The role of herbivore-induced plant volatiles (HIPVs) as indirect plant defense mechanism in a diverse plant and herbivore species; a review

Year 2018, Volume: 2 Issue: 4, 139 - 147, 20.12.2018

Haftay Gebreyesus Gebreziher

https://doi.org/10.31015/jaefs.18024

Cited By: 10

Abstract

When
plants are attacked by herbivores, they release plant volatiles
called herbivore-induced plant volatiles (HIPVs) to the environment to
communicate with higher trophic levels. HIPVs play different ecological roles
such as plant-plant interaction, plant-herbivore interaction, tritrophic interaction
and other related interactions. Attractiveness of HIPVs to natural enemies in a
tritrophic interaction varies depending on species diversity. Under natural and
multiple cropping systems, tritrophic interaction is expected to be more
complex than single tritrophic interaction with one species per trophic level.
In complex tritrophic interaction, diversity of different trophic levels
affects attractiveness of HIPVs to natural enemies. From plant diversity point
of view, HIPVs mixture emanating from herbivore-damaged multiple plant species
are reported to affect behavioral responses and foraging behavior of natural
enemies under laboratory and field conditions. Similarly, from herbivore
diversity point of view, in nature, plants are commonly attacked by more than
one herbivore species. Constituents of HIPVs vary between
plants infested by multiple and single herbivore species and this affects the
behavioral responses and foraging behavior of natural enemies. This
paper reviews recent
findings on the role of HIPVs as indirect plant defense in systems with simple
tritrophic interaction, and in diverse plants species and diverse herbivore
species.

Keywords

Herbivore-induced plant volatiles (HIPVs), Tritrophic interaction, Natural enemies, Herbivores, Species diversity

References

• Alhmedi, A., Haubruge, E., Francis, F. (2010). Identification of limonene as a potential kairomone of the harlequin ladybird Harmonia axyridis (Coleoptera: Coccinellidae). Eur. J. Entomol. 107: 541-548
• Arimura, G. Ozawa, R., Maffei, M.E. (2011). Recent advances in plant early signaling in response to herbivory. Intl J Molecul Sci 12: 3723-3739
• Baldwin, I.T., Halitsschke, R., Paschold, A., von Dahl, C.C., Preston, C.A. (2006). Valatiles signaling in plant-plant interaction: “Talking trees” in the genomics era. Science 311: 812-815
• Bernasconi, M.L., Turlings, T.C.J., Ambrosetti, L., Bassetti, P., Dorn, S. (1998). Herbivore-induced emissions of maize volatiles repel the corn aphid, Rhopalosiphum maidis. Entomologia Experimentalis et Applicata 87(2):133-142
• Bouwmeester, H.J., Verstappen, F.W.A., Aharoni, A., Lucker, J., Jongsma, M.A. (2003). Exploring multi-trophic plant-herbivore interactions for new crop protection methods. Proc. BCPC Interl Congress Crop Sc. and Tech 2: 1123-1134
• Cai, X.M., Sun, X.L., Dong, W.X., Wang, G.C., Chen, Z.M. (2014). Herbivore species, infestation time, and herbivore density affect induced volatiles in tea plants. Chemoecol 24: 1-14
• Carroll, M.J., Schmelz, E.A., Teal, P.E. (2008). The attraction of Spodoptera frugiperda Neonates to cowpea seedlings is mediated by volatiles induced by conspecific herbivory and the elicitor inceptin. J Chem Ecol 34: 291-300
• Choh, Y., Takabayashi, J. (2010). Herbivore-induced plant volatiles prime two indirect defenses in Lima bean. Trends in Acarology: Proc. Of the 12th international congress, DOI 10.1007/978-90-481-9837-5 41
