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Can Vibrational Playback Improve Control of an Invasive Stink Bug?

  • Jernej PolajnarEmail author
  • Lara Maistrello
  • Aya Ibrahim
  • Valerio Mazzoni
Chapter
Part of the Animal Signals and Communication book series (ANISIGCOM, volume 6)

Abstract

Improved understanding of the function of insect vibrational signals has spurred development of a vibrational method for mass-trapping the brown marmorated stink bug, which is currently one of the most notorious invasive insect pests. We outline the ongoing research program, which started with the basic description of close-range sexual behaviour that is mediated by vibrational signals, and continued with testing of a promising female vibrational signal that proved to be considerably attractive to males in playback trials. On this basis, a bi-modal trap was constructed, comprising an aggregation pheromone dispenser, the vibrational signal playback and a device for electrocuting the attracted animals in a pyramid trap design. Preliminary field trial results are discussed in the context of the interplay between chemical and vibrational modalities during reproductive behaviour in stink bugs, and the potential for achieving environmentally friendlier control of this pest.

Notes

Acknowledgements

The authors thank their colleagues who have contributed to the work presented here: Prof. Gianfranco Anfora (University of Trento), Prof. Roberto Guidetti (University of Modena and Reggio Emilia), and Dr. Marco Valerio Rossi Stacconi (Fondazione Edmund Mach). The authors also thank the students who contributed with their work to this research: Marta Baldini, Ambra Bertarella, Valeria Fattoruso and Roberto Miselli. The work on BMSB was funded by the grant “Innovative tools and protocols for monitoring and sustainable control of the alien stink bug Halyomorpha halys, a new phytosanitary threat, and of other harmful heteropterans for the fruit crops of the territory of Modena” (2013.065) of “Fondazione Cassa di Risparmio di Modena”. The first author was also supported by the Slovenian Research Agency (research core funding no. P1-0255). The authors also thank Vittorio Veronelli, Carlo Lotti and Marco Baldo of CBC-Europe for providing the necessary support to develop prototypes of vibrotraps.

References

  1. Abbott JC, Stewart KW (1993) Male search behavior of the stonefly, Pteronarcellabadia (Hagen) (Plecoptera: Pteronarcyidae), in relation to drumming. J Insect Behav 6(4):467–481CrossRefGoogle Scholar
  2. Abram P, Doyon J, Brodeur J, Gariépy T, Boivin G (2015) Susceptibility of Halyomorpha halys (Hemiptera: Pentatomidae) eggs to different life stages of three generalist predators. Can Entomol 147(2):222–226CrossRefGoogle Scholar
  3. Abram PK, Hoelmer KA, Acebes-Doria A, Andrews H, Beers EH, Bergh JC, Bessin R, Biddinger D, Botch P, Buffington ML, Cornelius LM, Costi E, Delfosse ES, Dieckhoff C, Dobson R, Donais Z, Grieshop M, Hamilton G, Haye T, Hedstrom C, Herlihy MV, Hoddle MS, Hooks CRR, Jentsch P, Joshi NK, Kuhar TP, Lara J, Lee JC, Legrand A, Leskey TC, Lowenstein D, Maistrello L, Mathews CR, Milnes JM, Morrison WR III, Nielsen AL, Ogburn EC, Pickett CH, Poley K, Pote J, Radl J, Shrewsbury PM, Talamas E, Tavella L, Walgenbach JF, Waterworth R, Weber DC, Welty C, Wiman NG (2017) Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe. J Pest Sci 90:1009–1020CrossRefGoogle Scholar
