Journal of Pest Science

, Volume 90, Issue 4, pp 1107–1118 | Cite as

Behavioral responses of predaceous minute pirate bugs to tridecane, a volatile emitted by the brown marmorated stink bug

  • Diego F. FragaEmail author
  • Joyce Parker
  • Antonio C. Busoli
  • George C. Hamilton
  • Anne L. Nielsen
  • Cesar Rodriguez-Saona
Original Paper


Since its introduction from Asia, the brown marmorated stink bug, Halyomorpha halys (Stål), has become a pest of many agricultural crops in the USA. Insect predators utilize H. halys as prey; however, the chemical cues used by them in prey location are largely unknown. Here, we hypothesized that tridecane, an H. halys-associated volatile, acts as a kairomone for the predaceous minute pirate bug, Orius insidiosus (Say). We conducted laboratory, greenhouse, and field experiments to: (1) assess the attraction of adult O. insidiosus to H. halys-damaged bean pods and tridecane in cage studies, and its effect on egg predation; (2) video record the behavioral response of O. insidiosus males and females to tridecane in a four-arm olfactometer; and (3) test whether Orius spp. are attracted to tridecane-baited sticky traps in peach, blueberry, and sunflower fields, and its effect on egg predation. In the greenhouse, O. insidiosus was attracted to H. halys-damaged pods and artificial plants baited with tridecane in the presence of prey (sentinel eggs); however, this attraction rarely led to increased egg predation. Although both O. insidiosus males and females spent more time in the arm of the olfactometer with tridecane, males were more responsive at a lower concentration than females. Similarly, Orius spp. were more attracted to tridecane-baited than unbaited traps in the field; however, there was no effect on egg predation. Altogether, while O. insidiosus is attracted to tridecane, this attraction did not always lead to higher predation, suggesting that this kairomone likely acts as an arrestant.


Orius insidiosus Halyomorpha halys BMSB Conservative biological control Invasive pests Kairomones 



Thanks to Big Buck Farms (Hammonton, NJ) for providing blueberry sites for this study and to Robert Holdcraft and Jordano Salamanca for assistance with volatile collections, olfactory assays, and data analysis. We also thank Kris Dahl, Charles Corris, Gabrielle Pintauro, Manuel Chacón-Fuentes, and Caryn Michel for their help with insect colony maintenance and field sampling, and Johnattan Hernández Cumplido, Elvira de Lange, and two anonymous reviewers for critical reading and comments on an earlier draft of the manuscript. Funding for this project was provided by USDA NIFA SCRI Grant #2011-51181-30937, multi-state hatch projects #NJ08270 and #NJ08225, a hatch project #NJ08192 to CR-S, and a scholarship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ, Brazil) (Process Number: 164869/2014-0) to DFF.


This study was funded by USDA NIFA SCRI Grant #2011-51181-30937 to GCH, ALN, and CR-S, multi-state hatch Projects #NJ08270 and #NJ08225 to CR-S, GCH, and ALN, a hatch Project #NJ08192 to CR-S, and a scholarship from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ, Brazil) (Process Number: 164869/2014-0) to DFF.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain studies with humans participants performed by any of the authors.


