Abstract
Plant-emitted volatile organic compounds play an important role in plant–insect interactions. Thanks to plant-emitted volatiles, herbivores are able to find 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 Phytoplasma prunorum’, a plant pathogen causing the European Stone Fruit Yellows, a severe plant disease. The preference of C. pruni for different Prunus species was monitored in the field. The sampling revealed a high abundance of C. pruni on Prunus spinosa, the natural host, as well as on different Prunus rootstock suckers. To investigate the influence of volatile profiles from different plants on the host preferences of C. pruni, the volatiles of two reproduction hosts and one overwintering host were sampled and analyzed by gas chromatography and mass spectrometry. The volatile compositions were compared, and important components that lead to the differentiation between plant species and growth stages were identified. Antennal responses of C. pruni females were elicited by eleven plant species and growth stage-specific 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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Explore related subjects
Discover the latest articles and news from researchers in related subjects, suggested using machine learning.References
Alquézar B, Volpe HXL, Magnani RF, de Miranda MP, Santos MA, Wulff NA, Bento JMS, Parra JRP, Bouwmeester H, Peña L (2017) β-caryophyllene emitted from a transgenic Arabidopsis or chemical dispenser repels Diaphorina citri, vector of Candidatus Liberibacters. Sci Rep 7:5639. https://doi.org/10.1038/s41598-017-06119-w
Anton S, Gadenne C (1999) Effect of juvenile hormone on the central nervous processing of sex pheromone in an insect. PNAS 96:5764–5767. https://doi.org/10.1073/pnas.96.10.5764
Brandt A, Gorenflo A, Siede R, Meixner M, Büchler R (2016) The neonicotinoids thiacloprid, imidacloprid, and clothianidin affect the immunocompetence of honey bees (Apis mellifera L.). J Insect Physiol 86:40–47. https://doi.org/10.1016/j.jinsphys.2016.01.001
Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects-finding the right mix. Phytochemistry 72:1605–1611. https://doi.org/10.1016/j.phytochem.2011.04.011
Bundesamt für Verbraucherschutz und Lebensmittelsicherheit (2018) Pflanzenschutzmittel-Verzeichnis 2018—Teil 2: Gemüsebau—Obstbau—Zierpflanzenbau, Braunschweig. www.bvl.bund.de/infopsm. Accessed 18 Feb 2019
Carraro L, Ferrini F, Ermacora P, Loi N (2002) Role of wild Prunus species in the epidemiology of European stone fruit yellows. Plant Pathol 51:513–517. https://doi.org/10.1046/j.1365-3059.2002.00732.x
Carraro L, Ferrini F, Ermacora P, Loi N (2004) Transmission of European stone fruit yellows phytoplasma to prunus species by using vector and graft transmission. Acta Hortic 657:449–453. https://doi.org/10.17660/ActaHortic.2004.657.72
Clavijo McCormick A, Gershenzon J, Unsicker SB (2014) Little peaks with big effects: establishing the role of minor plant volatiles in plant-insect interactions. Plant, Cell Environ 37:1836–1844. https://doi.org/10.1111/pce.12357
Cook SM, Khan ZR, Pickett JA (2007) The use of push-pull strategies in integrated pest management. Annu Rev Entomol 52:375–400. https://doi.org/10.1146/annurev.ento.52.110405.091407
Coutinho-Abreu IV, McInally S, Forster L, Luck R, Ray A (2014) Odor coding in a disease-transmitting herbivorous insect, the asian citrus psyllid. Chem Senses 39:539–549. https://doi.org/10.1093/chemse/bju023
Deletre E, Schatz B, Bourguet D, Chandre F, Williams L, Ratnadass A, Martin T (2016) Prospects for repellent in pest control: current developments and future challenges. Chemoecology 26:127–142. https://doi.org/10.1007/s00049-016-0214-0
