Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-26T03:19:03.711Z Has data issue: false hasContentIssue false
  • English
  • Français

Herbivory-induced plant volatiles from Oryza sativa and their influence on chemotaxis behaviour of Tibraca limbativentris stal. (Hemiptera: Pentatomidae) and egg parasitoids

Published online by Cambridge University Press:  12 March 2014

R.C. Melo Machado ,
J. Sant'Ana ,
M.C. Blassioli-Moraes ,
R.A. Laumann  and
M. Borges
R.C. Melo Machado
Affiliation:
Departamento de Fitossanidade, Faculdade de Agronomia, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil
J. Sant'Ana*
Affiliation:
Departamento de Fitossanidade, Faculdade de Agronomia, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brazil
M.C. Blassioli-Moraes
Affiliation:
Embrapa Recursos Genéticos e Biotecnologia, Brasília, Brazil
R.A. Laumann
Affiliation:
Embrapa Recursos Genéticos e Biotecnologia, Brasília, Brazil
M. Borges
Affiliation:
Embrapa Recursos Genéticos e Biotecnologia, Brasília, Brazil
*
*Author for correspondence Phone: +55 51 3308-7414 Fax: +55 51 3308-6015 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The rice stem bug, Tibraca limbativentris Stal. (Hemiptera: Pentatomidae) is one of the most important pests of rice crops, especially irrigated crops. Plant defence strategies against these bugs may involve the emission of chemical compounds, which are released following herbivore attacks, directly or indirectly harming pest performance. The aim of this study was to evaluate the influence of constitutive and herbivory-induced volatiles from rice plants (Oryza sativa L.) on the behavioural responses of T. limbativentris adults and egg parasitoids Trissolcus basalis (Wollaston) and Telenomus podisi (Ashmead) (Hymenoptera, Platygastridae). Plant volatiles were collected from undamaged plants of the rice cultivar IRGA 424 and from plants that suffered herbivory by five males or five females of T. limbativentris. Air-entrainment extracts were analysed by GC–flame ionization detector and GC–MS, and insect responses evaluated in a ‘Y’ olfactometer. T. limbativentris feeding damaged on rice plants induced the release of 16 volatiles compounds in a higher amounts compared to undamaged plants The main compounds induced were (E)-2-hexenal, (E)-2-octen-1-ol, methyl salicylate and α-muurolene. Female bugs were significantly attracted to air-entrainment extracts containing volatiles from undamaged plants compared with air-entrainment extracts containing volatiles emitted from plants damaged by T. limbativentris, whereas males showed no preference. Telenomus podisi females were significantly attracted to volatiles from air-entrainment extracts of plants damaged by females, whereas T. basalis showed no preference. These results suggest that rice plants may be emitting defence compounds, which could be avoided by T. limbativentris females and also acted indirectly by attracting natural enemies.

Keywords

rice plantsstink bugTrissolcus basalisTelenomus podisisemiochemicalkairomone
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 104 , Issue 3 , June 2014 , pp. 347 - 356
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Addesso, K.M. & Mcauslane, H.J. (2009) Pepper weevil attraction to volatiles from host and nonhost plants. Environmental Entomology 38, 216–224.Google Scholar
Addesso, K.M., Mcauslane, H.J. & Alborn, H.T. (2011) Attraction of pepper weevil to volatiles from damaged pepper plants. Entomologia Experimentalis et Applicata 91, 1–11.Google Scholar
Arimura, G., Matsui, K. & Takabayashi, J. (2009) Chemical and molecular ecology of herbivore-induced plant volatiles: proximate factors and their ultimate functions. Plant and Cell Physiology 50, 911–923.Google Scholar
