Journal of Pest Science

, Volume 90, Issue 4, pp 1219–1229 | Cite as

Use of substrate-borne vibrational signals to attract the Brown Marmorated Stink Bug, Halyomorpha halys

  • Valerio MazzoniEmail author
  • Jernej Polajnar
  • Marta Baldini
  • Marco Valerio Rossi Stacconi
  • Gianfranco Anfora
  • Roberto Guidetti
  • Lara Maistrello
Original Paper


Despite the increasing number of studies on the use of acoustic stimuli to control agricultural pests, this approach is still theoretical. Many insect pests, in particular hemipterans, use vibrational signals for mating communication, and therefore the application of a control strategy based on acoustic interference is a promising option. The Brown Marmorated Stink Bug, Halyomorpha halys, is causing severe economic damage to many crops in the USA and Italy. We tested a female vibrational signal, female signal 2 (FS2), to attract males in different settings, such as natural substrates, arenas and a cage representing an acoustic trap. We used video-tracking analysis and described the vibrational amplitude field around the individuals to study the male behavior. We found that FS2 can attract more than 50% of males to the source point and has a strong “loitering” effect on searching males that tend to remain in the stimulated area. We concluded that FS2 exhibits good attractiveness to H. halys males and that its potential use as a tool integrated into the currently existing pheromone traps should be tested in the field.


Biotremology Acoustic traps Integrated pest management Behavioral bioassays Hemiptera 



This research was supported by the grant ‘Innovative tools and protocols for monitoring and sustainable control of the alien stink bug H. 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’.

Compliance with ethical standards

Conflict of interest

There are no conflicts of interest involving the authors.

Animal rights statement

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Human rights statement

This article does not contain any studies with human participants performed by any of the authors.

Supplementary material

10340_2017_862_MOESM1_ESM.tiff (4.7 mb)
Online Resource 1 Scheme and vibrational amplitude field of the bean plants used in Test 1. Two bean plants were grown together in one pot having only one contact point at approximately mid-stem length. The mini-shaker (SH) was moved after each trial and thus the stimulated leaf (e.g., Lf1-SP) was randomly changed. The male releasing point was randomized among the non stimulated leaves. The Audio Sampling Points (ASPs) are indicated with black dots. Four of them were placed on the leaves (Lf1–Lf4) and other four on the stems (St1–St4). The mean (±SD) amplitude of the playback signal (as substrate velocity in μm/s) is reported. Different letters indicate significant differences between amplitude values recorded from the ASPs (p < 0.05) after Friedman’s test with replication followed by the Bonferroni post hoc test (TIFF 4827 kb)
10340_2017_862_MOESM2_ESM.tiff (3.5 mb)
Online Resource 2 Scheme of the arenas used in Test 2 (A) and Test 3 (B). (A) In Test 2, the mini-shaker was placed in direct contact with the arena surface. Four different Video Sampling Areas (VSA-T2), corresponding with as many Audio Sampling Points (ASP) were defined, one of them at the Stimulation Point (SP) and the others opposite (FR) and laterally (L1 and L2) to it. An additional ASP was placed on the Releasing Point (RP). (B) In Test 3, the SP was set at the external end of a paperboard rod and only two VSAs (VSA-T3) were defined, around the internal ends of the SP and FR rods, respectively. As a whole, the vibrational amplitude field was measured from 19 ASPs, 12 of them on the arena surface (a1–a8 plus L1, L2 and two inside each VSA) and 6 of them on the rods (SP, b1 and b2 on the vibrated rod, and b3, b4 and FR on the non-vibrated one). In (A), amplitude values (as substrate mean ± SD velocity in μm/s) are reported for each ASP; different letters indicate significant differences between amplitude values recorded from the ASPs (p < 0.05) after Friedman’s test with replication, followed by the Bonferroni post hoc test (TIFF 3570 kb)
10340_2017_862_MOESM3_ESM.tiff (5.5 mb)
Online Resource 3 Scheme (3D, above, and flattened diagram, below) of the acoustic trap used in Test 4. As a whole, 45 Audio Sampling Points (ASPs) were placed: 36 ASPs on the upper (Ceiling), lateral (Sides 1 and 2) and back (Back) faces (nine per face) of the net cage. Other four ASPs were placed on the Front face, two on the net Sleeve, one on the plastic Plastic funnel and two on the Cylinder, including the Stimulation Point (SP). Males were released inside the net cage (TIFF 5637 kb)
10340_2017_862_MOESM4_ESM.pdf (14 kb)
Supplementary material 4 (PDF 13 kb)
10340_2017_862_MOESM5_ESM.pdf (15 kb)
Supplementary material 5 (PDF 14 kb)
10340_2017_862_MOESM6_ESM.pdf (6 kb)
Supplementary material 6 (PDF 6 kb)
10340_2017_862_MOESM7_ESM.mp4 (1.4 mb)
Supplementary material 7 (MP4 1437 kb)