• Colazza, S., Fucarino, A., Peri, E., Salerno, G., Conti, E., Bin, F. (2004). Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. The Journal of Experimental Biology 207: 47-53
• Coll, M., Guershon, M. (2002). Omnivory in terrestrial arthropods: mixing plant and prey diets. Annual Review of Entomology 47: 267-297
• Cusumano, A., Weldegergis, B.T., Colazza, S., Dicke, M., Fatouros, N.E. (2015). Attraction of egg-killing parasitoids toward induced plant volatiles in a multi-herbivore context. Oecologia Doi. 10.1007/s00442-015-3325-3
• Das, A., Lee, S., Hyun, T.K., Kim, S., Kim, J. (2013). Plant volatiles as method of communication. Plant Biotechnol Rep 7:9-26
• De Boer, J.G., Hordijk, C.A., Posthumus, M.A., Dicke, M. (2008). Prey and non-prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction. J Chem Ecol 34: 281-290
• De Moraes, C.M., Mescher, M.C., Tumlinson, J.H. (2001). Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410: 577-580
• De Vos, M., Van Oosten, V.R., Van Poecke, R.M.P., Van Pelt, J.A., Pozo, M.J., Mueller, M.J., Buchala, A.J., Metraux, J., Van Loon, L.C., Dicke, M., Pieterse, M.J. (2005). Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. MPMI 18(9): 923-937
• Delphia, C.M., Mescher, M.C., De Moraes, C.M. (2007). Induction of volatiles by herbivores with different feeding habits and effects of induced defenses on host-plant selection by thrips. J Chem Ecol 33: 997-1012
• Dicke, M. (2009). Behavioral and community ecology of plants that cry for help. Plant Cell Environ 32: 654-665
• Dicke, M. (2015). Herbivore-induced plant volatiles as a rich source of information for arthropod predators: fundamental and applied aspect. J of Indian Institute of Science 95(1): 35-42
• Dicke, M., Van Beek, T.A., Posthumus, M.A., Ben Dom, N., Van Bokhoven, H., De Groot, A.E. (1990b). Isolation and identification of volatile kairomone that affects acarine predator-prey interactions. J Chem Ecol 16(2): 381-396
• Dicke, M., Baldwin, I.T. (2010). The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends in Plant Science 15: 167-175
• Dicke, M., de Boer, J.G., Hofte, M., Rocha-Granados, M.C. (2003). Mixed blends of herbivore-induced volatiles and foraging success of carnivorous arthropods. OIKOS 101:38-48
• Dicke, M., Sabelis, M.W. (1988). How plants obtain predatory mites as body guard. Netherlands J Zool 38: 148-165
• Dicke, M., Sabelis, M.W. (1989). Does it play plants to advertise for bodyguards? Towards a cost-benefit analyses of induced synomone production. In: Lambers H, Cambridge ML, Konings H and Pons TL eds Causes and Consequences of Variation in Growth Rate and Productivity of Higher Plants. SPB Publishing, The Hague, Netherlands, pp 341–358
• Dicke, M., Sabelis, M.W., De Jong, M. (1988). Analysis of prey preference in phytoseiid mites by using olfactometer, predation models and electrophoresis. Experimental and Applied Acarology 5: 225-241
• Dicke, M., Sabelis, M.W., Takabayashi, J., Bruin, J., Posthhumus, J. (1990a). Plant strategies of manipulating predator-prey interactions through allelochemicals: Prospects for application in pest control. J Chem Ecol 16: 3091-3118
• Dicke, M., Takabayashi, J., Posthumus, M.A., Schutter, C., Krips, O.E. (1998). Plant-phytoseiid interaction mediated by herbivore-induced plant volatiles: variation in production of cues and in response of predatory mites. Experimental & Applied Acarology 22: 311-333
• Dicke, M., van Loon, J.J.A. (2003). Multitrophic effects of herbivore-induced plant volatiles in an evolutionary context. Entomologia Experimentalis et Applicata 97: 237-249