  4. Aluja M, Prokopy RJ (1992) Host search behaviour by Rhagoletis pornoneffa flies: inter-tree movement patterns in response to wind-borne fruit volatiles under field conditions. Physiol Entomol 17:1–8CrossRefGoogle Scholar
  5. Blaauw BR, Polk D, Nielsen AL (2015) IPM-CPR for peaches: incorporating behaviorally-based methods to manage Halyomorpha halys and key pests in peach. Pest Manag Sci 71(11):1513–1522PubMedCrossRefPubMedCentralGoogle Scholar
  6. Blassioli-Moraes MC, Laumann RA, Čokl A, Borges M (2005) Vibratory signals of four Neotropical stink bug species. Physiol Entomol 30:175–188CrossRefGoogle Scholar
  7. Bomford M, O’Brien P (1990) Sonic deterrents in animal damage control: a review of device tests and effectiveness. Wildl Soc Bull 148:411–422Google Scholar
  8. Borges M, Jepson PC, Howse PE (1987) Long-range mate location and close-range courtship behaviour of the green stink bug, Nezara viridula, and its mediation by sex pheromones. Entomol Exp Appl 44:205–212CrossRefGoogle Scholar
  9. Cardé RT (1990) Principles of mating disruption. In: Ridgway RL, Silverstein RM, Inscoe MN (eds) Behavior-modifying chemicals for insect management. Marcel Dekker, New York, pp 47–71Google Scholar
  10. Castracani C, Bulgarini G, Giannetti D, Spotti FA, Maistrello L, Mori A, Grasso DA (2017) Predatory ability of the ant Crematogaster scutellaris on the brown marmorated stink bug Halyomorpha halys. J Pest Sci 90:1181–1190CrossRefGoogle Scholar
  11. Claridge MF (2014) Insect sounds and communication—an introduction. In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication. Taylor & Francis, Boca Raton, pp 3–10Google Scholar
  12. Cocroft RB, Hamel J, Su Q, Gibson J (2014) Vibrational playback experiments: challenges and solutions. In: Cocroft RB, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational communication. Springer, Heidelberg, pp 215–247Google Scholar
  13. Čokl A (1983) Functional properties of vibroreceptors in the legs of Nezara viridula (L.) (Heteroptera: Pentatomidae). J Comp Physiol 150:261–269CrossRefGoogle Scholar
  14. Čokl A (2008) Stink bug interaction with host plants during communication. J Insect Physiol 54:1113–1124CrossRefGoogle Scholar
  15. Čokl A, Millar JG (2009) Manipulation of insect signaling for monitoring and control of pest insects. In: Ishaaya I, Horowitz R (eds) Biorational control of arthropod pests: application and resistance management. Springer, Dordrecht, pp 279–316CrossRefGoogle Scholar
  16. Čokl A, Virant-Doberlet M (2003) Communication with substrate-borne signals in small plant-dwelling insects. Annu Rev Entomol 48:29–50CrossRefGoogle Scholar
  17. Čokl A, Virant-Doberlet M, McDowell A (1999) Vibrational directionality in the southern green stink bug Nezara viridula (L.) is mediated by female song. Anim Behav 58:1277–1283CrossRefGoogle Scholar
  18. Čokl A, Virant-Doberlet M, Stritih N (2000) The structure and function of songs emitted by southern green stink bugs from Brazil, Florida, Italy and Slovenia. Physiol Entomol 25:196–205CrossRefGoogle Scholar
  19. Čokl A, McBrien HL, Millar JG (2001) Comparison of substrate-borne vibrational signals of two stink bug species, Acrosternum hilare and Nezara viridula (Heteroptera: Pentatomidae). Ann Entomol Soc Am 94(3):471–479CrossRefGoogle Scholar
  20. Čokl A, Zorović M, Žunič A, Virant-Doberlet M (2005) Tuning of host plants with vibratory songs of Nezara viridula L (Heteroptera: Pentatomidae). J Exp Biol 208:1481–1488PubMedPubMedCentralCrossRefGoogle Scholar