  1. Aldrich JR (1988) Chemical ecology of the Heteroptera. Annu Rev Entomol 33:211–238CrossRefGoogle Scholar
  2. Aldrich JR (1995) Chemical communication in the true bugs and parasitoid exploitation. In: Carde RT, Bell WJ (eds) Chemical ecology of insects. Chapman & Hall, New York, pp 318–363CrossRefGoogle Scholar
  3. Aldrich JR, Kochansky JP, Abrams CB (1984) Attractant for a beneficial insect and its parasitoids: pheromone of the predatory spined soldier bug, Podisus maculiventris (Hemiptera: Pentatomidae). Environ Entomol 13:1031–1036CrossRefGoogle Scholar
  4. Aldrich JR, Lusby WR, Marron BE, Nicolaou KC, Hoffmann MP, Wilson LT (1989) Pheromone blends of green stink bugs and possible parasitoid selection. Naturwissenschaften 76:173–175CrossRefGoogle Scholar
  5. Aldrich JR, Oliver JE, Shifflet T, Smith CL, Dively GP (2007) Semiochemical investigations of the insidiosus flower bug, Orius insidiosus (Say). J Chem Ecol 33:1477–1493CrossRefPubMedGoogle Scholar
  6. Andow DA (1990) Characterization of predation on egg masses of Ostrinia nubilalis (Lepidoptera: Pyralidae). Ann Entomol Soc Am 83:482–486CrossRefGoogle Scholar
  7. Beale MH, Birkett MA, Bruce TJA, Chamberlain K, Field LM, Huttly AK, Martin JL, Parker R, Phillips AL, Pickett JA, Prosser IM, Shewry PR, Smart LE, Wadhams LJ, Woodcock CM, Zhang Y (2006) Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. Proc Natl Acad Sci 103:10509–10513CrossRefPubMedPubMedCentralGoogle Scholar
  8. Biddinger D, Tooker J, Surcica A, Krawczyk G (2012) Survey of native biocontrol agents of the brown marmorated stink bug in Pennsylvania fruit orchards and adjacent habitat. Pa Fruit News 43:47–54Google Scholar
  9. Chabaane Y, Laplanche D, Turlings TCJ, Desurmont GA (2015) Impact of exotic insect herbivores on native tritrophic interactions: a case study of the African cotton leafworm, Spodoptera littoralis and insects associated with the field mustard Brassica rapa. J Ecol 103:109–117CrossRefGoogle Scholar
  10. Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733CrossRefGoogle Scholar
  11. Colazza S, Salerno G, Wajnberg E (1999) Volatile and contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelinidae). Biol Control 16:310–317CrossRefGoogle Scholar
  12. Colazza S, McElfresh JS, Millar JG (2004) Identification of volatiles synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis. J Chem Ecol 30:945–964CrossRefPubMedGoogle Scholar
  13. Colazza S, Cusumano A, Giudice DL, Peri E (2014) Chemo-orientation responses in hymenopteran parasitoids induced by substrate-borne semiochemicals. BioControl 59:1–17CrossRefGoogle Scholar
  14. De Boer JG, Dicke M (2004) The role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. J Chem Ecol 30:255–271CrossRefPubMedGoogle Scholar
  15. De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlonson JH, Paré PW (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573CrossRefGoogle Scholar
  16. Desurmont GA, Harvey J, Van Dam NM, Cristescu SM, Schiestl FP, Cozzolino S, Anderson P, Larsson MC, Kindlmann P, Danner H, Turlings TCJ (2014) Alien interference: disruption of infochemical networks by invasive insect herbivores. Plant Cell Environ 37:1854–1865CrossRefPubMedGoogle Scholar
  17. Fucarino A, Millar JG, McElfresh JS, Colazza S (2004) Chemical and physical signals mediating conspecific and heterospecific aggregation behavior of first instar stink bugs. J Chem Ecol 30:1257–1269CrossRefPubMedGoogle Scholar
  18. Gadino AN, Walton VM, Lee JC (2012) Evaluation of methyl salicylate lures on populations of Typhlodromus pyri (Acari: Phytoseiidae) and other natural enemies in western Oregon vineyards. Biol Control 63:48–55CrossRefGoogle Scholar
  19. Hansen EA, Hansen EA, Funderburk JE, Reitz SR, Ramachandran S, Eger JE, McAuslane H (2003) Within-plant distribution of Frankliniella species (Thysanoptera: Thripidae) and Orius insidiosus (Heteroptera: Anthocoridae) in field pepper. Environ Entomol 32:1035–1044CrossRefGoogle Scholar
