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Host Plant Preferences and Detection of Host Plant Volatiles of the Migrating Psyllid Species Cacopsylla Pruni, the Vector of European Stone Fruit Yellows

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Host Plant Preferences and Detection of Host Plant Volatiles of the Migrating Psyllid Species Cacopsylla Pruni, the Vector of European Stone Fruit Yellows Journal of Pest Science (2020) 93:461–475 https://doi.org/10.1007/s10340-019-01135-3 ORIGINAL PAPER Host plant preferences and detection of host plant volatiles of the migrating psyllid species Cacopsylla pruni, the vector of European Stone Fruit Yellows Jannicke Gallinger1,4 · Barbara Jarausch2,3 · Wolfgang Jarausch3 · Jürgen Gross1,4 Received: 25 February 2019 / Revised: 15 May 2019 / Accepted: 11 June 2019 / Published online: 19 June 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Plant-emitted volatile organic compounds play an important role in plant–insect interactions. Thanks to plant-emitted vola- tiles, herbivores are able to fnd suitable hosts. Recognition and location of host plants are a key challenge for successful survival and reproduction of migrating insects, such as the plum psyllid Cacopsylla pruni. This psyllid migrates between Prunus spp. for reproduction and conifers for overwintering. C. pruni also is the only known vector of ‘Candidatus Phyto- plasma prunorum’, a plant pathogen causing the European Stone Fruit Yellows, a severe plant disease. The preference of C. pruni for diferent Prunus species was monitored in the feld. The sampling revealed a high abundance of C. pruni on Prunus spinosa, the natural host, as well as on diferent Prunus rootstock suckers. To investigate the infuence of volatile profles from diferent plants on the host preferences of C. pruni, the volatiles of two reproduction hosts and one overwinter- ing host were sampled and analyzed by gas chromatography and mass spectrometry. The volatile compositions were com- pared, and important components that lead to the diferentiation between plant species and growth stages were identifed. Antennal responses of C. pruni females were elicited by eleven plant species and growth stage-specifc volatiles, detected by electroantennography. The role of host plant volatiles on the migration behavior and the use of synthetic components in alternative control strategies are discussed. Keywords ‘Candidatus Phytoplasma prunorum’ · Plum leaf sucker · Host location · Olfaction · EAG · Migration · Prunus spp Key message Communicated by M. Traugott. Electronic supplementary material The online version of this • Cacopsylla pruni is the vector of European Stone Fruit article (https ://doi.org/10.1007/s1034 0-019-01135 -3) contains Yellows, which annually causes high economic losses in supplementary material, which is available to authorized users. European stone fruit production. • Species and growth stage-specifc volatiles of reproduc- * Jürgen Gross [email protected] tion and overwintering hosts were identifed. • Antennal responses of female plum psyllids to aldehydes, 1 Laboratory of Applied Chemical Ecology, Institute for Plant terpenes, acetophenone and (Z)-3-hexenyl acetate were Protection in Fruit Crops and Viticulture, Julius Kühn- detected. Institut, Federal Research Centre for Cultivated Plants, C. pruni Dossenheim, Germany • showed no olfactory preference for reproduction or overwintering hosts. 2 Laboratory of Zoology, Institute for Plant Protection in Fruit Crops and Viticulture, Julius Kühn-Institut, Federal Research • Results could be used for the development of innovative Centre for Cultivated Plants, Siebeldingen, Germany control strategies, such as push–pull or attract-and-kill 3 AlPlanta-Institute for Plant Research, RLP AgroScience, strategies. Neustadt an der Weinstrasse, Germany 4 Plant Chemical Ecology, Technical University of Darmstadt, Darmstadt, Germany Vol.:(0123456789)1 3 462 Journal of Pest Science (2020) 93:461–475 Introduction is the preferred reproduction host in natural habitats and is asymptomatically infected with ‘Ca. P. prunorum’ Olfaction is of high importance for insects. The develop- (Jarausch et al. 2019a, b). ment of specialized and sophisticated olfactory systems Former studies with another European migrating psyllid enabled insects to orientate and interact with their envi- species, Cacopsylla melanoneura, revealed diferences in ronment. Accordingly, olfactory cues are used to detect host plant preferences between emigrants and remigrants essential resources like food sources, oviposition sites (Mayer and Gross 2007). The carrot psyllid Trioza apicalis and mating partners even from a great distance (Gadenne was repelled by sawdust made from evergreen conifers, their et al. 2016). Detecting suitable host plants over distance overwintering hosts (Nehlin et al. 1994). Furthermore, repel- is crucial for herbivorous insects, especially for migrat- lent efects of VOCs from winter hosts were found in migrat- ing