Journal of Pest Science

, Volume 93, Issue 1, pp 461–475 | Cite as

Host plant preferences and detection of host plant volatiles of the migrating psyllid species Cacopsylla pruni, the vector of European Stone Fruit Yellows

  • Jannicke Gallinger
  • Barbara Jarausch
  • Wolfgang Jarausch
  • Jürgen GrossEmail author
Original Paper


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.


Candidatus Phytoplasma prunorum’ Plum leaf sucker Host location Olfaction EAG Migration Prunus spp 



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.


JGa was supported by a fund of the “Landwirtschaftliche Rentenbank” number 28RF4IP008. WJ was supported by the ZIM project KF2248403 MD9.

Compliance with ethical standards

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.

Supplementary material

10340_2019_1135_MOESM1_ESM.docx (132 kb)
Supplementary material 1 (DOCX 132 kb)
10340_2019_1135_MOESM2_ESM.docx (38 kb)
Supplementary material 2 (DOCX 37 kb)


  1. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Anton S, Gadenne C (1999) Effect of juvenile hormone on the central nervous processing of sex pheromone in an insect. PNAS 96:5764–5767. CrossRefPubMedGoogle Scholar
  3. 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. CrossRefPubMedGoogle Scholar
  4. Bruce TJA, Pickett JA (2011) Perception of plant volatile blends by herbivorous insects-finding the right mix. Phytochemistry 72:1605–1611. CrossRefPubMedGoogle Scholar
  5. Bundesamt für Verbraucherschutz und Lebensmittelsicherheit (2018) Pflanzenschutzmittel-Verzeichnis 2018—Teil 2: Gemüsebau—Obstbau—Zierpflanzenbau, Braunschweig. Accessed 18 Feb 2019
  6. 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. CrossRefGoogle Scholar
  7. 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. CrossRefGoogle Scholar
  8. 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. CrossRefGoogle Scholar
  9. Cook SM, Khan ZR, Pickett JA (2007) The use of push-pull strategies in integrated pest management. Annu Rev Entomol 52:375–400. CrossRefPubMedGoogle Scholar
  10. 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. CrossRefPubMedGoogle Scholar
  11. 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. CrossRefGoogle Scholar
  12. Dingle H (2009) Migration. In: Resh VH, Cardé RT (eds) Encyclopedia of insects. Elsevier/Academic Press, Amsterdamm, pp 628–633. CrossRefGoogle Scholar
  13. Drake V (1988) The influence of atmospheric structure and motions on insect migration. Annu Rev Entomol 33:183–210. CrossRefGoogle Scholar
  14. 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. CrossRefPubMedGoogle Scholar
  15. Farnier K, Dyer AG, Steinbauer MJ (2014) Related but not alike: not all Hemiptera are attracted to yellow. Front Ecol Evol 2:263. CrossRefGoogle Scholar
  16. 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. CrossRefPubMedGoogle Scholar
  17. 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. CrossRefPubMedCentralGoogle Scholar
  18. Gadenne C, Renou M, Sreng L (1993) Hormonal control of pheromone responsiveness in the male black cutworm Agrotis ipsilon. Experientia 49:721–724. CrossRefGoogle Scholar
  19. Gadenne C, Barrozo RB, Anton S (2016) Plasticity in Insect olfaction: to smell or not to smell? Annu Rev Entomol 61:317–333. CrossRefPubMedGoogle Scholar
  20. 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. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gallinger J, Dippel C, Gross J (2019) Interfering host location of Cacopsylla pruni with repellent plant volatiles. IOBC-WPRS Bulletin (in press)Google Scholar
  22. 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. CrossRefPubMedGoogle Scholar
  23. Gross J (2016) Chemical communication between phytopathogens, their host plants and vector insects and eavesdropping by natural enemies. Front Ecol Evol 4:104. CrossRefGoogle Scholar
  24. 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 9–26CrossRefGoogle Scholar
  25. Gross J, Mekonen N (2005) Plant odours influence the host finding behaviour of apple psyllids (Cacopsylla picta; C. melanoneura). IOBC/WPRS Bull 28:351–355Google Scholar
  26. 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 333–343CrossRefGoogle Scholar
  27. 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. CrossRefGoogle Scholar
  28. 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 19:278–284CrossRefGoogle Scholar
  29. Hodkinson ID (2009) Life cycle variation and adaptation in jumping plant lice (Insecta: Hemiptera: Psylloidea): a global synthesis. J Nat Hist 43:65–179. CrossRefGoogle Scholar
  30. Homberg U (2015) Sky compass orientation in desert locusts-evidence from field and laboratory studies. Front Behav Neurosci 9:346. CrossRefPubMedPubMedCentralGoogle Scholar
  31. Horton DR, Landolt PJ (2007) Attraction of male pear psylla, Cacopsylla pyricola, to female-infested pear shoots. Entomol Exp Appl 123:177–183. CrossRefGoogle Scholar
  32. Jarausch W, Jarausch B (2016) A permanent rearing system for Cacopsylla pruni, the vector of ‘Candidatus Phytoplasma prunorum’. Entomol Exp Appl 159:112–116. CrossRefGoogle Scholar
  33. 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 104:17–27CrossRefGoogle Scholar
  34. 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. CrossRefPubMedGoogle Scholar
  35. 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. CrossRefGoogle Scholar
  36. 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. CrossRefGoogle Scholar
  37. 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. CrossRefGoogle Scholar
  38. 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. CrossRefPubMedGoogle Scholar
  39. 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 657:465–470CrossRefGoogle Scholar