  21. Čokl A, Zorović M, Millar JG (2007) Vibrational communication along plants by the stink bugs Nezara viridula and Murgantia histrionica. Behav Process 75:40–54CrossRefGoogle Scholar
  22. Čokl A, Zorović M, Žunič Kosi A, Stritih N, Virant-Doberlet M (2014) Communication through plants in a narrow frequency window. In: Cocroft RB, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational communication. Springer, Heidelberg, pp 171–195Google Scholar
  23. Costi E, Haye T, Maistrello L (2017) Biological parameters of the invasive brown marmorated stink bug, Halyomorpha halys, in southern Europe. J Pest Sci 90:1059–1067CrossRefGoogle Scholar
  24. Elias DO, Mason AC (2014) The role of wave and substrate heterogeneity in vibratory communication: practical issues in studying the effect of vibratory environments in communication. In: Cocroft RB, Gogala M, Hill PSM, Wessel A (eds) Studying vibrational communication. Springer, Heidelberg, pp 215–247Google Scholar
  25. EPPO Reporting Service (2017) No. 5. European and Mediterranean Plant Protection Organization, Paris, p 3Google Scholar
  26. European Commission (2009a) Directive 2009/128/EC of the European Parliament and of the Council of 21 October 2009 establishing a framework for Community action to achieve the sustainable use of pesticides. Off J Eur Union 2009; L309/71, published 24.11.2009Google Scholar
  27. European Commission (2009b) Regulation (EC) No 1107/2009 of the European Parliament and of the Council of 21 October 2009 concerning the placing of plant protection products on the market and repealing Council Directives 79/117/EEC and 91/414/EEC. Off J Eur Union 2009; L309/1, published 24.11.2009Google Scholar
  28. Foster SP, Harris MO (1997) Behavioral manipulation methods for insect pest-management. Annu Rev Entomol 42:123–146PubMedCrossRefGoogle Scholar
  29. Gilsdorf JM, Hygnstrom SE, VerCauteren KC (2002) Use of frightening devices in wildlife damage management. Integr Pest Manag Rev 7:29–45CrossRefGoogle Scholar
  30. Gogala M (2006) Vibratory signals produced by Heteroptera—Pentatomorpha and Cimicomorpha. In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication. Taylor & Francis, Boca Raton, pp 275–295Google Scholar
  31. Goulson D, Birch MC, Wyatt TD (1994) Mate location in the deathwatch beetle, Xestobium rufovillosum De Geer (Anobiidae): orientation to substrate vibrations. Anim Behav 47:899–907CrossRefGoogle Scholar
  32. Hager FA, Glinka F, Kirchner WH (2016) Feel the women’s vibes: cues used for directional vibration sensing in Nezara viridula. In: Book of Abstracts. 1st International Symposium on Biotremology, San Michele all’Adige, Italy, 5–7 July 2016. https://eventi.fmach.it/content/download/10500/57362/file/Book%20of%20abstracts_FINAL.pdf
  33. Harris VE, Todd JW (1980) Temporal and numerical patterns of reproductive behavior in the southern green stink bug, Nezara viridula (Hemiptera: Pentatomidae). Entomol Exp Appl 27:105–116CrossRefGoogle Scholar
  34. Harris C, Abubeker S, Yu M, Leskey TC, Zhang A (2015) Semiochemical production and laboratory behavior response of the brown marmorated stink bug, Halyomorpha halys. PLoS One 10:e0140876PubMedPubMedCentralCrossRefGoogle Scholar
  35. Haye T, Weber DC (2017) Special issue on the brown marmorated stink bug, Halyomorpha halys: an emerging pest of global concern. J Pest Sci 90:987–988CrossRefGoogle Scholar
  36. Haye T, Abdallah S, Gariepy T, Wyniger D (2014) Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. J Pest Sci 87:407–418CrossRefGoogle Scholar