• Dicke, M., Van Loon, J.J.A., Soler, R. (2009). Chemical Complexity of volatiles from plants induced by multiple attacks. Nature Chemical Biology 5: 317-324
• Drukker, B., Bruin, J., Jacobs, G., Kroon, A., Sabelis, M.W. (2000a). How predatory mites learn to cope with variability in volatile plant signals in the environment of their herbivorous prey. Environmental and Applied Acarology 24: 881-895
• Drukker, B., Bruin, J., Sabelis, M.W. (2000b). Anthocorid predators learn to associate herbivore-induced plant volatiles with presence or absence of prey. Physiol Entomol. 25: 260-265
• Drukker, B., Scutareanu, P., 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., Sabelis, M.W. (1990). Anthocorid bugs respond to odor emanating from Psylla infested pear trees. Netherlands Entomological Society 1: 88-89
• Fadini, M.A.M., Venzone, M., Oliveira, H., Pallini, A., Vilela, E.F. (2010). Response of the predatory mite Phytoseiulus macropilis volatiles by strawberry plants in response to attack by Tetranychid mites (Acari: Phytoseiidae: Tetranychidae). Neotropical Entomol 39:248-252
• Ferrero, M., Tixier, M.S., Kreiter, S. (2014). Different feeding behaviors in a single predatory mite species. 2. Response of two populations of Phytoseiulus longipes (Acari: Phytoseiidae) to various prey species, prey stage and plant substrates. Exp Appl Acarol 62: 325-335
• Fortuna, T.M., Woelke, J.B., Hordijk, C.A., Jansen, J.J., van Dam, N.M., Vet, L.E.V., Harvey, J.A. (2013). A tritrophic approach to preference-performance hypothesis involving an exotic and native plant. Biol Invasions 15: 2387-2401
• Gohole, L.S., Overholt, W.A., Khan, Z.R., Vet, L.E.M. (2003). Role of volatiles emitted by host and non-host plants in the foraging behavior of Dentichasmias busseollae, a pupal parasitoid of the spotted stemborer Chilo partellus. Entomologia Experimentalis et Applicata 107: 1-9
• Guerrieri, E., Poppy, G.M., Powell, W., Tremblay, E., Pennacchio, F. (1999). Induction and systemic release of herbivore-induced plant volatiles mediating in-flight orientation of Aphidius ervi. J Chem Ecol 25(6):1247-1261
• Haddad, N.M., Crutsunger, G.M., Gross, K., Haarstad, J., Tilman, D. (2011). Plant diversity and the stability of food webs. Ecol Lett 14: 42-46 Haftay, G.G., Nakamuta, K. (2016a). Responses of a predatory bug to a mixture of herbivore-induced plant volatiles from multiple plant species. Arthropod-Plant Interactions 10:429-444
• Haftay G.G., Nakamuta, K. (2016b). A mixture of herbivore-induced plant volatiles from multiple host plant species enhances the attraction of a predatory bug under field-cage conditions. Arthropod-Plant Interactions 10: 507-515
• Harris, C.M., Ruberson, J.R., Meagher, R., Tumlinson, J.H. (2012). Host suitability affects odor association in Cotesia marginiventris implications in generalist parasitoid host-finding. J Chem Ecol 38: 340-347
• Heil, M., Karban, R. (2010). Explaining evolution of plant communication by airborne signals. Trends in Ecology and Evolution 25(3): 137-144
• Hoballah, M.E.F., Turlings, T.C.J. (2001). Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids. Evol Ecol Res 3: 553-565
• Holopainene, J.K., Gershenzon, J. (2010). Multiple stress factors and the emission of plant VOCs Trends in Plant Science 15(3): 176-184 James, D.G. (2003a). Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: methyl salicylate and the green lacewing, Chrysopa nigricornis. J Chem Ecol 29(7): 1601-1609
• James, D.G. (2003b). Synthetic herbivore-induced plant volatiles as field attractants for beneficial insects. Environ. Entomol. 32(5): 977-982