  1. Aldrich JR (1988) Chemical ecology of the Heteroptera. Annu Rev Entomol 33:211–238. doi: 10.1146/annurev.ento.33.1.211 CrossRefGoogle Scholar
  2. Aldrich JR, Khrimian A, Chen X, Camp MJ (2009) Semiochemically based monitoring of the invasion of the brown marmorated stink bug and unexpected attraction of the native green stink bug (Heteroptera: Pentatomidae) in Maryland. Fla Entomol 92:483–491. doi: 10.1653/024.092.0310 CrossRefGoogle Scholar
  3. Beck SD (1965) Resistance of plants to insects. Annu Rev Entomol 10:207–232CrossRefGoogle Scholar
  4. Cocroft RB, Rodríguez RL (2005) The behavioral ecology of insect vibrational communication. Bioscience 55:323–334. doi: 10.1641/0006-3568(2005)055[0323:TBEOIV]2.0.CO;2
  5. Čokl A, Virant-Doberlet M (2003) Communication with substrate-borne signals in small plant-dwelling insects. Annu Rev Entomol 48:29–50. doi: 10.1146/annurev.ento.48.091801.112605 CrossRefPubMedGoogle Scholar
  6. 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 58:1277–1283. doi: 10.1006/anbe.1999.1272 CrossRefPubMedGoogle Scholar
  7. Eriksson A, Anfora G, Lucchi A et al (2012) Exploitation of insect vibrational signals reveals a new method of pest management. PLoS ONE. doi: 10.1371/journal.pone.0032954 Google Scholar
  8. Foster SP, Harris MO (1997) Behavioral manipulation methods for insect pest-management. Annu Rev Entomol 42:123–146. doi: 10.1146/annurev.ento.42.1.123 CrossRefPubMedGoogle Scholar
  9. Hager FA, Kirchner WH (2014) Directional vibration sensing in the termite Macrotermes natalensis. J Exp Biol 217:2526–2530CrossRefPubMedGoogle Scholar
  10. James DG, Heffer R, Amaike M (1996) Field attraction of Biprorulus bibax Breddin (Hemiptera: Pentatomidae) to synthetic aggregation pheromone and (E)-2-hexenal, a pentatomid defense chemical. J Chem Ecol 22:1697–1708. doi: 10.1007/bf02272408 CrossRefPubMedGoogle Scholar
  11. Johnson BJ, Ritchie SA, Arthur BJ et al (2016) The siren’s song: exploitation of female flight tones to passively capture male Aedes aegypti (Diptera: Culicidae). J Med Entomol 53:245–248. doi: 10.1093/jme/tjv165 CrossRefPubMedGoogle Scholar
  12. Joseph SV, Bergh JC, Wright SE, Leskey TC (2013) Factors affecting captures of brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae), in baited pyramid traps. J Entomol Sci 48:43–51CrossRefGoogle Scholar
  13. Khrimian A, Zhang A, Weber DC et al (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 77:1708–1717. doi: 10.1021/np5003753 CrossRefPubMedGoogle Scholar
  14. Kuhelj A, de Groot M, Pajk F et al (2015) Energetic cost of vibrational signalling in a leafhopper. Behav Ecol Sociobiol 69:815–828. doi: 10.1007/s00265-015-1898-9 CrossRefGoogle Scholar
  15. Lee D-H, Short BD, Joseph SV et al (2013) Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environ Entomol 42:627–641. doi: 10.1603/EN13006 CrossRefPubMedGoogle Scholar
  16. Leskey TC, Hamilton GC, Nielsen AL et al (2012) Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag 23:218–226. doi: 10.1564/23oct07 CrossRefGoogle Scholar
  17. Leskey TC, Lee D-H, Glenn DM, Morrison WR (2015) Behavioral responses of the invasive Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) to light-based stimuli in the laboratory and field. J Insect Behav 28:674–692. doi: 10.1007/s10905-015-9535-z CrossRefGoogle Scholar
  18. Maistrello L, Dioli P, Bariselli M et al (2016) Citizen science and early detection of invasive species: phenology of first occurrences of Halyomorpha halys in Southern Europe. Biol Invasions 18:3109–3116. doi: 10.1007/s10530-016-1217-z CrossRefGoogle Scholar
  19. Mazzoni V, Prešern J, Lucchi A, Virant-Doberlet M (2009) Reproductive strategy of the Nearctic leafhopper Scaphoideus titanus Ball (Hemiptera: Cicadellidae). Bull Entomol Res. doi: 10.1017/S0007485308006408 PubMedGoogle Scholar
  20. Mazzoni V, Eriksson A, Anfora G et al (2014) Active space and the role of amplitude in plant-borne vibrational communication. Springer, Berlin, pp 125–145Google Scholar