  37. Haye T, Fischer S, Zhang J, Gariepy T (2015) Can native egg parasitoids adopt the invasive brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae), in Europe? J Pest Sci 88(4):693–705CrossRefGoogle Scholar
  38. Hill PSM, Wessel A (2016) Biotremology. Curr Biol 26:R181–R191CrossRefGoogle Scholar
  39. Hoebeke ER, Carter ME (2003) Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proc Entomol Soc Wash 105:225–237Google Scholar
  40. Hofstetter RW, Dunn DD, McGuire R, Potter KA (2014) Using acoustic technology to reduce bark beetle reproduction. Pest Manag Sci 70:24–27PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hofstetter RW, McGuire R, Dunn DD (2016) Use of acoustics to disrupt and deter wood-infesting insects and other invertebrates from and within trees and wood products. United States Patent 2016/9,480,248 B2Google Scholar
  42. Horowitz AR, Ellsworth PC, Ishaaya I (2009) Biorational pest control – an overview. In: Ishaaya I, Horowitz R (eds) Biorational control of arthropod pests: application and resistance management. Springer, Dordrecht, pp 1–20Google Scholar
  43. Ibrahim SA, Henderson G, Zhu BCR, Fei H, Laine RA (2004) Toxicity and behavioral effects of nootkatone, 1,10-dihydronootkatone, and tetrahydronootkatone to the Formosan subterranean termite (Isoptera: Rhinotermitidae). J Econ Entomol 97(1):102–111PubMedCrossRefPubMedCentralGoogle Scholar
  44. Kawada H, Kitamura C (1983) The reproductive behavior of the brown marmorated stink bug, Halyomorpha mista Uhler (Heteroptera: Pentatomidae) I. Observation of mating behavior and multiple copulation. Appl Entomol Zool 18:234–242CrossRefGoogle Scholar
  45. Khrimian A, Zhang A, Weber DS, Ho H-Y, Aldrich JR, Vermillion KE, Siegler MA, Shirali S, Guzman F, Leskey TC (2014) Discovery of the aggregation pheromone of the brown marmorated stink bug (Halyomorpha halys) through the creation of stereoisomeric libraries of 1-bisabolen-3-ols. J Nat Prod 77(7):1708–1717PubMedCrossRefPubMedCentralGoogle Scholar
  46. Kirkpatrick RL, Harein PK (1965) Inhibition of reproduction of Indian meal moths, Plodia interpunctella, by exposure to amplified sound. J Econ Entomol 58(5):920–921CrossRefGoogle Scholar
  47. Kiruba S, Jinham AP, Kumaran JTT, Das SSM, Papadopoulou S (2009) Effectiveness of audible sound waves in reaching larvae of Corcyra cephalonica concealed under flour cover (Lepidoptera: Pyralidae). Entomol Gen 31(4):327–336CrossRefGoogle Scholar
  48. Korinšek G, Derlink M, Virant-Doberlet M, Tuma T (2016) An autonomous system of detecting and attracting leafhopper males using species- and sex-specific substrate borne vibrational signals. Comput Electron Agric 23:29–39CrossRefGoogle Scholar
  49. Kriticos DJ, Kean JM, Phillips CB, Senay SD, Acosta H, Haye T (2017) The potential global distribution of the brown marmorated stink bug, Halyomorpha halys, a critical threat to plant biosecurity. J Pest Sci 90:1033–1043CrossRefGoogle Scholar
  50. Kuhar TP, Short BD, Krawczyk G, Leskey TC (2017) Deltamethrin-incorporated nets as an integrated pest management tool for the invasive Halyomorpha halys (Hemiptera: Pentatomidae). J Econ Entomol 110:543–545PubMedCrossRefPubMedCentralGoogle Scholar
  51. Lamine C, Barbier M, Blanc J, Buurma J, Scherer-Haynes I, Lehota J, Maraccini E, Egon N, Paratte R, Szabo Z, Wierzbicka A (2010) Reducing the dependence on pesticides: a matter of transitions within the whole agri-food system. In: Building sustainable rural futures – the added value of systems approaches in times of change and uncertainty, Proceedings of the 9th European IFSA Symposium (4–7 July 2010). University of Natural Resources and Applied Life Sciences, Vienna, pp 1943–1954. http://ifsa.boku.ac.at/cms/index.php?id=107