• James, D.G. (2005). Further field evaluation of synthetic herbivore-induced plan volatiles as attractants for beneficial insects. J Chem Ecol 31:481–495. Doi: 10.1007/s10886-005-2020-y
• James, D.G., Grasswitz, T.R. (2005). Synthetic herbivore-induced plant volatiles increase field captures of parasitic wasps. BioControl 50: 871-880. doi: 10.1007/s10526-005-3313-3
• Jams, D.G. and Price, T.S. (2004). Field testing of Methyl Salicylate for recruitment and retention of beneficial insects in grapes and hops. J Chem Ecol 30(8): 1613-1628
• Johnson, S.N., Clark, K.E., Hartley, S.E., Jones, T.H., McKenzie, S.W., Koricheva, J. (2012). Aboveground-belowground herbivore interaction: a meta-analysis. Ecology 93(10): 2208-2215
• Jones, V.P., Steffan, S.A., Wiman, N.G., Horton, D.R., Miliczky, E., Zhang, Q., Baker, C.C. (2011). Evaluation of herbivore-induced plant volatiles for monitoring green lacewings in Washington apple orchards. Biological Control 56: 98-105
• Kaplan, I. (2012). Attracting carnivorous arthropods with plant volatiles: The future of biocontrol or playing with fire? Biological Control 60: 77-89
• Kessler, A., Baldwin, I.T. (2002). Plant responses to insect herbivory: the emerging molecular analysis. Annu. Rev. Plant Biol. 53:299-328
• Kost, C., Heil, M. (2006). Herbivore-induced plant volatiles induce an indirect defense in neighboring plants. J Ecol 94:619-628
• Maeda, T., Kishimoto, H., Wright, L.C., James, D.G. (2015). Mixture of synthetic herbivore-induced plant volatiles attracts more Stethorus punctum picipes (Casey) (Coleoptera: Coccinellidae) than a single volatile. J Insect Behav. Doi: 10.1007/s10905-015-9489-1
• Maeda, T., Takabayashi, J., Yano, S., Takafuji, A. (1999). Response of the predatory mite, Amblyseius womersleyi (Acari: Phytoseiidae) toward herbivore-induced plant volatiles: variation in response to two local populations. Appl. Entomol. Zool. 34(4): 449-454
• Maffei, M.E., Mithofer, A., Boland, W. (2007). Insect feeding on plants: Rapid signals and responses preceding the induction of phytochemical release. Phytochemistry 68: 2946-2959
• Mattiacci, L., Dicke, M., Posthumus, A. (1994). Induction of parasitoid attracting synomone in Brussels sprouts plants by feeding of Pieris brassicae larvae: role of mechanical damaged and herbivore elicitor. J Chem Ecol 20(9): 2229-2247
• Menzel, T.R., Weldegergis, B.T., David, A., Boland, W., Gols, R., Van Loon, J.J.A., Dicke, M. (2014). Synergism in the effect of prior jasmonic acid application on herbivore-induced volatile emission by Lima bean plants: transcription of monoterpene synthase gene and volatile emission. J of Exp Bot. doi:10.1093/jxb/eru242
• Moayeri, H.R.S., Ashouri, A., Brodsgaard, H.F., Enkegaard, A. (2006a). Odor-mediated preference and prey preference of Macrolophus caliginosus between spider mites and green peach aphids. J of Appl Entomol 130(9-10): 504-508
• Moayeri, H.R.S., 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: 326-332
• Moreira, X., Mooney, K.A., Zas, R., Samperdo, L. (2012). Bottom-up effects of host-plant species diversity and top-down effects of ants interactively increase plant performance. Proc Royal Soc B doi:10.1098/rspb.2012.0893
• Murchie, A.K., Smart, L.E., Williams, I.H. (1997). Responses of Dasineura brassicae and its parasitoids Platygaster subuliformis and Omphale clypealis to field traps baited with organic isothiocyanates. J Chem Ecol 23(4): 917-926
• Ninkovic, V., Al Abassi, S., Pettersson, J. (2001). The influence of aphid-induced plant volatiles on ladybird beetle searching behavior. Biological Control 21: 191-195