Aquino, M.F.S., Dias, A.M., Borges, M., Moraes, M.C.B. & Laumann, R.A. (2012) Influence of visual cues on host-searching and learning behaviour of the egg parasitoids Telenomus podisi and Trissolcus basalis . Entomologia Experimentalis et Applicata 145, 162–174.CrossRefGoogle Scholar
Blackmer, J.L., Rodriguez-Saona, C., Byers, J.A., Shope, K.L. & Smith, J.P. (2004) Behavioural response of Lygus hesperus to conspecifics and headspace volatiles of alfalfa in a y-tube olfactometer. Journal of Chemical Ecology 30, 1547–1564.CrossRefGoogle Scholar
Blassioli-Moraes, M.C., Borges, M. & Laumann, R.A. (2013) The application of chemical cues in Arthropod Pest management for arable crops. pp. 225–239 in Wajnberg, E. & Colazza, S. (Eds) Chemical ecology of insect parasitoids. West Sussex-UK, Wiley–Blackwell.Google Scholar
Borges, M., Schmidt, F.G.V., Sujii, E.R., Medeiros, M.A., Mori, K., Zarbin, P.H.G. & Ferreira, J.T.B. (1998) Field responses of stink bugs to the natural and synthetic pheromone of the Neotropical brown stink bug, Euschistus heros (Heteroptera : Pentatomidae). Physiological Entomology 23, 202–207.CrossRefGoogle Scholar
Borges, M., Colazza, S., Ramirez-Lucas, P., Chauhan, K.R., Moraes, M.C.B. & Aldrich, J.R. (2003) Kairomonal effect of walking traces from Euschistus heros (Heteroptera: Pentatomidae) on two strains of Telenomus podisi (Hymenoptera: Pentatomidae). Physiological Entomology 28, 349–355.CrossRefGoogle Scholar
Borges, M., Birkett, M., Aldrich, J.R., Oliver, J.E., Chiba, M., Murata, Y., Laumann, R.A., Barrigossi, J.A., Pickett, J.A. & Moraes, M.C.B. (2006) Sex attractant pheromone from the rice stalk stink bug, Tibraca limbativentris Stal. Journal of Chemical Ecology 32, 2749–2761.CrossRefGoogle ScholarPubMed
Bruce, T.J.A. & Pickett, J.A. (2011) Perception of plant volatile blends by herbivorous insects – finding the right mix. Phytochemistry 72, 1605–1611.Google Scholar
Bruce, T.J.A., Midega, C.A.O., Birkett, M.A., Pickett, J.A. & Khan, Z.R. (2010) Is quality more important than quantity? Insect behavioural responses to changes in a volatile blend after stemborer oviposition on an African grass. Biology Letters 6, 314–317.Google Scholar
Cheng, A.X., Xiang, C.Y., Li, J.X., Yang, C.Q., Hu, W.L., Wang, L.J., Lou, Y.G. & Chen, X.Y. (2007) The rice (E)-β-caryophyllene synthase (OsTPS3) accounts for the major inducible volatile sesquiterpenes. Phytochemistry 68, 1632–1641.CrossRefGoogle ScholarPubMed
Colazza, S., Salerno, G. & Wajnberg, E. (1999) Volatile and contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biological Control 16, 310–317.Google Scholar
Colazza, S., Mcelfresh, J.S. & Millar, J.G. (2004 a) Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attracts the egg parasitoid Trissolcus basalis . Journal of Chemical Ecology 30, 945–964.Google Scholar
Colazza, S., Fucarino, A., Peri, E., Salerno, G., Conti, E. & Bin, F. (2004 b) Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids. Journal of Experimental Biology 207, 47–53.Google Scholar
Colazza, S., Bue, M.L., Giudice, D.L. & Peri, E. (2009) The response of Trissolcus basalis to footprint contact kairomones from Nezara viridula females is mediated by leaf epicuticular waxes. Naturwissenschaften 96, 975–981.Google Scholar
Conti, E. & Colazza, S. (2012) Chemical Ecology of Egg Parasitoids Associated with True Bugs. Psyche 2012, 1–11.Google Scholar
Cook, S.M., Khan, Z.R. & Pickett, J.A. (2007) The use of push-pull strategies in Integrated Pest Management. Annual Review of Entomology 52, 375–400.Google Scholar
D'Alessandro, M. & Turlings, T.C.J. (2005) In situ modification of herbivore-induced plant odors: a novel approach to study the attractiveness of volatiles organic compound to parasitic wasps. Chemical Senses 30, 739–753.Google Scholar
