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Behavioral Responses of Hyalesthes Obsoletus to Host-Plant Volatiles Cues

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Behavioral Responses of Hyalesthes Obsoletus to Host-Plant Volatiles Cues Arthropod-Plant Interactions (2017) 11:71–78 DOI 10.1007/s11829-016-9467-3 ORIGINAL PAPER Behavioral responses of Hyalesthes obsoletus to host-plant volatiles cues 1 1 2 1 Paola Riolo • Roxana L. Minuz • Ezio Peri • Nunzio Isidoro Received: 6 May 2016 / Accepted: 7 October 2016 / Published online: 25 November 2016 Ó Springer Science+Business Media Dordrecht 2016 Abstract The polyphagous planthopper Hyalesthes obso- identified suggest the possibility of using them in moni- letus Signoret is considered to be the principal vector of toring and management of H. obsoletus. stolbur phytoplasma, which is associated with yellow dis- eases of grapevine. To explore the possibility of developing Keywords Phytoplasma vector Á Plant volatiles Á novel control strategies, the behavioral responses to six Semiochemical Á Y-tube olfactometer synthetic mixtures and nine single compounds, previously identified from the headspace of Vitex agnus-castus L. (chaste tree) and Urtica dioica L. (nettle), were investi- Introduction gated in Y-tube bioassays. Choice tests revealed differ- ences in the behavioral responses of males and females to Bois noir (BN) is a grapevine (Vitis vinifera L.) disease that the volatiles that they were exposed to. Males were is associated with ‘Candidatus Phytoplasma solani’ attracted to a mixture containing (E)-b-caryophyllene, 1,8- (16SrXII-A subgroup) (Quaglino et al. 2013). Infected cineole, (E,E)-a-farnesene, (E)-b-farnesene, and methyl grapevine symptoms include chlorosis and downward salicylate (mixture 2). The addition of methyl benzoate to rolling of leaves, stunted shoots, and shriveling of berries this five-compound mixture (mixture 3) did not attract (Belli et al. 2010). In recent years, rapid spreading of BN males but elicited positive responses in females. Further- has been seen frequently, and this can be a limiting factor more, females were attracted to a mixture containing (E)-b- in grapevine production (Maixner 2011; Zahavi et al. caryophyllene, (E,E)-a-farnesene, (Z)-3-hexenyl acetate, 2013). (Z)-3-hexen-1-ol, and benzothiazole (mixture 4), but here The epidemiology of vector-borne plant pathogens is addition of methyl salicylate (mixture 5) did not attract directly dependent on the insect vector species and its life females. Neither males nor females showed attractivity or strategy, which include its host-plant specificity, feeding repellency toward the singly tested compounds. This study preferences, dispersal capacity, and sex behavioral differ- enhances knowledge on the interaction of insect behav- ences (Hoy et al. 1999; Weintraub and Beanland 2006; iorally effective constituents in complex plant volatile Maixner 2010). mixtures. The attractive mixtures of plant volatiles The planthopper Hyalesthes obsoletus Signoret (Hemi- ptera: Cixiidae) is considered to be the principal vector of the BN causal agent in both southern and central European Handling Editor: Jarmo Holopainen. vineyards (Maixner et al. 1994; Sforza and Boudon-Padieu 1998). Postembryonic development occurs on the roots of & Paola Riolo host plants, on which the young stages feed and overwinter [email protected] (Sforza et al. 1999). Adults live above ground and transmit 1 Dipartimento di Scienze Agrarie, Alimentari ed Ambientali, the phytoplasma on healthy plants by feeding (Bressan Universita` Politecnica delle Marche, 60131 Ancona, Italy et al. 2007). 2 Dipartimento di Scienze Agrarie e Forestali, Universita` degli The occurrence and spread of BN are associated also Studi di Palermo, 90128 Palermo, Italy with the presence in the vineyard agroecosystem of wild 123 72 P. Riolo et al. vegetation that can host both the insect vector and the single compounds that can be used as cues by H. obsoletus. phytoplasma (Murolo et al. 2010; Landi et al. 2013, 2015; Such key mixtures or single compounds could be part of a Kosovac et al. 2015). Adults of H. obsoletus can feed on sustainable and environmentally friendly strategy to con- various plants, although only a few species are generally trol H. obsoletus adults in vineyard agroecosystems. selected to complete their whole life cycle (primary hosts). Its host-plant range is still under investigation, as it includes very different plant families and it changes Materials and methods depending on geographic area (Hoch and Remane 1985; Riolo et al. 2012, and references therein). Grapevines Insects represent only an occasional host plant for adults, whereby they can transmit the phytoplasma during their feeding Adults of H. obsoletus were collected from nettle plants in probing (Maixner 2010). the Ancona area (43°320 N; 13°230 E) of the Marche region The life history of H. obsoletus, its affiliation (prefer- in central-eastern Italy. The insects were transferred to the ence of adult for the plant species on which it developed) to laboratory, separated according to sex, and caged with wild host