• Orre, G.U.S., Wratten, S.D., Jonsson, M., Hale, R.J. (2010). Effects of an herbivore-induced plant volatile on arthropods from three trophic levels in brassicas. Biological Control 53:62–67
• Ozawa, R., Arimura, G., Takabayashi, J., Shimoda, T., Nishioka, T. (2000) Involvement of Jasmonate- and salicylate-related signaling pathways for the production of specific herbivore-induced volatiles in plants. Plant Cell Physiology 41(4): 391-398
• Pare, P.W., Tumlinson, J.H. (1999). Plant volatiles as a defense against insect herbivores. Plant Physiology 121: 325-331
• Pearse, I., Hughes, K., Shiojiri, K., Ishizaki, S. and Karban, R. (2013). Interplant volatile signaling in willows: revisiting the original talking trees. Oecologia 172: 869-875 Price, P.W., Bouton, C.E., Gross, P., McPheron, B.A., Thompson, J.N., Weis, A.E. (1980). Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41-65
• Rasmann, S., Turlings, T.C.J. (2007). Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Oikos 10(10): 926-936
• Robert, C.A., Erb, M., Duployer, M., Zwahlen, C., Doyen, G.R., Turlings, T.C.J. (2012). Herbivore-induced plant volatiles mediate host selection by a root herbivore. New Phytologist 194: 1061-1069
• Rodriguez-Saona, C., Chalmer, J.A., Raj, S., Thaler, J.S. (2005). Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoids. Oecologia 143: 566-577
• Rose, U.S.R., Lewis, W.J., Tumlinson, J.H. (1998). Specificity of systemically released cotton volatiles as attractants for specialist and generalis parasitic wasps. J Chem Ecol 24(2):303-319
• Sabelis, M.W., Van den Baan, H.E. (1983). Location of distant spider mite colonies by phytoseid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi. Ent. Exp. and appl. 33: 303-314
• Shiojiri, K., Takabayashi, J., Takafuji, S.Y.A. (2001). Infochemically mediated interaction webs on cabbage plants. Population Ecology 43: 23-29
• Tatemoto, S., Shimoda, T. (2008). Olfactory response of predatory mites (Neoseiulus cucumeris and insects (Orius strigicollis) to two different plant species infested with onion thrips (Thrips tabaci). J Chem Ecol 34: 605-613
• Titayavan, M., Altieri, M.A. (1990). Synomone-mediated interactions between the parasitoid Diaeretiella rapae and Brevicoryne brassicae under field conditions. Entomophaga 35(4): 499-507
• Turlings, T.C.J., Tumlinson, J.H. (1992). Systemic release of chemical signals by herbivore-injured corn. Proc. Natl. Acad. Sci 89: 8399-8402
• Turlings, T.C.J., Tumlinson, J.H., Heath, R.R., Proveaux, A.T., Doolittle, R.E. (1991). Isolation and identification of allelochemicals that attract the larval parasitoid, Cotesia marginiventris (Cresson), to the microhabitat of one of its host. J Chem Ecol 17(11): 2235-2250
• Turlings, T.C.J., Tumlinson, J.H., Lewis, W.J. (1990). Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250: 1251-1253
• Turlings, T.C.J., Wackers, F. (2004). Recruitment of predators and parasitoids by herbivore-injured plants. In: Advances in Insect Chemical Ecology, R T Carde and J G Millar (eds) pp 21-75. Cambridge University Press 2004
• Uefune, M., Kugimiya, S., Ozawa, R., Takabayashi, J. (2013). Parasitic was females are attracted to blends of host induced plant volatiles: do qualitative and quantitative differences in the blend matter? F1000Research 2: 57
• Uefune, M., Kugimiya, S., Takabayashi, J. (2012). Herbivore-induced carnivore attractants enhance the residence time of carnivores on a host food plant. J ournal of Plant Interaction 6(2-3)