De Moraes, C.M., Lewis, W.J., Pare, P.W., Alborn, H.T. & Tumlinson, J.H. (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393, 570–573.Google Scholar
De Moraes, C.M., Mescher, M.C. & Tumlinson, J.H. (2001) Caterpillar induced nocturnal plant volatiles repel conspecific females. Nature 40, 577–580.Google Scholar
Dicke, M. (1994) Local and systemic production of volatile herbivore-induced terpenoids – their role in plant-carnivore mutualism. Journal of Plant Physiology 143, 465–472.Google Scholar
Dicke, M. (1999) Are herbivore-induced plant volatiles reliable indicators of herbivore identity to foraging carnivorous arthropods? Entomologia Experimentalis et Applicata 91, 131–142.Google Scholar
Dicke, M. & Van Loon, J.J.A. (2000) Multitrophic effects of herbivore-induced plant volatile in an evolutionary context. Entomologia Experimentalis et Applicata 97, 237–249.Google Scholar
Dudareva, N., Negre, F., Nagegowda, D.A. & Orlova, I. (2009) Plant volatiles: recent advances and future perspectives Critical. Reviews in Plant Sciences 25, 417–440.CrossRefGoogle Scholar
Frati, F., Salerno, G., Conti, E. & Bin, F. (2008) Role of the plant – conspecific complex in host location and intra-specific communication of Lygus rugulipennis . Physiological Entomology 33, 129–137.Google Scholar
Fürstenberg-Hägg, J., Zagrobelny, M. & Bak, S. (2013) Plant defense against insect herbivores. International Journal of Molecular Sciences 14, 10242–10297.Google Scholar
Gomi, K., Satoh, M., Ozawa, R., Shinonaga, Y., Sanada, S., Sasaki, K., Matsumura, M., Ohashi, Y., Kanno, H., Akimitsu, K. & Takabayashi, J. (2010) Role of hydroperoxide lyase in white-backed planthopper (Sogatella furcifera Horváth)-induced resistance to bacterial blight in rice, Oryza sativa L. Plant Journal 61, 46–57.Google Scholar
Halitschke, R., Stenberg, J.A., Kessler, D., Kessler, A. & Baldwin, I.T. (2008) Shared signals – ‘alarm calls’ from plants increase apparency to herbivores and their enemies in nature. Ecology Letters 11, 24–34.CrossRefGoogle ScholarPubMed
Hare, J.D. (2011) Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annual Review of Entomology 56, 161–180.Google Scholar
Heil, M. (2010) Plastic defence expression in plants. Ecology and Evolution 24, 555–569.Google Scholar
Heil, M. & Ton, J. (2008) Long-distance signalling in plant defence. Trends in Plant Science 13, 264–272.Google Scholar
Hilker, M. & Meiners, T. (2010) How do plants ‘notice’ attack by herbivorous arthropods? Biological Reviews 85, 267–280.Google Scholar
Hoballah, M.E.F. & Turlings, T.C.J. (2001) Experimental evidence that plants under caterpillar attack may benefit from attracting parasitoids. Evolutionary Ecology Research 3, 553–565.Google Scholar
Howe, G.A. & Jander, G. (2008) Plant immunity to insect herbivores. Annual Review of Plant Biology 59, 41–66.Google Scholar
Hu, Z., Shen, Y., Shen, F., Luo, Y. & Su, X. (2009) Evidence for the signaling role of methyl jasmonate, methyl salicylate and benzothiazole between poplar (Populus simonii X P. pyramidalis ‘Opera 8277’) cuttings. Trees 23, 1003–1011.Google Scholar
James, D.G. (2003) Field evaluation of herbivore-induced plant volatiles as attractants for beneficial insects: methyl salicylate and the green lacewing, Chrysopa nigricornis . Journal of Chemical Ecology 29, 1601–1609.Google Scholar
James, D.G. (2005) Further field evaluation of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. Journal of Chemical Ecology 31, 481–495.CrossRefGoogle ScholarPubMed
Kaplan, I. (2012) Attracting carnivorous arthropods with plant volatiles: the future of biocontrol or playing with fire? Biological Control 60, 77–89.CrossRefGoogle Scholar
Kessler, A. & Baldwin, I.T. (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 2141–2144.Google Scholar
