Abstract
The polyphagous planthopper Hyalesthes obsoletus Signoret is considered to be the principal vector of stolbur phytoplasma, which is associated with yellow diseases of grapevine. To explore the possibility of developing novel control strategies, the behavioral responses to six synthetic mixtures and nine single compounds, previously identified from the headspace of Vitex agnus-castus L. (chaste tree) and Urtica dioica L. (nettle), were investigated in Y-tube bioassays. Choice tests revealed differences in the behavioral responses of males and females to the volatiles that they were exposed to. Males were attracted to a mixture containing (E)-β-caryophyllene, 1,8-cineole, (E,E)-α-farnesene, (E)-β-farnesene, and methyl salicylate (mixture 2). The addition of methyl benzoate to this five-compound mixture (mixture 3) did not attract males but elicited positive responses in females. Furthermore, females were attracted to a mixture containing (E)-β-caryophyllene, (E,E)-α-farnesene, (Z)-3-hexenyl acetate, (Z)-3-hexen-1-ol, and benzothiazole (mixture 4), but here addition of methyl salicylate (mixture 5) did not attract females. Neither males nor females showed attractivity or repellency toward the singly tested compounds. This study enhances knowledge on the interaction of insect behaviorally effective constituents in complex plant volatile mixtures. The attractive mixtures of plant volatiles identified suggest the possibility of using them in monitoring and management of H. obsoletus.
Similar content being viewed by others
References
Arimura GI, Kost C, Boland W (2005) Herbivore-induced, indirect plant defences. Biochim Biophys Acta 1734:91–111
Belli G, Bianco PA, Conti M (2010) Grapevine yellows: past, present and future. J Plant Pathol 92:303–326
Bernays EA (2001) Neural limitations in phytophagous insects: implications for diet breadth and evolution of host affiliation. Annu Rev Entomol 46:703–727
Blande JD, Korjus M, Holopainen JK (2010) Foliar methyl salicylate emissions indicate prolonged aphid infestation on silver birch and black alder. Tree Physiol 30:404–416
Bressan A, Turata R, Maixner M, Spiazzi S, Boudon-Padieu E, Girolami V (2007) Vector activity of Hyalesthes obsoletus living on nettles and transmitting a stolbur phytoplasma to grapevines: a case study. Ann Appl Biol 150:331–339
Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects—finding the right mix. Phytochemistry 72:1605–1611
Dudareva N, Pichersky E, Gershenzon J (2004) Biochemistry of plant volatiles. Plant Physiol 135:1893–1902
Eben A, Gross J (2013) Innovative control of psyllid vectors of European fruit tree phytoplasmas. Phytopathog Moll 3:37–39
Gripenberg S, Mayhew PJ, Parnell M, Roslin T (2010) A meta-analysis of preference–performance relationships in phytophagous insects. Ecol Lett 13:383–393
Hoch H, Remane R (1985) Evolution und speziation der zikaden-gattung Hyalesthes Sign., 1865 (Hom. Auch. Fulgoroidea Cixiidae). Marburger Entomol Publ 2:1–427
Hoy CW, Zhou X, Nault LR, Miller SA, Styrer J (1999) Host plant, phytoplasma, and reproductive status effects on flight behaviour of aster leafhopper (Homoptera: Cicadellidae). Ann Entomol Soc Am 92:523–528
Ingwell LL, Eigenbrode SD, Bosque-Pérez NA (2012) Plant viruses alter insect behavior to enhance their spread. Sci Rep 2:578
Jansen RMC, Wildt J, Kappers IF, Bouwmeester HJ, Hofstee JW, Van Henten EJ (2011) Detection of diseased plants by analysis of volatile organic compound emission. Annu Rev Phytopathol 49:157–174
Johannesen J, Lux B, Michel K, Seitz A, Maixner M (2008) Invasion biology and host specificity of the grapevine yellows disease vector Hyalesthes obsoletus in Europe. Entomol Exp Appl 126:217–227