  20. Harris C, Abubeker S, Yu M, Leskey T, Zhang A (2015) Semiochemical production and laboratory behavior response of the brown marmorated stink bug, Halyomorpha halys. PLoS ONE 10:e0140876CrossRefPubMedPubMedCentralGoogle Scholar
  21. Harwood J, Yoo H, Greenstone M, Rowley D, O’Neil R (2009) Differential impact of adults and nymphs of a generalist predator on an exotic invasive pest demonstrated by molecular gut-content analysis. Biol Invasions 11:895–903CrossRefGoogle Scholar
  22. Herring JL (1966) The genus Orius of the western hemisphere (Hemiptera: Anthocoridae). Ann Entomol Soc Am 59:1093–1109CrossRefGoogle Scholar
  23. Ho HY, Millar JG (2001) Compounds in metathoracic glands of adults and dorsal abdominal glands of nymphs of the stink bugs, Chlorochroa uhleri, C. sayi, and C. ligata (Hemiptera: Pentatomidae). Zool Stud 40:193–198Google Scholar
  24. 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
  25. Iglinsky W, Rainwater CF (1950) Orius insidiosus, an enemy of a spider mite on cotton. J Econ Entomol 43:567–568CrossRefGoogle Scholar
  26. James DG (2003) Synthetic herbivore-induced plant volatiles as field attractants for beneficial insects. Environ Entomol 32:977–982CrossRefGoogle Scholar
  27. James DG (2005) Further field evaluation of synthetic herbivore-induced plan volatiles as attractants for beneficial insects. J Chem Ecol 31:481–495CrossRefPubMedGoogle Scholar
  28. James DG, Price TS (2004) Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. J Chem Ecol 30:1613–1628CrossRefPubMedGoogle Scholar
  29. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  30. Kelly JL, Hagler JR, Kaplan I (2014) Semiochemical lures reduce emigration and enhance pest control services in open-field predator augmentation. Biol Control 71:70–77CrossRefGoogle Scholar
  31. Khan ZR, James DG, Midega CAO, Pickett JA (2008) Chemical ecology and conservation biological control. Biol Control 45:210–224CrossRefGoogle Scholar
  32. Khrimian A, Zhang A, Weber DC, 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 77:1708–1717CrossRefPubMedGoogle Scholar
  33. Kou R, Tang DS, Chow YS (1989) Alarm pheromone of pentatomid bug, Erthesina fullo Thunberg (Hemiptera: Pentatomidae). J Chem Ecol 15:2695–2702CrossRefPubMedGoogle Scholar
  34. Kuhar TP, Kamminga KL, Whalen J, Dively GP, Brust G, Hooks CRR, Hamilton G, Herbert DA (2012) The pest potential of brown marmorated stink bug on vegetable crops. Plant Health Prog. doi: 10.1094/PHP-2012-0523-01-BR Google Scholar
  35. Lattin JD (1990) Bionomics of the Anthocoridae. Annu Rev Entomol 44:207–231CrossRefGoogle Scholar
  36. Leroy PD, Almohamad R, Attia S, Capella Q, Verheggen FJ, Haubruge E, Francis F (2014) Aphid honeydew: an arrestant and a contact kairomone for Episyrphus balteatus (Diptera: Syrphidae) larvae and adults. Eur J Entomol 111:237–242Google Scholar
  37. Leskey TC, Hamilton GC, Nielsen AL, Polk DF, Rodriguez-Saona C, Bergh CJ, Herbert AD, Kuhar TP, Pfeiffer D, Dively GP, Hooks CRR, Raupp MJ, Shrewsbury PM, Krawczyk G, Shearer PW, Whalen J, Koplinka-Loehr C, Myers E, Inkley D, Hoelmer KA, Lee DH, Wright SE (2012a) Pest status of the brown marmorated stink bug, Halyomorpha halys in the USA. Outlooks Pest Manag 23:218–226CrossRefGoogle Scholar
  38. 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 2012:1–14CrossRefGoogle Scholar
  39. Morrison WRIII, Mathews CR, Leskey TC (2016) Frequency, efficiency, and physical characteristics of predation by generalist predators of brown marmorated stink bug (Hemiptera: Pentatomidae) eggs. Biol Control 97:120–130CrossRefGoogle Scholar
  40. Musser FR, Shelton AM (2003) Predation of Ostrinia nubilalis (Lepidoptera: Crambidae) eggs in sweet corn by generalist predators and the impact of alternative foods. Environ Entomol 32:1131–1138CrossRefGoogle Scholar