Dingle H (2009) Migration. In: Resh VH, Cardé RT (eds) Encyclopedia of insects. Elsevier/Academic Press, Amsterdamm, pp 628–633. https://doi.org/10.1016/b978-0-12-374144-8.00176-4
Drake V (1988) The influence of atmospheric structure and motions on insect migration. Annu Rev Entomol 33:183–210. https://doi.org/10.1146/annurev.ento.33.1.183
Ellis C, Park KJ, Whitehorn P, David A, Goulson D (2017) The neonicotinoid insecticide thiacloprid impacts upon bumblebee colony development under field conditions. Environ Sci Technol 51:1727–1732. https://doi.org/10.1021/acs.est.6b04791
Farnier K, Dyer AG, Steinbauer MJ (2014) Related but not alike: not all Hemiptera are attracted to yellow. Front Ecol Evol 2:263. https://doi.org/10.3389/fevo.2014.00067
Farnier K, Dyer AG, Taylor GS, Peters RA, Steinbauer MJ (2015) Visual acuity trade-offs and microhabitat-driven adaptation of searching behaviour in psyllids (Hemiptera: Psylloidea: Aphalaridae). J Exp Biol 218:2660. https://doi.org/10.1242/jeb.128967
Farnier K, Davies NW, Steinbauer MJ (2018) Not led by the nose: volatiles from undamaged eucalyptus hosts do not influence psyllid orientation. Insects 9:166–179. https://doi.org/10.3390/insects9040166
Gadenne C, Renou M, Sreng L (1993) Hormonal control of pheromone responsiveness in the male black cutworm Agrotis ipsilon. Experientia 49:721–724. https://doi.org/10.1007/BF01923960
Gadenne C, Barrozo RB, Anton S (2016) Plasticity in Insect olfaction: to smell or not to smell? Annu Rev Entomol 61:317–333. https://doi.org/10.1146/annurev-ento-010715-023523
Gallinger J, Gross J (2018) Unraveling the host plant alternation of Cacopsylla pruni—adults but not nymphs can survive on conifers due to phloem/xylem composition. Front Plant Sci 9:484. https://doi.org/10.3389/fpls.2018.00484
Gallinger J, Dippel C, Gross J (2019) Interfering host location of Cacopsylla pruni with repellent plant volatiles. IOBC-WPRS Bulletin (in press)
George J, Robbins PS, Alessandro RT, Stelinski LL, Lapointe SL (2016) Formic and acetic acids in degradation products of plant volatiles elicit olfactory and behavioral responses from an insect vector. Chem Senses 41:325–338. https://doi.org/10.1093/chemse/bjw005
Gross J (2016) Chemical communication between phytopathogens, their host plants and vector insects and eavesdropping by natural enemies. Front Ecol Evol 4:104. https://doi.org/10.3389/fevo.2016.00104
Gross J, Gündermann G (2016) Principles of IPM in cultivated crops and implementation of innovative strategies for sustainable plant protection. In: Horowitz AR (ed) Advances in insect control and resistance management. Springer, Cham, pp 9–26
Gross J, Mekonen N (2005) Plant odours influence the host finding behaviour of apple psyllids (Cacopsylla picta; C. melanoneura). IOBC/WPRS Bull 28:351–355
Gross J, Gallinger J, Rid M (2019) Collection, identification, and statistical analysis of volatile organic compound patterns emitted by phytoplasma infected plants. In: Musetti R, Pagliari L (eds) Phytoplasmas. Springer, New York, pp 333–343
Han B, Zhang Q-H, Byers JA (2012) Attraction of the tea aphid, Toxoptera aurantii, to combinations of volatiles and colors related to tea plants. Entomol Exp Appl 144:258–269. https://doi.org/10.1111/j.1570-7458.2012.01303.x
Hardie J, Visser JH, Piron PGM (1994) Perception of volatiles associated with sex and food by different adult forms of the black bean aphid, Aphis fabae. Physiol Entomol 19:278–284
Hodkinson ID (2009) Life cycle variation and adaptation in jumping plant lice (Insecta: Hemiptera: Psylloidea): a global synthesis. J Nat Hist 43:65–179. https://doi.org/10.1080/00222930802354167
Homberg U (2015) Sky compass orientation in desert locusts-evidence from field and laboratory studies. Front Behav Neurosci 9:346. https://doi.org/10.3389/fnbeh.2015.00346