Kessler, A. & Baldwin, I.T. (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annual Review of Plant Biology 53, 299–328.Google Scholar
Kessler, A., Halitschke, R. & Baldwin, I.T. (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 35, 665–668.Google Scholar
Laumann, R.A., Aquino, M.F.S., Moraes, M.C.B., Pareja, M. & Borges, M. (2009) Response to egg parasitoids Trissolus basalis and Telenomus podisi to compounds from defensive secretions of stink bugs. Journal of Chemical Ecology 35, 8–19.Google Scholar
Laumann, R.A., Cokl, A., Lopes, A.P.S., Ferreira, J.B.C., Moraes, M.C.B. & Borges, M. (2011) Silent singers are not safe: selective response of a parasitoid to substrate-borne vibratory signals of stink bugs. Animal Behaviour 82, 1175–1183.Google Scholar
Lin, C., Shen, B., Xu, Z., Köllner, T.G., Degenhard, J. & Dooner, H. (2008) Characterization of monoterpene synthase gene tps 26, the ortholog of a gene induced by insect herbivory in maize. Plant Physiology 146, 940–951.Google Scholar
Loch, A.D. (2000) Abundance, distribution, and availability of Trissolcus basalis (Wollaston) (Hymenoptera: Scelionidae) hosts in a soybean agricultural system in southeastern Queensland. Biological Control 18, 120–135.Google Scholar
Lopes, A.P.S., Diniz, I.R., Moraes, M.C.B., Borges, M. & Laumann, R.A. (2012) Defesas induzidas por herbivoria e interações específicas no sistema tritrófico soja-percevejos-parasitoides de ovos. Pesquisa Agropecuária Brasileira 47, 875–878.CrossRefGoogle Scholar
Maciel, A.A.S., Lemos, R.N.S., Souza, J.R., Costa, V.A., Barrigossi, J.A.F. & Chagas, E.F. (2007) Parasitismo de ovos de Tibraca limbativentris Stal (Hemiptera: Pentatomidae) na cultura do arroz no Maranhão. Neotropical Entomology 36, 616–618.Google Scholar
Martins, J.F.S., Barrigossi, J.A.F., Oliveira, J.V. & Cunha, U.S. (2009) Situação do manejo integrado de insetos-praga na cultura do arroz no Brasil. Pelotas, Embrapa Clima Temperado. (Documentos, 290).Google Scholar
Mazid, M., Khan, T.A. & Mohammad, F. (2011) Role of secondary metabolites in defence mechanisms of plants. Biology and Medicine 3, 232–249.Google Scholar
Meiners, T. & Hilker, M. (1997) Host location in Oomyzus gallerucae (Hymenoptera: Eulophidae), an egg parasitoid of the elm leaf beetle Xanthogaleruca luteola (Coleoptera: Chrysomelidae). Oecologia 112, 87–93.Google Scholar
Meiners, T. & Hilker, M. (2000) Induction of plant synomones by oviposition of a phytophagus insect. Journal of Chemical Ecology 26, 221–232.Google Scholar
Metcalf, R.L. & Metcalf, E.R. (1992) Plant Kairomones in Insect Ecology and Control. New York, Chapman & Hall.Google Scholar
Michereff, M.F.F., Laumann, R.A., Borges, M., Michereff-Filho, M., Diniz, I.R., Neto, A.L.F. & Moraes, M.C.B. (2011) Volatiles mediating a plant-herbivore-natural enemy interaction in resistant and susceptible soybean cultivars. Journal of Chemical Ecology 37, 273–285.Google Scholar
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. Journal of Applied Entomology 131, 326–332.Google Scholar
Moraes, M.C.B., Laumann, R., Sujii, E.R., Pires, C. & Borges, M. (2005) Induced volatiles in soybean and pigeon pea plants artificially infested with the neotropical brow stink bug, Euschistus heros, and their effect on the egg parasitoid, Telenomus podisi . Entomologia Experimentalis et Applicata 115, 227–237.Google Scholar
Moraes, M.C.B., Birkett, M.A., Gordon-Weeks, R., Smart, L.E., Martin, J.L., Pye, B.J., Bromilow, R. & Pickett, J.A. (2008 a) Cis-Jasmone induces accumulation of defence compounds in wheat, Triticum aestivum . Phytochemistry 69, 9–17.Google Scholar
Moraes, M.C.B., Pareja, M. & Laumann, R.A. & Borges, M. (2008 b) The chemical volatiles (Semiochemicals) produced by neotropical stink bugs (Hemiptera: Pentatomidae). Neotropical Entomology 37, 489–505.Google Scholar