  52. Lampson BD, Han YJ, Khalilian A, Greene J, Mankin RW, Foreman EG (2013) Automatic detection and identification of brown stink bug, Euschistus servus, and southern green stink bug, Nezara viridula, (Heteroptera: Pentatomidae) using intraspecific substrate-borne vibrational signals. Comput Electron Agric 91:154–159CrossRefGoogle Scholar
  53. Lanier GN (1990) Principles of attraction-annihilation: mass trapping and other means. In: Ridgway RL, Silverstein RM, Inscoe MN (eds) Behavior-modifying chemicals for insect management. Marcel Dekker, New York, pp 25–45Google Scholar
  54. Laumann RA, Bottura Maccagnan DH, Čokl A (2017) Use of vibratory signals for stink bug monitoring and control. In: Čokl A, Borges M (eds) Stink Bugs: biorational control based on communication processes. CRC Press, Boca Raton, pp 226–245CrossRefGoogle Scholar
  55. Lee D-H, Leskey TC (2015) Flight behavior of foraging and overwintering brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). Bull Entomol Res 105(5):566–573PubMedPubMedCentralCrossRefGoogle Scholar
  56. Lee D-H, Short BD, Joseph SV, Bergh JC, Leskey TC (2013) Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environ Entomol 42:627–641PubMedCrossRefPubMedCentralGoogle Scholar
  57. Lee D-H, Nielsen AL, Leskey TC (2014) Dispersal capacity and behavior of nymphal stages of Halyomorpha halys (Hemiptera: Pentatomidae) evaluated under laboratory and field conditions. J Insect Behav 27(5):639–651CrossRefGoogle Scholar
  58. Leskey TC, Nielsen AL (2018) Impact of the invasive brown marmorated stink bug in North America and Europe: history, biology, ecology, and management. Annu Rev Entomol 63:599–618PubMedCrossRefPubMedCentralGoogle Scholar
  59. Leskey TC, Lee D-H, Short BD, Wright SE (2012a) Impact of insecticides on the invasive Halyomorpha halys (Hemiptera: Pentatomidae): analysis of insecticide lethality. J Econ Entomol 105(5):1726–1735PubMedCrossRefPubMedCentralGoogle Scholar
  60. Leskey TC, Short BD, Butler BR, Wright SE (2012b) Impact of the invasive brown marmorated stink bug, Halyomorpha halys (Stål), in mid-Atlantic tree fruit orchards in the United States: case studies of commercial management. Psyche 2012:535062Google Scholar
  61. Leskey TC, Short BD, Lee D-H (2014) Efficacy of insecticide residues on adult Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) mortality and injury in apple and peach orchards. Pest Manag Sci 70:1097–1104PubMedCrossRefGoogle Scholar
  62. Lujo S, Hartman E, Norton K, Pregmon EA, Rohde BB, Mankin RW (2016) Disrupting mating behavior of Diaphorina citri (Liviidae). J Econ Entomol 109(6):2373–2379PubMedPubMedCentralCrossRefGoogle Scholar
  63. Maistrello L, Dioli P, Bariselli M, Mazzoli GL, Giacalone-Forini I (2016) Citizen science and early detection of invasive species: phenology of first occurrences of Halyomorpha halys in Southern Europe. Biol Invasions 18:3109–3116CrossRefGoogle Scholar
  64. Maistrello L, Vaccari G, Caruso S, Costi E, Bortolini S, Macavei L, Foca G, Ulrici A, Bortolotti PP, Nannini R, Casoli L, Fornaciari M, Mazzoli GL, Dioli P (2017) Monitoring of the invasive Halyomorpha halys, a new key pest of fruit orchards in northern Italy. J Pest Sci 90:1231–1244CrossRefGoogle Scholar