plants, and its erratic feeding behavior on fresh shoots of nettle. Twenty-four hours before the grapevine impede the effective control of this planthopper beginning of the bioassays, adult H. obsoletus were trans- (Maixner 2010). In H. obsoletus both sexes produce ferred to clean cages and fed with aqueous sucrose solution vibratory signals: the females have a major role in the (5% sucrose, 0.5 % sorbitol), to avoid any influence on the stimulation of the male search process, whereas the males compounds used in the subsequent experiments. The adults are more vibrationally active in the courtship and precopula were kept at 26 ± 1 °C and 60 ± 10 % relative humidity, stages. There is no evidence of the presence of sex pher- under a natural photoperiod (L16:D8). omones in this species (Mazzoni et al. 2010). Generally, synthetic herbicides and insecticides have Volatiles sources and experiments been proposed for the control of H. obsoletus on vineyard ground cover and the surrounding vegetation (Maixner Experiment 1 2010; Mori et al. 2015). Among possible alternatives to synthetic pesticides, the use of plant volatiles to manipulate This experiment was designed to determine the olfactory insect behavior has become a suitable tool for management responses of H. obsoletus males and females to relatively of a number of insect pests, including vectors of plant complex synthetic mixtures that contained 4–6 chaste tree- pathogens (Szendrei and Rodriguez-Saona 2010; Eben and derived compounds (Table 1, Mixtures 1–3) and 5–7 net- Gross 2013). Volatiles provide important cues for insects in tle-derived compounds (Table 1, Mixtures 4–6), versus a their search for host plants on which to feed or lay eggs and blank. The first mixtures evaluated included the major in the avoidance of plants that might be unsuitable as hosts antennally active volatiles (in terms of relative abundance) (Visser 1986; Szendrei and Rodriguez-Saona 2010). Also, of the chaste tree [i.e., 1,8-cineole, (E,E)-a-farnesene, (E)- volatile compounds in mixtures can act antagonistically, b-farnesene, (E)-b-caryophyllene] and nettle [i.e., (Z)-3- additively, or synergistically, depending on whether the hexenyl acetate, benzothiazole, (Z)-3-hexen-1-ol, (E,E)-a- insect response to a mixture of such volatiles is less than, farnesene, (E)-b-caryophyllene]. In the subsequent mix- equal to, or more intense than the sum of responses to the tures tested were added some antennally active compounds individual components, respectively (Bruce and Pickett that are present in small amounts in shoot blends from the 2011). natural chaste tree (i.e., methyl salicylate, methyl benzoate) In our previous studies, where the attractiveness to and nettle [i.e., methyl salicylate, (Z)-jasmone] (Riolo et al. H. obsoletus females and males of volatiles from nettle, 2012; Table 1). The aim of the mixtures was to mimic the field bindweed, hedge bindweed, chaste tree, and grapevine natural ratios of antennally active compounds emitted by was tested, we showed significant attraction of males to the shoots of chaste tree and nettle (Riolo et al. 2012; chaste tree volatiles, and of females to nettle volatiles. Table 1). For every mixture, a hexane ([99 % pure; Furthermore, volatiles from these two host plants were Sigma-Aldrich, Italy) stock solution was prepared at the collected and analyzed, and compounds that elicited elec- concentration of 10 lg/ll. The concentration specified trophysiological responses in planthopper antennae were refers to the most abundant compound, which was 1,8- identified (Riolo et al. 2012). cineole for mixtures 1–3, and (Z)-3-hexenyl acetate for Hence, the objective of the current study was to examine mixtures 4–6 (Riolo et al. 2012). The mixtures were pre- the olfactory responses of males and females to synthetic pared from the stock solutions each day and diluted to volatiles and to identify key mixtures of compounds or 0.1 lg/ll before the bioassays. 123 Behavioral responses of Hyalesthes obsoletus to host-plant volatiles cues 73 Table 1 Composition of the Compound Sourcea Chaste tree mixturesb Nettle mixturesb synthetic mixtures tested in the bioassays, according to the 123 456 ratios of the natural blend of compounds emitted by fresh Alcohol shoots of the chaste tree and (Z)-3-hexen-1-ol SA – – – 5 5 5 nettle (Riolo et al. 2012) Ester (Z)-3-hexenyl acetate SA – – – 100 100 100 Aromatics Methyl salicylate SA – 0.5 0.5 – 0.2 0.2 Methyl benzoate SA – – 0.05 – – – Benzothiazole SA – – – 10 10 10 Monoterpene 1,8-cineole SA 100 100 100 – – – Sesquiterpenes (E,E)-a-farnesene C 40 40 40 10 10 10 (E)-b-farnesene F 10 10 10 – – – (E)-b-caryophyllene SA 20 20 20 1 1 1 Other compound (Z)-jasmone SA – – – – – 0.05 a Standards obtained from Sigma-Aldrich, Italy (SA), Contech Inc., Canada (C), Fluka Chemie, Switzerland (F) b Numbers represent doses of each compound, expressed in ng/ll Experiment 2 square of filter paper (1 cm2; Whatman, grade 5), with the blank represented by a square of filter paper with 10 ll Each single synthetic compound present in volatile mix- hexane applied.
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