  40. Lapointe SL, Hall DG, George J (2016) A phagostimulant blend for the Asian citrus psyllid. J Chem Ecol 42:941–951. CrossRefPubMedGoogle Scholar
  41. Lauterer P (1999) Results of the investigations on Hemiptera in Moravia, made by the Moravian museum (Psylloidea 2). Acta Musei Moraviae Sci Biol (Brno) 84:71–151Google Scholar
  42. Liaw A, Wiener M (2002) Classification and regression by randomforest. R News 2:18–22Google Scholar
  43. 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. CrossRefGoogle Scholar
  44. Linstrom P, Mallard, WG (1997) NIST Chemistry WebBook, NIST standard reference database 69. Accessed 16 Feb 2019Google Scholar
  45. Marcone C, Jarausch B, Jarausch W (2010) Candidatus Phytoplasma prunorum, the causal agent of European stone fruit yellows: an overview. J Plant Pathol 92:19–34Google Scholar
  46. 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 233–241CrossRefGoogle Scholar
  47. 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. CrossRefGoogle Scholar
  48. 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. CrossRefGoogle Scholar
  49. 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. CrossRefPubMedGoogle Scholar
  50. 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 30:177–184Google Scholar
  51. Mayer CJ, Vilcinskas A, Gross J (2008a) Pathogen-induced release of plant allomone manipulates vector insect behavior. J Chem Ecol 34:1518–1522. CrossRefPubMedGoogle Scholar
  52. Mayer CJ, Vilcinskas A, Gross J (2008b) Phytopathogen lures its insect vector by altering host plant odor. J Chem Ecol 34:1045–1049. CrossRefPubMedGoogle Scholar
  53. 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. CrossRefGoogle Scholar
  54. Meier U (2018) Growth stages of mono- and dicotyledonous plants: BBCH Monograph.
  55. 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 70:171–176Google Scholar
  56. 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. CrossRefGoogle Scholar
  57. 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. CrossRefPubMedGoogle Scholar
  58. Ossiannilsson F (ed) (1992) The Psylloidea (Homoptera) of Fennoscandia and Denmark. Fauna entomologica Scandinavica, vol 26. Brill, Leiden, New York, KölnGoogle Scholar
  59. 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. CrossRefGoogle Scholar
  60. 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. CrossRefPubMedGoogle Scholar
  61. 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. CrossRefPubMedGoogle Scholar
  62. Powell G, Hardie J (2001) The chemical ecology of aphid host alternation: How do return migrants find the primary host plant? Appl Entomol Zool 36:259–267CrossRefGoogle Scholar
  63. Ranganathan Y, Borges RM (2010) Reducing the babel in plant volatile communication: using the forest to see the trees. Plant Biol 12:735–742. CrossRefPubMedGoogle Scholar
  64. Rankin M (1992) The cost of migration in insects. Annu Rev Entomol 37:533–559. CrossRefGoogle Scholar
  65. R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 21 Oct 2018
  66. Reppert SM, Guerra PA, Merlin C (2016) Neurobiology of monarch butterfly migration. Annu Rev Entomol 61:25–42. CrossRefPubMedGoogle Scholar
  67. Richter S (2002) Susceptibility of Austrian apricot and peach cultivars to ESFY. Plant Protect Sci 38:281–284CrossRefGoogle Scholar
  68. 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. CrossRefGoogle Scholar
  69. 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. CrossRefGoogle Scholar
  70. Rosenberg J, Burt PJA (1999) Windborne displacements of desert locusts from Africa to the Caribbean and South America. Aerobiologia 15:167–175CrossRefGoogle Scholar
  71. Sandström J (2000) Nutritional quality of phloem sap in relation to host plant-alternation in the bird cherry-oat aphid. Chemoecology 10:17–24. CrossRefGoogle Scholar
  72. 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. CrossRefGoogle Scholar
  73. 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. CrossRefPubMedGoogle Scholar
  74. 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. CrossRefPubMedGoogle Scholar
  75. Visser JH (1988) Host-plant finding by insects: orientation, sensory input and search patterns. J Insect Physiol 34:259–268CrossRefGoogle Scholar
  76. Visser JH, Piron PGM, Hardie J (1996) The aphids’ peripheral perception of plant volatiles. Entomol Exp Appl 80:35–38. CrossRefGoogle Scholar
  77. Weintraub P, Gross J (2013) Capturing insect vectors of phytoplasmas. In: Dickinson M, Hodgetts J (eds) Phytoplasma, vol 938. Humana Press, Totowa, pp 61–72CrossRefGoogle Scholar
  78. 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. CrossRefGoogle Scholar
  79. Wickham H (2009) ggplot2: elegant graphics for data analysis. Use R. Springer, New YorkCrossRefGoogle Scholar
  80. Wolda H (1988) Insect seasonality: Why? Ann Rev Ecol Syst 19:1–18CrossRefGoogle Scholar
  81. 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. CrossRefGoogle Scholar
  82. 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. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratory of Applied Chemical Ecology, Institute for Plant Protection in Fruit Crops and ViticultureJulius Kühn-Institut, Federal Research Centre for Cultivated PlantsDossenheimGermany
  2. 2.Laboratory of Zoology, Institute for Plant Protection in Fruit Crops and ViticultureJulius Kühn-Institut, Federal Research Centre for Cultivated PlantsSiebeldingenGermany
  3. 3.AlPlanta-Institute for Plant ResearchRLP AgroScienceNeustadt an der WeinstrasseGermany
  4. 4.Plant Chemical EcologyTechnical University of DarmstadtDarmstadtGermany

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