  65. Malek R, Tattoni C, Ciolli M, Corradini S, Andreis D, Ibrahim A, Mazzoni V, Eriksson A, Anfora G (2018) Coupling traditional monitoring and citizen science to disentangle the invasion of Halyomorpha halys. ISPRS Int J Geo-Inf 7(5):171.  https://doi.org/10.3390/ijgi7050171 CrossRefGoogle Scholar
  66. Mankin RW (2012) Applications of acoustics in insect pest management. CAB Rev 7(1):1–7CrossRefGoogle Scholar
  67. Mankin RW, Hagstrum DW, Smith MT, Roda AL, Kairo MTK (2011) Perspective and promise: a century of insect acoustic detection and monitoring. Am Entomol 57:30–44CrossRefGoogle Scholar
  68. Mankin RW, Rohde BB, McNeill SA, Paris TM, Zagvazdina NI, Greenfeder S (2013) Diaphorina citri (Hemiptera: Liviidae) responses to microcontroller-buzzer communication signals of potential use in vibration traps. Fla Entomol 96(4):1546–1555CrossRefGoogle Scholar
  69. Mankin RW, Rohde BB, McNeill SA (2015) Vibrational duetting mimics to trap and disrupt mating of the devastating Asian citrus psyllid insect pest. Proc Meetings Acoust 25:010006CrossRefGoogle Scholar
  70. Mazzoni V, Polajnar J, Virant-Doberlet M (2015) Secondary spectral components of substrate-borne vibrational signals affect male preference. Behav Process 115:53–60CrossRefGoogle Scholar
  71. Mazzoni V, Polajnar J, Baldini M, Rossi Stacconi MV, Anfora G, Guidetti R, Maistrello L (2017a) Use of substrate-borne vibrational signals to attract the brown marmorated stink bug, Halyomorpha halys. J Pest Sci 90:1219–1229CrossRefGoogle Scholar
  72. Mazzoni V, Gordon SD, Nieri R, Krugner R (2017b) Design of a candidate vibrational signal for mating disruption against the glassy-winged sharpshooter, Homalodisca vitripennis. Pest Manag Sci 73(11):2328–2333PubMedPubMedCentralCrossRefGoogle Scholar
  73. McBrien HL, Čokl A, Millar JG (2002) Comparison of substrate-borne vibrational signals of two congeneric stink bug species, Thyanta pallidovirens and T. custator accerra (Heteroptera: Pentatomidae). J Insect Behav 15(6):715–738CrossRefGoogle Scholar
  74. Metcalf RL (1994) Insecticides in pest management. In: Metcalf RL, Luckmann WH (eds) Introduction to insect pest management, 3rd edn. Wiley, New York, pp 245–314Google Scholar
  75. Miklas N, Stritih N, Čokl A, Virant-Doberlet M, Renou M (2001) The influence of substrate on male responsiveness to the female calling song in Nezara viridula. J Insect Behav 14(3):313–332CrossRefGoogle Scholar
  76. Miklas N, Lasnier T, Renou M (2003) Male bugs modulate pheromone emission in response to vibratory signals from conspecifics. J Chem Ecol 29:561–574PubMedPubMedCentralCrossRefGoogle Scholar
  77. Miles RN (2016) An analytical model for the propagation of bending waves on a plant stem due to vibration of an attached insect. Heliyon 2:e00086PubMedPubMedCentralCrossRefGoogle Scholar
  78. Millar JG, McBrien HL, Ho H-Y, Rice RE, Cullen E, Zalom FG, Čokl A (2002) Pentatomid bug pheromones in IPM: possible applications and limitations. IOBC wprs Bull 25(9):1–11Google Scholar
  79. Morrison WR III, Lee D-H, Short BD, Khrimian A, Leskey TC (2016a) Establishing the behavioral basis for an attract-and-kill strategy to manage the invasive Halyomorpha halys in apple orchards. J Pest Sci 89(1):81–96CrossRefGoogle Scholar
  80. Morrison WR III, Mathews CR, Leskey TC (2016b) Frequency, efficiency, and physical characteristics of predation by generalist predators of brown marmorated stink bug (Hemiptera: Pentatomidae) eggs. Biol Control 97:120–130CrossRefGoogle Scholar
