salicylic acid in plant abiotic stress. Zeitschrift Fur Naturforschung Sect C J Biosci 63:313–320Google Scholar
  185. Zakir A, Sadek MM, Bengtsson M, Hansson BS, Witzgall P, Anderson P, Heil M (2013) Herbivore-induced plant volatiles provide associational resistance against an ovipositing herbivore. J Ecol 101:410–417CrossRefGoogle Scholar
  186. Zangerl AR, Berenbaum MR (2009) Effects of florivory on floral volatile emissions and pollination success in the wild parsnip. Arthropod Plant Interact 3:181–191CrossRefGoogle Scholar
  187. Zarate SI, Kempema LA, Walling LL (2007) Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses. Plant Physiol 143:866–875PubMedPubMedCentralCrossRefGoogle Scholar
  188. Zhang P-J, Zheng S-J, van Loon JJA, Boland W, David A, Mumm R, Dicke M (2009) Whiteflies interfere with indirect plant defense against spider mites in Lima bean. Proc Natl Acad Sci USA 106:21202–21207PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Departamento de Biologia Animal, Instituto de BiologiaUniversidade Estadual de Campinas—UNICAMPCampinasBrazil
  2. 2.Laboratório de Ecologia Química, Departamento de Ecologia, Centro de Ciências Biológicas e da SaúdeUniversidade Federal de Sergipe—UFSSão CristóvãoBrazil

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