Moraes, M.C.B., Laumann, R.A., Pareja, M., Sereno, F.T.P.S., Michereff, M.F.F., Birkett, M.A., Pickett, J.A. & Borges, M. (2009) Attraction of the stink bug egg parasitoid Telenomus podisi to defence signals from soybean activated by treatment with cis-jasmone. Entomologia Experimentalis et Applicata 131, 178–188.Google Scholar
Oliveira, M.W.M., Borges, M., Andrade, C.K.Z., Laumann, R.A., José Barrigossi, J.A.F., Blassioli-Moraes, M.C. (2013) Zingiberenol, (1S,4R,1′S)-4-(1′,5′-Dimethylhex-4′-enyl)-1-methylcyclohex-2-en-1-ol, identified as the sex pheromone produced by males of the rice stink bug Oebalus poecilus (Heteroptera: Pentatomidae). Journal of Agricultural and Food Chemistry 61, 7777–7785.Google Scholar
Price, P.W., Bouton, C., 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. Annual review of Ecology and Systematics 11, 41–65.Google Scholar
R Development Core Team (2012) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Rasmann, S. & Turlings, T.C.J. (2008) First insights into specificity of belowground tritrophic interactions. Oikos 117, 362–369.Google Scholar
Riffel, C.T., Prando, H.F. & Boff, M.I.C. (2010) First record of Telenomus podisi (Ashmead) and Trissolcus urichi (Crawford) (Hymenoptera: Scelionidae) parasitizing eggs of the rice stern bug, Tibraca limbativentris (Stal) (Hemiptera: Pentatomidae), in Santa Catarina, Brazil. Neotropical Entomology 39, 447–448.Google Scholar
Rodriguez-Saona, C., Crafts-Brandner, S.J., Williams, L. & Paré, P.W. (2002) Lygus hesperus feeding and salivary gland extracts induce volatile emissions in plants . Journal of Chemical Ecology 28, 1733–1747.Google Scholar
Scutareanu, P., Bruin, J., Posthumus, M.A. & Drukker, B. (2003) Constitutive and herbivore-induced volatiles in pear, alder and hawthorn trees. Chemoecology 13, 63–74.Google Scholar
SOSBAI, Sociedade Sul-Brasileira de Arroz Irrigado (2012) Arroz Irrigado: Recomendações técnicas da pesquisa para o Sul do Brasil. Porto Alegre, Sosbai.Google Scholar
Sun, X.L., Wang, G.C., Gao, Y. & Chen, Z.M. (2012) Screening and field evaluation of synthetic volatile blends attractive to adults of the tea weevil, Myllocerinus aurolineatus . Chemoecology 22, 229–237.Google Scholar
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.Google Scholar
Turlings, T.C.J., Lengwiler, U.B., Bernasconi, M.L. & Wechsler, D. (1998) Timing of induced volatile emissions in maize seedlings. Planta 207, 146–152.Google Scholar
Vet, L.E.M. & Dicke, M. (1992) Ecology infochemical use by natural enemies in a tritrophic context. Annual review of Entomology 37, 141–72.Google Scholar
Vinson, S.B. (1984) Parasitoid-host relationship: chemical ecology of insects. pp. 205–233 in Bell, W.J. & Cardé, R.T. (Eds) The Chemical Ecology of Insects. New York: Chapman & Hall.Google Scholar
Vinson, S.B. (1985) The behaviour of parasitoids, pp. 417–469 in Kerkut, E.A. & Gilbert, L.I. (Eds.), Comprehensive insect physiology, biochemistry and pharmacology. New York, Pergamon Press.Google Scholar
Yan, Z.G. & Wang, C.Z. (2006) Identification of Mythmna separata-induced maize volatile synomones that attract the parasitoid Campoletis chlorideae. Journal of Applied Entomology 130, 213–219.CrossRefGoogle Scholar
Williams, L., Blackmer, J.L., Rodriguez-Saona, C. & Zhu, S. (2010) Plant volatiles influence electrophysiological and behavioral responses of Lygus hesperus . Journal of Chemical Ecology 36, 467–478.CrossRefGoogle ScholarPubMed
Zhang, Q.H., Ma, J.H., Yang, Q.Q., Byers, J.A., Klein, M.G., Zhao, F.Y. & Luo, Y.Q. (2011) Olfactory and visual responses of the long-legged chafer Hoplia spectabilis Medvedev (Coleoptera: Scarabaeidae) in Qinghai Province, China. Pest Management Science 67, 162–169.Google Scholar