Artículos de revistas
Attraction Of A Ladybird To Sweet Pepper Damaged By Two Aphid Species Simultaneously Or Sequentially
Registro en:
Arthropod-plant Interactions. Kluwer Academic Publishers, v. 8, n. 6, p. 547 - 555, 2014.
18728855
10.1007/s11829-014-9336-x
2-s2.0-84922088189
Autor
Oliveira M.S.
Pareja M.
Institución
Resumen
Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Natural enemies of insect herbivores use volatile organic compounds (VOCs) released by plants to locate suitable patches for foraging. When a plant is damaged by herbivores, it can modify its VOC profile, enhancing attraction of the herbivore’s natural enemies. In both natural and agricultural ecosystems, plants are usually attacked by more than one species of herbivore, either simultaneously or sequentially. Different herbivores, even those with similar feeding habits, can activate different defensive responses in the same plant and this can alter the attraction of natural enemies. This study aimed to understand how simultaneous and sequential damage to sweet pepper, Capsicum annuum, by two aphid species, Aphis gossypii and Myzus persicae, affects attraction of the aphid predator Cycloneda sanguinea to plant odours. Undamaged plants did not attract C. sanguinea, but plants damaged by either aphid were attractive to this predator. When plants were damaged simultaneously, the predator did not distinguish between the odours of plants damaged by both species from those damaged by a single species. When damage was sequential, a certain combination of damage (A. gossypii followed by M. persicae) made the plants more attractive than plants damaged by A. gossypii only. Odour from plants from all other combinations of sequential damage proved equally attractive to C. sanguinea as plants damaged by a single species. The study allows us to conclude that, unlike for simultaneous damage, a specific sequence of sequential damage enhances attraction of the predator. This could potentially create enemy-dense space on previously damaged plants. 8 6 547 555 562307/2010-9; CAPES; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior; CNPq; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) Agbogba, B.C., Powell, W., Effect of the presence of a non-host herbivore on the response of the aphid parasitoid Diaeretiella rapae to host-infested cabbage plants (2007) J Chem Ecol, 33, pp. 2229-2235. , COI: 1:CAS:528:DC%2BD2sXhtl2ks7rP, PID: 17968626 Alborn, H.T., Turlings, T.C.J., Jones, T.H., Stenhagen, G., Loughrin, J.H., Tumlinson, J.H., An elicitor of plant volatiles from beet armyworm oral secretion (1997) Science, 276, pp. 945-948. , COI: 1:CAS:528:DyaK2sXjt1agsbg%3D Almeida, L.M., Ribeiro-Costa, C.S., Coleopteros predadores (Coccinellidae) (2009) Bioecologia e Nutrição de Insetos: Base para o Manejo Integrado de Pragas, pp. 931-968. , Panizzi AR, Parra JRP, (eds), Embrapa Informação Tecnológica, Brasília: Bernasconi, M.L., Turlings, T.C.J., Ambrosetti, L., Bassetti, P., Dorn, S., Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis (1998) Entomol Exp Appl, 87, pp. 133-142. , COI: 1:CAS:528:DyaK1cXks1Wqtro%3D Bostock, R.M., Signal crosstalk and induced resistance: straddling the line between cost and benefit (2005) Annu Rev Phytopathol, 43, pp. 545-580. , COI: 1:CAS:528:DC%2BD2MXhtVOksrjO, PID: 16078895 Bruce, T.J.A., Pickett, J.A., Perception of plant volatile blends by herbivorous insects—Finding the right mix (2011) Phytochemistry, 72, pp. 1605-1611. , COI: 1:CAS:528:DC%2BC3MXptlWrsbw%3D, PID: 21596403 Bukovinszky, T., Poelman, E.H., Kamp, A., Hemerik, L., Prekatsakis, G., Dicke, M., Plants under multiple herbivory: consequences for parasitoid search behaviour and foraging efficiency (2012) Anim Behav, 83, pp. 501-509 de Boer, J.G., Posthumus, M.A., Dicke, M., Identification of volatiles that are used in discrimination between plants infested with prey or non-prey herbivores by a predatory mite (2004) J Chem Ecol, 30, pp. 2215-2230. , PID: 15672666 de Boer, J.G., Snoeren, T.A.L., Dicke, M., Predatory mites learn to discriminate between plant volatiles induced by prey and non-prey herbivores (2005) Anim Behav, 69, pp. 869-879 de Boer, J.G., Hordijk, C.A., Posthumus, M.A., Dicke, M., Prey and non-prey arthropods sharing a host plant: effects on induced volatile emission and predator attraction (2008) J Chem Ecol, 34, pp. 281-290. , PID: 18185960 De Moraes, C.M., Lewis, W.J., Paré, P.W., Alborn, H.T., Tumlinson, J.H., Herbivore-infested plants selectively attract parasitoids (1998) Nature, 393, pp. 570-573 De Moraes, C.M., Mescher, M.C., Tumlinson, J.H., Caterpillar-induced nocturnal plant volatiles repel conspecific females (2001) Nature, 410, pp. 577-580. , PID: 11279494 de Rijk, M., Dicke, M., Poelman, E.H., Foraging behaviour by parasitoids in multiherbivore communities (2013) Anim Behav, 85, pp. 1517-1528 Du, Y.-J., Poppy, G.M., Powell, W., Relative importance of semiochemicals from first and second trophic levels in host foraging behavior of Aphidius ervi (1996) J Chem Ecol, 22, pp. 1591-1605. , COI: 1:CAS:528:DyaK28Xmt1Snsrc%3D, PID: 24226473 Du, Y.-J., Poppy, G.M., Powell, W., Pickett, J.A., Wadhams, L.J., Woodcock, C.M., Identification of semiochemicals released during aphid feeding that attract the parasitoid Aphidius ervi (1998) J Chem Ecol, 24, pp. 1355-1368. , COI: 1:CAS:528:DyaK1cXlt1equ7g%3D Erb, M., Foresti, N., Turlings, T.C.J., A tritrophic signal that attracts parasitoids to host-damaged plants withstands disruption by non-host herbivores (2010) BMC Plant Biology, p. 10 Gencer, N.S., Kumral, N.A., Sivritepe, H.O., Seidi, M., Susurluk, H., Senturk, B., Olfactory response of the ladybird beetle Stethorus gilvifrons to two preys and herbivore-induced plant volatiles (2009) Phytoparasitica, 37, pp. 217-224 Han, B.Y., Chen, Z.M., Behavioral and electrophysiological responses of natural enemies to synomones from tea shoots and kairomones from tea aphids, Toxoptera aurantii (2002) J Chem Ecol, 28, pp. 2203-2219. , COI: 1:CAS:528:DC%2BD38Xos1KntbY%3D, PID: 12523563 Hare, J.D., Ecological role of volatiles produced by plants in response to damage by herbivorous insects (2011) Annu Rev Entomol, 56, pp. 161-180. , COI: 1:CAS:528:DC%2BC3MXhtlSiu7s%3D, PID: 21133760 Hare, J.D., Sun, J.J., Production of induced volatiles by Datura wrightii in response to damage by insects: effect of herbivore species and time (2011) J Chem Ecol, 37, pp. 751-764. , COI: 1:CAS:528:DC%2BC3MXotFClsrs%3D, PID: 21691808 Hatano, E., Kunert, G., Michaud, J.P., Weisser, W.W., Chemical cues mediating aphid location by natural enemies (2008) Eur J Entomol, 105, pp. 797-806. , COI: 1:CAS:528:DC%2BD1MXivVGmsro%3D Heil, M., Indirect defence via tritrophic interactions (2008) New Phytol, 178, pp. 41-61. , COI: 1:CAS:528:DC%2BD1cXks1SmtL4%3D, PID: 18086230 Hoballah, M.E., Turlings, T.C.J., The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles (2005) J Chem Ecol, 31, pp. 2003-2018. , COI: 1:CAS:528:DC%2BD2MXptVWltLg%3D, PID: 16132209 BioControl, , Lins Jr. JC, Loon JJAv, Bueno VHP, Lucas-Barbosa D, Dicke M, Lenteren JCv (In Press) Response of the zoophytophagous predators Macrolophus pygmaeus and Nesidiocoris tenuis to volatiles of uninfested plants and to plants infested by prey or conspecifics Kessler, A., Baldwin, I.T., Defensive function of herbivore-induced plant volatile emissions in nature (2001) Science, 291, pp. 2141-2144. , COI: 1:CAS:528:DC%2BD3MXitFCltr0%3D, PID: 11251117 Kessler, A., Halitschke, R., Specificity and complexity: the impact of herbivore-induced plant responses on arthropod community structure (2007) Curr Opin Plant Biol, 10, pp. 409-414. , COI: 1:CAS:528:DC%2BD2sXosFGrsbk%3D, PID: 17652009 Martínez, A.S., Hardie, J., Hygroreception in olfactometer studies (2009) Physiol Entomol, 34, pp. 211-216 Mattiacci, L., Dicke, M., Posthumus, M.A., Glucosidase: an elicitor of herbivore-induced plant odor that attracts host-searching parasitic wasps (1995) Proc Natl Acad Sci USA, 92, pp. 2036-2040. , COI: 1:CAS:528:DyaK2MXksVCqsbo%3D, PID: 11607516 Moayeri, H.R.S., Ashouri, A., Poll, L., Enkegaard, A., Olfactory response of a predatory mirid to herbivore induced plant volatiles: multiple herbivory vs. single herbivory (2007) J Appl Entomol, 131, pp. 326-332. , COI: 1:CAS:528:DC%2BD2sXot12ktr8%3D Moraes, M.C.B., Laumann, R., Sujii, E.R., Pires, C., Borges, M., Induced volatiles in soybean and pigeon pea plants artificially infested with the neotropical brown stink bug, Euschistus heros, and their effect on the egg parasitoid, Telenomus podisi (2005) Entomol Exp Appl, 115, pp. 227-237. , COI: 1:CAS:528:DC%2BD2MXkvFOku74%3D Moran, P.J., Thompson, G.A., Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways (2001) Plant Physiol, 125, pp. 1074-1085. , COI: 1:CAS:528:DC%2BD3MXhs1Klt7Y%3D, PID: 11161062 Musser, R.O., Mum-Musser, S.M., Eichenseer, H., Peiffer, M., Ervin, G., Murphy, J.B., Felton, G.W., Caterpillar saliva beats plant defences (2002) Nature, 416, pp. 599-600. , COI: 1:CAS:528:DC%2BD38XjtFahsbs%3D, PID: 11948341 Ninkovic, V., Al Abassi, S., Pettersson, J., The influence of aphid-induced plant volatiles on ladybird beetle searching behavior (2001) Biol Control, 21, pp. 191-195 Pareja, M., Mohib, A., Birkett, M.A., Dufour, S., Glinwood, R.T., Multivariate statistics coupled to generalized linear models reveal complex use of chemical cues by a parasitoid (2009) Anim Behav, 77, pp. 901-909 Pareja, M., Qvarfordt, E., Webster, B., Mayon, P., Pickett, J., Birkett, M., Glinwood, R., Herbivory by a phloem-feeding insect inhibits floral volatile production (2012) PLoS One, 7, p. e31971. , COI: 1:CAS:528:DC%2BC38XjsVyjurs%3D, PID: 22384116 Pettersson, J., Ninkovic, V., Glinwood, R., Abassi, S.A., Birkett, M., Pickett, J., Wadhams, L., Chemical stimuli supporting foraging behaviour of Coccinella septempunctata L. (Coleoptera: coccinellidae): volatiles and allelobiosis (2008) Appl Entomol Zool, 43, pp. 315-321 Reddy, G.V.P., Plant volatiles mediate orientation and plant preference by the predator Chrysoperla carnea Stephens (Neuroptera: Chrysopidae) (2002) Biol Control, 25, pp. 49-55. , COI: 1:CAS:528:DC%2BD38Xntlyqurw%3D Rodríguez-Saona, C., Chalmers, J.A., Raj, S., Thaler, J.S., Induced plant responses to multiple damagers: differential effects on an herbivore and its parasitoid (2005) Oecologia, 