species. Migration behavior is well studied in species ing aphids (Pettersson et al. 1994). Based on these fnd- which show a movement over a very long distance, such ings, we hypothesize that C. pruni remigrants are attracted as the monarch butterfy (Reppert et al. 2016) and desert to volatiles emitted from Prunus spp. plants, during their locusts (Homberg 2015; Rosenberg and Burt 1999). Lit- spring migration period (reproduction host), and repelled tle is known, however, about seasonal migration occur- by volatiles typically released from conifers (overwinter- ring in psyllid species (known vectors of diferent plant ing hosts). Potentially, this preference is reversed during pathogens), like the univoltine and specialized plum psyl- their summer migration period and induces the migration lid Cacopsylla pruni, which alternates between evergreen of C. pruni emigrants from Prunus spp. to conifers located conifers and deciduous stone fruit trees (Prunus spp.) in higher altitudes. (Hodkinson 2009; Jarausch and Jarausch 2016; Ossian- In the present study, the occurrence of C. pruni in the nilsson 1992; Thébaud et al. 2009). At the end of win- feld was monitored to determine psyllid preference for spe- ter/early spring, C. pruni remigrants move from conifers cifc host species and varieties over three years. The results back to Prunus ssp. for oviposition. The new generation of this survey lead to the identifcation of attractive and develops through fve larval instars, and the emigrant non-attractive Prunus cultivars. Emitted volatile organic adults leave the reproduction hosts from May until the compounds (VOCs) of one cultivar from a non-attractive beginning of July (Thébaud et al. 2009). With migration species (P. persica) and one from an attractive species (Pru- between such divergent host plant species, the challenge nus insititia) were analyzed at diferent phenological stages. of long-range host location comes along. While plant Additionally, the volatile blends from an overwintering volatiles are exploited by psyllids to fnd their reproduc- host (Abies alba) were frstly sampled during the migration tion or overwintering host plants during migration (Gross period of C. pruni from conifers to Prunus spp. and secondly 2016; Mayer and Gross 2007; Mayer et al. 2011), the full during the migration period of the new generation from set of factors triggering psyllids’ migratory behavior still Prunus spp. to conifers. Species-specifc and developmen- remain unknown (Gallinger and Gross 2018; Jarausch tal stage-specifc compounds were identifed, and the elec- et al. 2019a). trophysiological response of C. pruni toward (+)-limonene, The migrating psyllid C. pruni is the vector of ‘Can- α-pinene, terpinolene, myrcene, camphene, bornylacetate, didatus Phytoplasma prunorum’, a cell wall-lacking hexanal, octanal, nonanal, decanal, dodecanal, (Z)-3-hexenyl bacteria, causing European Stone Fruit Yellows (ESFY) acetate, (Z)-3-hexene-1-ol, 1-phenylethane-1-one and tride- in various cultivated species of Prunus (Marcone et al. cane was investigated to identify compounds, which may 2010). Today, ESFY is of considerable economic sig- drive psyllid preferences for diferent hosts. Identifcation nifcance in European agriculture, particularly in peach of attractant and repellent VOCs could improve the devel- (Prunus persica) and apricot (Prunus armeniaca) cultiva- opment of alternative plant protection measurements like tion (Marcone et al. 2010, 2011). Diverse crossbreedings push–pull or attract-and-kill strategies against C. pruni. of diferent Prunus spp. ofer a wide range of available rootstocks and cultivars. Various stone fruit species show diferent susceptibilities to ESFY infections in targeted Materials and methods grafting experiments (Carraro et al. 2002, 2004; Kison and Seemüller 2001) and varying infestation rates in feld Insects surveys (Jarausch et al. 1998, 2000, 2019b; Richter 2002). Diferences in the natural occurrence of infection rates of In early spring (March/April), C. pruni remigrants (over- Prunus spp. could be linked to diferent infestation lev- wintered adults) were caught using beating tray method els with C. pruni (Carraro et al. 2002; Mergenthaler et al. according to Weintraub and Gross (2013). Remigrants used 2017) due to their host plant preferences. Prunus spinosa for olfactometer trails were sampled from P. spinosa and Prunus besseyi x Prunus cerasifera (cv. Ferlenain) trees at 1 3 Journal of Pest Science (2020) 93:461–475 463 an experimental orchard of Dienstleistungszentrum Ländli- to trees of approximately 2 m height. Detailed information cher Raum (DLR) Rheinpfalz, Neustadt an der Weinstrasse, on the setting of the Prunus orchard is provided in Fig. S1 Germany, and from P. spinosa, P. cerasifera, P. insititia (cv. (Supplementary material 1). All Prunus genotypes were GF 655-2) and P. domestica (cv. Wavit) at the experimen- sampled weekly, starting with the arrival
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