• Van Poecke RMP, Dicke M (2002) Induced parasitoid attraction by Arabidopsis thaliana: involvement of the octadecanoid and salicylic acid pathway. J of Experimental Botany 53(375): 1793-1799
• Van Poecke, R.M.P., Posthumus, M.A., Dicke, M. (2001). Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid Cotesia rubecula: chemical, behavioral, and gene-expression analysis. J Chem Ecol 27(10): 1911-1928
• Venzon, M., Janssen, A., Sabelis, M.W. (1999). Attraction of a generalist predator towards herbivore-infested plants. Entomologia Experimentalis et Applicata 93: 305-314
• Vos. M,, Berrocal, S.M., Karamaouna, F., Hemerik, L., Vet, L.E.M. (2001). Plant-mediated indirect effects and the persistence of parasitoid-herbivore communities. Ecology Letters 4: 38-45
• War, A.R., Paulraj, M.G., Ignacimuthu, S., Sharma, H.C. (2015). Induced resistance to Helicoverpa armigera through exogenous application of jasmonic acid and salicylic acid in groundnut, Arachis hypogaea. Pest Manag Sci 71: 72-82
• Waschke, N., Hardge, K., Hancock, C., Hilker, M., Obermaier, E. et al. (2014). Habitats as complex odor environments: How does plant diversity affect herbivore and parasitoid orientation? PLoS ONE 9(1): e85152
• Waschke, N., Meiners, T., Rostas, M. (2013). Foraging strategies of parasitoids in complex chemical environments. In: Wajnberg E and Colazza S (eds) Chemical ecology of insect parasitoids, first edition. John Wiley and Sons, Ltd, Wiley-Blackwell, Chichester
• Wei, J., Van Loon, J.J.A., Gols, R., Menzel, T.R., Li, N., Kang, L.d., Dicke, M. (2014). Reciprocal crosstalk between jasmonate and salicylate defense-signaling pathways modulates plant volatile emission and herbivore host-selection behavior. J of Experimental Botany doi:10.1093/jxb/eru181
• Xu, X., Borgemeister, C., Poehling, H. (2006). Interactions in the biological control of western flower thrips Frankliniella occidentalis (Pergande) and two-spotted spider mites Tetranychus urticae Koch by predatory Orius insidious Say on beans. Biological Control 36: 57-64
• Yan, Y., Yan, Y., Wang, C. (2005). Attractiveness of tobacco volatiles induced by Helicoverpa armigera and Helicoverpa assulta to Compoletis chloridae. Chinese Science Bulletin 50(13): 1334-1341
• Yu, H., Zhang, Y., Wu, K., Gao, X.W., Guo, Y.Y. (2008). Field-testing of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. Environ Entomol 37(6): 1410-1415.
• Yu, H., Zhang, Y., Wychuys, K.A.G., Wu, K., Gao, X., Guo, Y. (2010). Electrophysiological and behavioral response of Microplitis mediator (Hymenoptera: Braconidae) to caterpillar-induced volatiles from cotton. J of Environ Entomol 39: 606-609
• Zhang, Y., Xie, Y., Xue, J., Peng, G., Wang, X. (2009). Effect of Volatile Emissions, especially α-pinene, From Persimmon Trees Infested by Japanese Wax Scales or Treated with Methyl Jasmonate on Recruitment of Ladybeetle Predators. Environ Entomol 38: 1439-1445
• Zhang, Y., Xie, Y., Xue, J., Yang, Z., Gong, S. (2012). Response of predatory insect, Chrysopa sinica, toward the volatiles of persimmon trees infested with the herbivore Japanese Wax scalw. International J of Ecology 2012, ID 653869. doi:10.1155/2012/653869
• Zhu, J., Cosse, A.A., Obry, C.K.I., JJ Boo, K.S., Baker, T.C. (1999). Olfactory reactions of the twelve-spotted lady beetle, Coleomegilla maculate and the green lacewing, Chrysoperla carnea to semiochemicals released from prey and host plant: Electroantenogram and behavioral responses. J Chem Ecol 25(5): 1163-1177
• Zhu, J., Park, K. (2005). Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J Chem Ecol 31(8): 1733-1746