Horton DR, Landolt PJ (2007) Attraction of male pear psylla, Cacopsylla pyricola, to female-infested pear shoots. Entomol Exp Appl 123:177–183. https://doi.org/10.1111/j.1570-7458.2007.00537.x
Jarausch W, Jarausch B (2016) A permanent rearing system for Cacopsylla pruni, the vector of ‘Candidatus Phytoplasma prunorum’. Entomol Exp Appl 159:112–116. https://doi.org/10.1111/eea.12427
Jarausch W, Lansac M, Saillard C, Broquaire JM, Dosba F (1998) PCR Assay for specific detection of European stone fruit yellows phytoplasmas and its use for epidemiological studies in France. Eur J Plant Pathol 104:17–27
Jarausch W, Saillard C, Broquaire JM, Garnier M, Dosba F (2000) PCR-RFLP and sequence analysis of a non-ribosomal fragment for genetic characterization of European stone fruit yellows phytoplasmas infecting various Prunus species. Mol Cell Probes 14:171–179. https://doi.org/10.1006/mcpr.2000.0304
Jarausch W, Jarausch B, Fritz M, Runne M, Etropolska A, Pfeilstetter E (2019a) Epidemiology of European stone fruit yellows in Germany: the role of wild Prunus spinosa. Eur J Plant Pathol 50:185. https://doi.org/10.1007/s10658-019-01669-3
Jarausch B, Tedeschi R, Sauvion N, Gross J, Jarausch W (2019b) Psyllid vectors. In: Bertaccini A, Weintraub P, Rao GP, Mori N (eds) Phytoplasmas: Plant Pathogenic Bacteria - II. Springer, Singapore, pp 53–78. https://doi.org/10.1007/978-981-13-2832-9_3
Kison H, Seemüller E (2001) Differences in Strain virulence of the European stone fruit yellows phytoplasma and susceptibility of stone fruit trees on various rootstocks to this pathogen. J Phytopathol 149:533–541. https://doi.org/10.1046/j.1439-0434.2001.00671.x
Kristoffersen L, Larsson MC, Anderbrant O (2008) Functional characteristics of a tiny but specialized olfactory system: olfactory receptor neurons of carrot psyllids (Homoptera: Triozidae). Chem Senses 33:759–769. https://doi.org/10.1093/chemse/bjn034
Labonne G, Lichou J (2004) Data on the life cycle of cacopsylla pruni, psyllidae vector of European stone fruit yellows (ESFY) phytoplasma, in France. Acta Hortic 657:465–470
Lapointe SL, Hall DG, George J (2016) A phagostimulant blend for the Asian citrus psyllid. J Chem Ecol 42:941–951. https://doi.org/10.1007/s10886-016-0745-4
Lauterer P (1999) Results of the investigations on Hemiptera in Moravia, made by the Moravian museum (Psylloidea 2). Acta Musei Moraviae Sci Biol (Brno) 84:71–151
Liaw A, Wiener M (2002) Classification and regression by randomforest. R News 2:18–22
Loch AD (2005) Mortality and recovery of eucalypt beetle pest and beneficial arthropod populations after commercial application of the insecticide alpha-cypermethrin. For Ecol Manage 217:255–265. https://doi.org/10.1016/j.foreco.2005.06.006
Linstrom P, Mallard, WG (1997) NIST Chemistry WebBook, NIST standard reference database 69. Accessed 16 Feb 2019
Marcone C, Jarausch B, Jarausch W (2010) Candidatus Phytoplasma prunorum, the causal agent of European stone fruit yellows: an overview. J Plant Pathol 92:19–34
Marcone C, Jarausch B, Jarausch W, Dosba F (2011) CHAPTER 43: European stone fruit yellows phytoplasma. In: Hadidi A, Barba M, Candresse T, Jelkmann W (eds) Virus and virus-like diseases of pome and stone fruits. APS Press/American Phytopathological Society, St. Paul, pp 233–241
Markheiser A, Rid M, Biancu S, Gross J, Hoffmann C (2018) Physical factors influencing the oviposition behaviour of European grapevine moths Lobesia botrana and Eupoecilia ambiguella. J Appl Entomol 142:201–210. https://doi.org/10.1111/jen.12423
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. https://doi.org/10.1007/s11829-014-9326-z
Mas F, Vereijssen J, Suckling DM (2014) Influence of the pathogen Candidatus Liberibacter solanacearum on tomato host plant volatiles and psyllid vector settlement. J Chem Ecol 40:1197–1202. https://doi.org/10.1007/s10886-014-0518-x