143, pp. 566-577. , PID: 15791425 Sarmento, R.A., Venzon, M., Pallini, A., Oliveira, E.E., Janssen, A., Use of odours by Cycloneda sanguinea to assess patch quality (2007) Entomol Exp Appl, 124, pp. 313-318 Sarmento, R.A., Fd, L., Dias, C.R., Pallini, A., Venzon, M., Infoquímicos induzidos por herbivoria mediando a comunicação entre plantas de tomate e o predador Cycloneda sanguinea (Coleoptera: Coccinellidae) (2008) Ceres, 55, pp. 439-444 Sarmento, R.A., A herbivore that manipulates plant defence (2011) Ecol Lett, 14, pp. 229-236. , PID: 21299823 Schwartzberg, E.G., Boroczky, K., Tumlinson, J.H., Pea aphids, Acyrthosiphon pisum, suppress induced plant volatiles in broad bean, Vicia faba (2011) J Chem Ecol, 37, pp. 1055-1062. , COI: 1:CAS:528:DC%2BC3MXhtlGisbbM, PID: 21870158 Shiojiri, K., Takabayashi, J., Yano, S., Takafuji, A., Flight response of parasitoids toward plant-herbivore complexes: a comparative study of two parasitoid-herbivore systems on cabbage plants (2000) Appl Entomol Zool, 35, pp. 87-92 Shiojiri, K., Takabayashi, J., Yano, S., Takafuji, A., Infochemically mediated tritrophic interaction webs on cabbage plants (2001) Popul Ecol, 43, pp. 23-29 Soler, R., Bezemer, T.M., Cortesero, A.M., Van der Putten, W.H., Vet, L.E.M., Harvey, J.A., Impact of foliar herbivory on the development of a root-feeding insect and its parasitoid (2007) Oecologia, 152, pp. 257-264. , PID: 17334787 Soler, R., Root herbivores influence the behaviour of an aboveground parasitoid through changes in plant-volatile signals (2007) Oikos, 116, pp. 367-376. , COI: 1:CAS:528:DC%2BD2sXkvFWmsL4%3D Soler, R., Badenes-Perez, F.R., Broekgaarden, C., Zheng, S.J., David, A., Boland, W., Dicke, M., Plant-mediated facilitation between a leaf-feeding and a phloem-feeding insect in a brassicaceous plant: from insect performance to gene transcription (2012) Funct Ecol, 26, pp. 156-166 Steidle, J.L.M., van Loon, J.J.A., Dietary specialization and infochemical use in carnivorous arthropods: testing a concept (2003) Entomol Exp Appl, 108, pp. 133-148 Turlings, T.C.J., Tumlinson, J.H., Lewis, W.J., Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps (1990) Science, 250, pp. 1251-1253. , COI: 1:CAS:528:DyaK3MXpvVKktA%3D%3D, PID: 17829213 van Poecke, R.M.P., Roosjen, M., Pumarino, L., Dicke, M., Attraction of the specialist parasitoid Cotesia rubecula to Arabidopsis thaliana infested by host or non-host herbivore species (2003) Entomol Exp Appl, 107, pp. 229-236 Vet, L.E.M., Dicke, M., Ecology of infochemical use by natural enemies in a tritophic context (1992) Annu Rev Entomol, 37, pp. 141-172 Zarate, S.I., Kempema, L.A., Walling, L.L., Silverleaf whitefly induces salicylic acid defenses and suppresses effectual jasmonic acid defenses (2007) Plant Physiol, 143, pp. 866-875. , COI: 1:CAS:528:DC%2BD2sXhvFWntrs%3D, PID: 17189328 Zhang, P.-J., Zheng, S.-J., van Loon, J.J.A., Boland, W., David, A., Mumm, R., Dicke, M., Whiteflies interfere with indirect plant defense against spider mites in Lima bean (2009) Proc Natl Acad Sci USA, 106, pp. 21202-21207. , COI: 1:CAS:528:DC%2BC3cXjvFOhsr0%3D, PID: 19965373 Zhang, P.J., Broekgaarden, C., Zheng, S.J., Snoeren, T.A.L., van Loon, J.J.A., Gols, R., Dicke, M., Jasmonate and ethylene signaling mediate whitefly-induced interference with indirect plant defense in Arabidopsis thaliana (2013) New Phytol, 197, pp. 1291-1299. , COI: 1:CAS:528:DC%2BC3sXitVOju7w%3D, PID: 23311965