Kessler S, Schaerer S, Delabays N, Turlings TC, Trivellone V, Kehrli P (2011) Host plant preferences of Hyalesthes obsoletus, the vector of the grapevine yellows disease ‘Bois noir’, in Switzerland. Entomol Exp Appl 139:60–67
Knight AL, Light DM (2005) Seasonal flight patterns of codling moth (Lepidoptera: Tortricidae) monitored with pear ester and codlemone-baited traps in sex pheromone-treated apple orchards. Environ Entomol 34:1028–1035
Knudsen JT, Eriksson R, Gershenzon J, Ståhl B (2006) Diversity and distribution of floral scent. Bot Rev 72:1–120
Kosovac A, Radonjić S, Hrnčić S, Krstić O, Toševski I, Jović J (2015) Molecular tracing of the transmission routes of bois noir in Mediterranean vineyards of Montenegro and experimental evidence for the epidemiological role of Vitex agnus-castus (Lamiaceae) and associated Hyalesthes obsoletus (Cixiidae). Plant Pathol. doi:10.1111/ppa.12409
Landi L, Isidoro N, Riolo P (2013) Natural phytoplasma infection of four phloem-feeding Auchenorrhyncha across vineyard agroecosystems in central-Eastern Italy. J Econ Entomol 106:604–613
Landi L, Riolo P, Murolo S, Romanazzi G, Nardi S, Isidoro N (2015) Genetic variability of stolbur phytoplasma in Hyalesthes obsoletus (Hemiptera: Cixiidae) and its main host plants in vineyard agroecosystems. J Econ Entomol 108:1506–1515
Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166
Maixner M (2010) Phytoplasma epidemiological systems with multiple plant hosts. In: Weintraub PJ, Jones P (eds) Phytoplasmas: genomes, plant hosts and vectors. CABI International, Wallingford, pp 213–232
Maixner M (2011) Recent advances in Bois noir research. Petria 21:95–108
Maixner M, Ahrens U, Seemüller E (1994) Detection of mycoplasmalike organisms associated with a yellows disease of grapevine in Germany. J Phytopathol 142:1–10
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:e1002610
Martel JW, Alford AR, Dickens JC (2005) Synthetic host volatiles increase efficacy of trap cropping for management of Colorado potato beetle, Leptinotarsa decemlineata (Say). Agric For Entomol 7:79–86
Martini X, Kuhns EH, Hoyte A, Stelinski LL (2014) Plant volatiles and density-dependent conspecific female odors are used by Asian citrus psyllid to evaluate host suitability on a spatial scale. Arthropod Plant Interact 8:453–460
Martini X, Hoffmann M, Coy MR, Stelinski LL, Pelz-Stelinski KS (2015) Infection of an insect vector with a bacterial plant pathogen increases its propensity for dispersal. PLoS One 10(6):e0129373
Mazzoni V, Lucchi A, Ioriatti C, Virant-Doberlet M, Anfora G (2010) Mating behavior of Hyalesthes obsoletus (Hemiptera: Cixiidae). Ann Entomol Soc Am 103:813–822
Minuz RL, Isidoro N, Casavecchia S, Burgio G, Riolo P (2013) Sex-dispersal differences of four phloem-feeding vectors and their relationship to wild-plant abundance in vineyard agroecosystems. J Econ Entomol 106:2296–2309
Mori N, Quaglino F, Tessari F, Pozzebon A, Bulgari D, Casati P, Bianco PA (2015) Investigation on ‘bois noir’ epidemiology in north-eastern Italian vineyards through a multidisciplinary approach. Ann Appl Biol 166:75–89
Murolo S, Marcone C, Prota V, Garau R, Foissac X, Romanazzi G (2010) Genetic variability of the stolbur phytoplasma vmp1 gene in grapevines, bindweeds and vegetables. J Appl Microbiol 109:2049–2059
Oluwafemi S, Bruce TJA, Pickett JA, Ton J, Birkett MA (2011) Behavioral responses of the leafhopper, Cicadulina storeyi China, a major vector of maize streak virus, to volatile cues from intact and leafhopper-damaged maize. J Chem Ecol 37:40–48