Mayer CJ, Gross J (2007) Different host plant odours influence migration behaviour of Cacopsylla melanoneura (Förster), an insect vector of the apple proliferation phytoplasma. IOBC/WPRS Bull 30:177–184
Mayer CJ, Vilcinskas A, Gross J (2008a) Pathogen-induced release of plant allomone manipulates vector insect behavior. J Chem Ecol 34:1518–1522. https://doi.org/10.1007/s10886-008-9564-6
Mayer CJ, Vilcinskas A, Gross J (2008b) Phytopathogen lures its insect vector by altering host plant odor. J Chem Ecol 34:1045–1049. https://doi.org/10.1007/s10886-008-9516-1
Mayer CJ, Vilcinskas A, Gross J (2011) Chemically mediated multitrophic interactions in a plant-insect vector-phytoplasma system compared with a partially nonvector species. Agric For Entomol 13:25–35. https://doi.org/10.1111/j.1461-9563.2010.00495.x
Meier U (2018) Growth stages of mono- and dicotyledonous plants: BBCH Monograph. https://doi.org/10.5073/20180906-074619
Mergenthaler E, Kiss B, Kiss E, Viczián O (2017) Survey on the occurrence and infection status of Cacopsylla pruni, vector of European stone fruit yellows in Hungary. Bull Insectol 70:171–176
Michaud JP, Grant AK (2003) IPM-compatibility of foliar insecticides for citrus: Indices derived from toxicity to beneficial insects from four orders. J Insect Sci 3:265. https://doi.org/10.1093/jis/3.1.18
Nehlin G, Valterová I, Borg-Karlson AK (1994) Use of conifer volatiles to reduce injury caused by carrot psyllid, Trioza apicalis, Förster (Homoptera, Psylloidea). J Chem Ecol 20:771–783. https://doi.org/10.1007/BF02059612
Ossiannilsson F (ed) (1992) The Psylloidea (Homoptera) of Fennoscandia and Denmark. Fauna entomologica Scandinavica, vol 26. Brill, Leiden, New York, Köln
Paleskić C, Bachinger K, Brader G, Kickenweiz M, Engel C, Wurm L, Czipin L, Riedle-Bauer M (2017) Cage and field experiments as basis for the development of control strategies against Cacopsylla pruni, the vector of European stone fruit yellows. Ann Appl Biol 170:357–368. https://doi.org/10.1111/aab.12340
Patt JM, Sétamou M (2010) Responses of the Asian citrus psyllid to volatiles emitted by the flushing shoots of its rutaceous host plants. Environ Entomol 39:618–624. https://doi.org/10.1603/EN09216
Pettersson J, Pickett JA, Pye BJ, Quiroz A, Smart LE, Wadhams LJ, Woodcock CM (1994) Winter host component reduces colonization by bird-cherry-oat aphid, Rhopalosiphum padi (L.) (homoptera, aphididae), and other aphids in cereal fields. J Chem Ecol 20:2565–2574. https://doi.org/10.1007/BF02036192
Powell G, Hardie J (2001) The chemical ecology of aphid host alternation: How do return migrants find the primary host plant? Appl Entomol Zool 36:259–267
Ranganathan Y, Borges RM (2010) Reducing the babel in plant volatile communication: using the forest to see the trees. Plant Biol 12:735–742. https://doi.org/10.1111/j.1438-8677.2009.00278.x
Rankin M (1992) The cost of migration in insects. Annu Rev Entomol 37:533–559. https://doi.org/10.1146/annurev.ento.37.1.533
R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 21 Oct 2018
Reppert SM, Guerra PA, Merlin C (2016) Neurobiology of monarch butterfly migration. Annu Rev Entomol 61:25–42. https://doi.org/10.1146/annurev-ento-010814-020855
Richter S (2002) Susceptibility of Austrian apricot and peach cultivars to ESFY. Plant Protect Sci 38:281–284
Rid M, Mesca C, Ayasse M, Gross J (2016) Apple proliferation phytoplasma influences the pattern of plant volatiles emitted depending on pathogen virulence. Front Ecol Evol 3:271. https://doi.org/10.3389/fevo.2015.00152
Rid M, Markheiser A, Hoffmann C, Gross J (2018) Waxy bloom on grape berry surface is one important factor for oviposition of European grapevine moths. J Pest Sci 91:1225–1239. https://doi.org/10.1007/s10340-018-0988-7