  21. Mazzoni V, Polajnar J, Virant-Doberlet M (2015) Secondary spectral components of substrate-borne vibrational signals affect male preference. Behav Process 115:53–60. doi: 10.1016/j.beproc.2015.02.019 CrossRefGoogle Scholar
  22. Miklas N, Stritih N, Čokl A et al (2001) The influence of substrate on male responsiveness to the female calling song in Nezara viridula. J Insect Behav 14:313–332. doi: 10.1023/A:1011115111592 CrossRefGoogle Scholar
  23. Nielsen AL, Hamilton GC, Shearer PW (2011) Seasonal phenology and monitoring of the non-native Halyomorpha halys (Hemiptera: Pentatomidae) in soybean. Environ Entomol 40:231–238. doi: 10.1603/EN10187 CrossRefGoogle Scholar
  24. Pedigo LP, Rice ME (2014) Entomology and pest management, 6th edn. Waveland, Long GroveGoogle Scholar
  25. Pertot I, Caffi T, Rossi V et al (2016) A critical review of plant protection tools for reducing pesticide use on grapevine and new perspectives for the implementation of IPM in viticulture. Crop Prot. doi: 10.1016/j.cropro.2016.11.025 Google Scholar
  26. Polajnar J, Svensek D, Čokl A (2012) Resonance in herbaceous plant stems as a factor in vibrational communication of pentatomid bugs (Heteroptera: Pentatomidae). J R Soc Interface 9:1898–1907. doi: 10.1098/rsif.2011.0770 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Polajnar J, Eriksson A, Rossi Stacconi MV et al (2014) The process of pair formation mediated by substrate-borne vibrations in a small insect. Behav Process. doi: 10.1016/j.beproc.2014.07.013 Google Scholar
  28. Polajnar J, Eriksson A, Virant-Doberlet M, Mazzoni V (2016a) Mating disruption of a grapevine pest using mechanical vibrations: from laboratory to the field. J Pest Sci (2004) 89:909–921. doi: 10.1007/s10340-015-0726-3 CrossRefGoogle Scholar
  29. Polajnar J, Maistrello L, Bertarella A, Mazzoni V (2016b) Vibrational communication of the brown marmorated stink bug (Halyomorpha halys). Physiol Entomol 41:249–259. doi: 10.1111/phen.12150 CrossRefGoogle Scholar
  30. Rice KB, Bergh CJ, Bergmann EJ et al (2014) Biology, ecology, and management of Brown Marmorated Stink Bug (Hemiptera: Pentatomidae). J Integr Pest Manag 5(3):A1–A13CrossRefGoogle Scholar
  31. Sargent C, Martinson HM, Raupp MJ (2014) Traps and trap placement may affect location of brown marmorated stink bug (Hemiptera: Pentatomidae) and increase injury to tomato fruits in home gardens. Environ Entomol 43:432–438. doi: 10.1603/EN13237 CrossRefPubMedGoogle Scholar
  32. Virant-Doberlet M, Čokl A (2004) Vibrational communication in insects. Neotrop Entomol 33:121–134. doi: 10.1590/S1519-566X2004000200001 CrossRefGoogle Scholar
  33. Virant-Doberlet M, Čokl A, Zorovič M (2006) Use of substrate vibrations for orientation: from behaviour to physiology. In: Drosopoulus S, Claridge MF (eds) Insect sounds and communication: physiology, bahaviour, ecology and evolution. Taylor & Francis, New York, pp 81–97Google Scholar
  34. Virant-Doberlet M, King RA, Polajnar J, Symondson WOC (2011) Molecular diagnostics reveal spiders that exploit prey vibrational signals used in sexual communication. Mol Ecol 20:2204–2216. doi: 10.1111/j.1365-294X.2011.05038.x CrossRefPubMedGoogle Scholar
  35. Weber DC, Leskey TC, Walsh GC, Khrimian A (2014) Synergy of aggregation pheromone with methyl (E,E,Z)-2,4,6-decatrienoate in attraction of Halyomorpha halys (Hemiptera: Pentatomidae). J Econ Entomol 107:1061–1068CrossRefPubMedGoogle Scholar
  36. Witzgall P, Kirsch P, Cork A (2010) Sex pheromones and their impact on pest management. J Chem Ecol 36:80–100. doi: 10.1007/s10886-009-9737-y CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Fondazione Edmund MachSan Michele all’adigeItaly
  2. 2.National Institute of BiologyLjubljanaSlovenia
  3. 3.University of Modena and Reggio EmiliaReggio EmiliaItaly
  4. 4.Center Agriculture Food Environment (CAFE)University of TrentoTrentoItaly

Personalised recommendations