  81. Mullen MA (1975) Infrasound retards development of Tribolium castaneum and Tribolium confusum. J Stored Prod Res 11:111–113CrossRefGoogle Scholar
  82. Nielsen AL, Hamilton GC (2009) Life history of the invasive species Halyomorpha halys (Hemiptera: Pentatomidae) in Northeastern United States. Ann Entomol Soc Am 102(4):608–616CrossRefGoogle Scholar
  83. Nielsen AL, Hamilton GC, Matadha D (2008) Developmental rate estimation and life table analysis for Halyomorpha halys (Hemiptera: Pentatomidae). Environ Entomol 37(2):348–355PubMedCrossRefPubMedCentralGoogle Scholar
  84. Nielsen AL, Dively G, Pote J, Zinati G, Mathews C (2016) Identifying a potential trap crop for a novel insect pest, Halyomorpha halys (Hemiptera: Pentatomidae), in organic farms. Environ Entomol 45(2):472–478PubMedCrossRefPubMedCentralGoogle Scholar
  85. Nieri R, Mazzoni V (2018) The reproductive strategy and the vibrational duet of the leafhopper Empoasca vitis. Insect Sci 25(5):869–882PubMedPubMedCentralCrossRefGoogle Scholar
  86. Nieri R, Mazzoni V, Gordon SD, Krugner R (2017) Mating behavior and vibrational mimicry in the glassy-winged sharpshooter, Homalodisca vitripennis. J Pest Sci 90(3):887–899CrossRefGoogle Scholar
  87. Norton MP, Karczub DG (2003) Fundamentals of noise and vibration analysis for engineers, 2nd edn. Cambridge University Press, Cambridge (NY), pp 259–260CrossRefGoogle Scholar
  88. Ota D, Čokl A (1991) Mate location in the Southern Green Stink Bug, Nezara viridula (Heteroptera: Pentatomidae), mediated through substrate-borne signals on ivy. J Insect Behav 4:441–447CrossRefGoogle Scholar
  89. Polajnar J, Čokl A (2008) Effect of vibratory disturbance on sexual behaviour of the southern green stink bug Nezara viridula (Heteroptera, Pentatomidae). Cent Eur J Biol 3(2):189–197Google Scholar
  90. Polajnar J, Svenšek D, Čokl A (2012) Resonance in herbaceous plant stems as a factor in vibrational communication of pentatomid bugs (Heteroptera: Pentatomidae). J R Soc Interface 9(73):1898–1907PubMedPubMedCentralCrossRefGoogle Scholar
  91. Polajnar J, Kavčič A, Žunič A, Čokl A (2013) Palomena prasina (Hemiptera: Pentatomidae) vibratory signals and their tuning with plant substrates. Cent Eur J Biol 8(7):670–680Google Scholar
  92. Polajnar J, Eriksson A, Lucchi A, Anfora G, Virant-Doberlet M, Mazzoni V (2015) Manipulating behaviour with substrate-borne vibrations – potential for insect pest control. Pest Manag Sci 71(1):15–23PubMedPubMedCentralCrossRefGoogle Scholar
  93. Polajnar J, Maistrello L, Bertarella A, Mazzoni V (2016a) Vibrational communication of the brown marmorated stink bug (Halyomorpha halys). Physiol Entomol 41(3):249–259CrossRefGoogle Scholar
  94. Polajnar J, Eriksson A, Virant-Doberlet M, Lucchi A, Mazzoni V (2016b) Developing a bioacoustic method for mating disruption of a leafhopper pest in grapevine. In: Horowitz AR, Ishaaya I (eds) Advances in insect control and resistance management. Springer, Heidelberg, pp 165–190CrossRefGoogle Scholar
  95. Polajnar J, Eriksson A, Virant-Doberlet M, Mazzoni V (2016c) Mating disruption of a grapevine pest using mechanical vibrations: from laboratory to the field. J Pest Sci 89:909–921CrossRefGoogle Scholar
  96. Potamitis I, Ganchev T, Kontomidas D (2009) On automatic bioacoustic detection of pests: the cases of Rhynchophorus ferrugineus and Sitophilus oryzae. J Econ Entomol 102:1681–1690CrossRefGoogle Scholar
  97. Pote JM, Nielsen AL (2017) Life stage specific predation of Halyomorpha halys (Stål) by generalist predators. Biol Control 114:1–7CrossRefGoogle Scholar