Rosenberg J, Burt PJA (1999) Windborne displacements of desert locusts from Africa to the Caribbean and South America. Aerobiologia 15:167–175
Sandström J (2000) Nutritional quality of phloem sap in relation to host plant-alternation in the bird cherry-oat aphid. Chemoecology 10:17–24. https://doi.org/10.1007/s000490050003
Soroker V, Talebaev S, Harari A, Wesley SD (2004) The role of chemical cues in host and mate location in the pear psylla Cacopsylla bidens (Homoptera: Psyllidae). J Insect Behav 17:613–626. https://doi.org/10.1023/B:JOIR.0000042544.35561.1c
Thébaud G, Yvon M, Alary R, Sauvion N, Labonne G (2009) Efficient transmission of ‘Candidatus phytoplasma prunorum’ Is delayed by eight months due to a long latency in its host-alternating vector. Phytopathology 99:265–273. https://doi.org/10.1094/PHYTO-99-3-0265
Tooming E, Merivee E, Must A, Sibul I, Williams I (2014) Sub-lethal effects of the neurotoxic pyrethroid insecticide Fastac 50EC on the general motor and locomotor activities of the non-targeted beneficial carabid beetle Platynus assimilis (Coleoptera: Carabidae). Pest Manag Sci 70:959–966. https://doi.org/10.1002/ps.3636
Visser JH (1988) Host-plant finding by insects: orientation, sensory input and search patterns. J Insect Physiol 34:259–268
Visser JH, Piron PGM, Hardie J (1996) The aphids’ peripheral perception of plant volatiles. Entomol Exp Appl 80:35–38. https://doi.org/10.1111/j.1570-7458.1996.tb00880.x
Weintraub P, Gross J (2013) Capturing insect vectors of phytoplasmas. In: Dickinson M, Hodgetts J (eds) Phytoplasma, vol 938. Humana Press, Totowa, pp 61–72
Wenninger EJ, Stelinski LL, Hall DG (2009) Roles of olfactory cues, visual cues, and mating status in orientation of Diaphorina citri Kuwayama (Hemiptera: Psyllidae) to four different host plants. Environ Entomol 36:225–234. https://doi.org/10.1603/022.038.0128
Wickham H (2009) ggplot2: elegant graphics for data analysis. Use R. Springer, New York
Wolda H (1988) Insect seasonality: Why? Ann Rev Ecol Syst 19:1–18
Xu Q, Hatt S, Lopes T, Zhang Y, Bodson B, Chen J, Francis F (2018) A push–pull strategy to control aphids combines intercropping with semiochemical releases. J Pest Sci 91:93–103. https://doi.org/10.1007/s10340-017-0888-2
Yuvaraj JK, Andersson MN, Steinbauer MJ, Farnier K, Anderbrant O (2013) Specificity and sensitivity of plant odor-detecting olfactory sensory neurons in Ctenarytaina eucalypti (Sternorrhyncha: Psyllidae). J Insect Physiol 59:542–551. https://doi.org/10.1016/j.jinsphys.2013.03.004
Acknowledgements
We thank Svenja Stein, Sabine Wetzel, Sebastian Faus and Kai Lukat (Dossenheim, Germany) for experimental assistance. We are particularly grateful to Uwe Harzer (DLR Rheinpfalz, Neustadt, Germany) for the permission to conduct experiments and sampling in institute’s orchards. We thank Eva Gross (Schriesheim, Germany) for language editing. We are grateful to Stephen Lapointe, Justin George and Paul S. Robbins (USDA, Fort Pierce, USA) for helpful advices for conducting EAG with psyllids.
Funding
JGa was supported by a fund of the “Landwirtschaftliche Rentenbank” number 28RF4IP008. WJ was supported by the ZIM project KF2248403 MD9.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Human and animal rights
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by M. Traugott.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Gallinger, J., Jarausch, B., Jarausch, W. et al. Host plant preferences and detection of host plant volatiles of the migrating psyllid species Cacopsylla pruni, the vector of European Stone Fruit Yellows. J Pest Sci 93, 461–475 (2020). https://doi.org/10.1007/s10340-019-01135-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-019-01135-3