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 77:901–909
Quaglino F, Zhao Y, Casati P, Bulgari D, Bianco PA, Wei W, Davis RE (2013) ‘Candidatus Phytoplasma solani’, a novel taxon associated with stolbur and bois noir related diseases of plants. Int J Syst Evol Microbiol 63:2879–2894
Riolo P, Landi L, Nardi S, Isidoro N (2007) Relationships among Hyalesthes obsoletus, its herbaceous host plants and “Bois noir” phytoplasma strains in vineyard ecosystems in the Marche region (central-eastern Italy). Bull Insectol 60:353–354
Riolo P, Minuz RL, Anfora G, Stacconi MVR, Carlin S, Isidoro N, Romani R (2012) Perception of host plant volatiles in Hyalesthes obsoletus: behavior, morphology, and electrophysiology. J Chem Ecol 38:1017–1030
Rodriguez-Saona CR, Stelinski LL (2009) Behavior-modifying strategies in IPM: theory and practice. In: Pimentel D (ed) Integrated pest management: innovation-development process. Springer, Amsterdam, pp 263–315
Sforza R, Boudon-Padieu E (1998) Le principal vecteur de la maladie du bois noir. Phytoma 510:33–37
Sforza R, Bourgoin T, Wilson SW, Boudon-Padieu E (1999) Field observations, laboratory rearing and descriptions of immatures of the planthopper Hyalesthes obsoletus (Hemiptera: Cixiidae). Eur J Entomol 96:409–418
Sharon R, Soroker V, Wesley SD, Zahavi T, Harari A, Weintraub PG (2005) Vitex agnus-castus is a preferred host plant for Hyalesthes obsoletus. J Chem Ecol 31:1051–1063
Szendrei Z, Rodriguez-Saona C (2010) A meta-analysis of insect pest behavioral manipulation with plant volatiles. Entomol Exp Appl 134:201–210
Vacas S, Melita O, Michaelakis A, Milonas P, Minuz RL, Riolo P, Abbass MK, Lo Bue P, Colazza S, Peri E, Soroker V, Livne Y, Primo J, Navarro-Llopis V (2016) Lures for red palm weevil trapping systems: aggregation pheromone and synthetic kairomone. Pest Manag Sci. doi:10.1002/ps.4289
Visser JH (1986) Host odor perception in phytophagous insects. Annu Rev Entomol 31:121–144
Weintraub PG, Beanland L (2006) Insect vectors of phytoplasmas. Annu Rev Entomol 51:91–111
Zahavi T, Sharon R, Sapir G, Mawassi M, Dafny-Yelin M, Naor V (2013) The long-term effect of stolbur phytoplasma on grapevines in the Golan Heights. Aust J Grape Wine Res 19:277–284
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle River
Zhao N, Guan J, Ferrer JL, Engle N, Chern M, Ronald P, Tschaplinski TJ, Chen F (2010) Biosynthesis and emission of insect-induced methyl salicylate and methyl benzoate from rice. Plant Physiol Biochem 48:279–287
Zhu JW, Park KC (2005) Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J Chem Ecol 31:1733–1746
Acknowledgements
This study was funded by the Italian Ministry of Education, Universities and Research (MIUR), Research Project of National Interest (PRIN) ‘Mechanisms of host-plant location and host-plant preferences in two leafhoppers (Hemiptera: Auchenorrhyncha), vectors of grapevine yellow diseases’. Comments and suggestions made by three anonymous reviewers have helped us to improve the manuscript.
Authors’ contribution
PR and RLM conceived and designed the experiments. PR, RLM, and EP performed the experiments. PR, RLM, EP, and NI analyzed the results. PR contributed reagents/materials/analysis tools. PR, RLM, EP, and NI wrote the manuscript.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Handling Editor: Jarmo Holopainen.
Rights and permissions
About this article
Cite this article
Riolo, P., Minuz, R.L., Peri, E. et al. Behavioral responses of Hyalesthes obsoletus to host-plant volatiles cues. Arthropod-Plant Interactions 11, 71–78 (2017). https://doi.org/10.1007/s11829-016-9467-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11829-016-9467-3