  98. Prešern J, Polajnar J, de Groot M, Zorović M, Virant-Doberlet M (2018) On the spot: utilization of directional cues in vibrational communication of a stink bug. Sci Rep 8:5418.  https://doi.org/10.1038/s41598-018-23710-x CrossRefPubMedPubMedCentralGoogle Scholar
  99. Rice KB, Bergh CJ, Bergmann EJ, Biddinger DJ, Dieckhoff C, Dively G, Fraser H, Gariepy T, Hamilton G, Haye T, Herbert A, Hoelmer K, Hooks CR, Jones A, Krawczyk G, Kuhar T, Martinson H, Mitchell W, Nielsen AL, Pfeiffer DG, Raupp MJ, Rodriguez-Saona C, Shearer P, Shrewsbury P, Venugopal PD, Whalen J, Wiman NG, Leskey TC, Tooker JF (2014) Biology, ecology, and management of brown marmorated stink bug (Hemiptera: Pentatomidae). J Integr Pest Manag 5(3):1–13CrossRefGoogle Scholar
  100. Saxena KN, Kumar H (1980) Interruption of acoustic communication and mating in a leafhopper and a planthopper by aerial sound vibrations picked up by plants. Experientia 36:933–936CrossRefGoogle Scholar
  101. Shestakov LS (2015) A comparative analysis of vibrational signals in 16 sympatric bug species (Pentatomidae, Heteroptera). Entomol Rev 95(3):310–325CrossRefGoogle Scholar
  102. Tillman PG, Cottrell TE (2016) Stink bugs (Hemiptera: Pentatomidae) in pheromone-baited traps near crop field edges in Georgia, USA. Fla Entomol 99(3):363–370CrossRefGoogle Scholar
  103. Toyama A, Ihara F, Yaginuma K (2006) Formation of aggregations in adults of the brown marmorated stink bug, Halyomorpha halys (Stål) (Heteroptera: Pentatomidae): The role of antennae in short-range locations. Appl Entomol Zool 41:309–315CrossRefGoogle Scholar
  104. Virant-Doberlet M, Čokl A (2004) Vibrational communication in insects. Neotrop Entomol 33(2):121–134CrossRefGoogle Scholar
  105. Weber DC, Morrison WR III, Khrimian A, Rice KB, Leskey TC, Rodriguez-Saona C, Nielsen AL, Blaauw BR (2017) Chemical ecology of Halyomorpha halys: discoveries and applications. J Pest Sci 90(4):989–1008CrossRefGoogle Scholar
  106. Witzgall P, Kirsch P, Cork A (2010) Sex pheromones and their impact on pest management. J Chem Ecol 36:80–100PubMedPubMedCentralCrossRefGoogle Scholar
  107. Xu J, Foneseca DM, Hamilton GC, Hoelmer KA, Nielsen AL (2014) Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biol Invasions 16:153–166CrossRefGoogle Scholar
  108. Zgonik V, Čokl A (2014) The role of signals of different modalities in initiating vibratory communication in Nezara viridula. Cent Eur J Biol 9:200–211Google Scholar
  109. Zhang QH, Schneidmiller RG, Hoover DR, Zhou G, Margaryan A, Bryant P (2014) Essential oils as spatial repellents for the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). J Appl Entomol 138(7):490–499CrossRefGoogle Scholar
  110. Zorovič M, Čokl A (2015) Laser vibrometry as a diagnostic tool for detecting wood-boring beetle larvae. J Pest Sci 88:107–112CrossRefGoogle Scholar
  111. Žunič A, Virant-Doberlet M, Čokl A (2011) Species recognition during substrate-borne communication in Nezara viridula (L.) (Pentatomidae: Heteroptera). J Insect Behav 24:468CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Jernej Polajnar
    • 1
    Email author
  • Lara Maistrello
    • 2
  • Aya Ibrahim
    • 3
    • 4
  • Valerio Mazzoni
    • 3
  1. 1.National Institute of BiologyLjubljanaSlovenia
  2. 2.University of Modena and Reggio EmiliaReggio EmiliaItaly
  3. 3.Fondazione Edmund MachSan Michele all’AdigeItaly
  4. 4.University of UdineUdineItaly

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