  41. Nielsen AL, Hamilton GC (2009) Life history of the invasive species Halyomorpha halys (Hemiptera: Pentatomidae) in northeastern United States. Ann Entomol Soc Am 102:608–616CrossRefGoogle Scholar
  42. Ninkovic V, Al Abassi S, Pettersson J (2001) The influence of aphid-induced plant volatiles on ladybird beetle searching behavior. Biol Control 21:191–195CrossRefGoogle Scholar
  43. Northeastern IPM Center (2016) Where is BMSB? Accessed 15 Oct 2016
  44. Osekre EA, Wright DL, Marois JJ, Mailhot DJ (2008) Predator-prey interactions between Orius insidiosus (Heteroptera: Anthocoridae) and Frankliniella tritici (Thysanoptera: Thripidae) in cotton blooms. J Cotton Sci 201:195–201Google Scholar
  45. Peiffer M, Felton GW (2014) Insights into the saliva of the brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae). PLoS ONE 9(2):e88483CrossRefPubMedPubMedCentralGoogle Scholar
  46. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288CrossRefGoogle Scholar
  47. Reddy GVP, Holopainen JK, Guerrero A (2002) Olfactory responses of Plutella xylostella natural enemies to host pheromone, larval frass, and green leaf cabbage volatiles. J Chem Ecol 28:131–143CrossRefPubMedGoogle Scholar
  48. Reid CD, Lampman RL (1989) Olfactory responses of Orius insidiosus (Hemiptera: Anthocoridae) to volatiles of corn silks. J Chem Ecol 15:1109–1115CrossRefPubMedGoogle Scholar
  49. 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 5:1–13CrossRefGoogle Scholar
  50. Rodriguez-Saona CR, Rodriguez-Saona LE, Frost CJ (2009) Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signaling. J Chem Ecol 35:163–175CrossRefPubMedGoogle Scholar
  51. Rodriguez-Saona C, Kaplan I, Braasch J, Chinnasamy D, Williams L (2011) Field responses of predaceous arthropods to methyl salicylate: a meta-analysis and case study in cranberries. Biol Control 59:294–303CrossRefGoogle Scholar
  52. Rodriguez-Saona C, Blaauw BR, Isaacs R (2012) Manipulation of natural enemies in agroecosystems habitat and semiochemicals for sustainable insect pest control. In: Soloneski S (ed) Integrated pest management and pest control–current and future tactics. InTech, Rijeka, pp 89–126. doi: 10.5772/30375 Google Scholar
  53. Shipp JL, Ramakers PMJ (2004) Biological control of thrips on vegetable crops. In: Heinz KM, Van Driesche RG, Parella MP (eds) Biocontrol in protected culture. Ball Publishing, Batavia, pp 265–276Google Scholar
  54. Soergel DC, Ostiguy N, Fleischer SJ, Troyer RR, Rajotte EG, Krawczyk G (2015) Sunflower as a potential trap crop of Halyomorpha halys (Hemiptera: Pentatomidae) in pepper fields. Environ Entomol 44:1581–1589CrossRefPubMedGoogle Scholar
  55. Solomon D, Dutcher D, Raymond T (2013) Characterization of Halyomorpha halys (brown marmorated stink bug) biogenic volatile organic compound emissions and their role in secondary organic aerosol formation. J Air Waste Manag Assoc 63:1264–1269CrossRefPubMedGoogle Scholar
  56. Teerling CR, Gillespie DR, Borden JH (1993) Utilization of western flower thrips alarm pheromone as a prey-finding kairomone by predators. Can Entomol 125:431–437CrossRefGoogle Scholar
  57. Thaler JS (1999) Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686–688CrossRefGoogle Scholar
  58. Tholl D, Röse USR (2006) Detection and identification of floral scent compounds. In: Dudareva N, Pichersky E (eds) The biology of floral scent. CRC Press, New York, pp 3–25CrossRefGoogle Scholar
  59. Tillman PG (2011) Natural biological control of stink bug (Heteroptera: Pentatomidae) eggs in corn, peanut, and cotton farmscapes in Georgia. Environ Entomol 40:303–314CrossRefGoogle Scholar
  60. Tillman PG, Greenstone MH, Hu JS (2015) Predation of stink bugs (Hemiptera: Pentatomidae) by a complex of predators in cotton and adjoining soybean habitats in Georgia, USA. Fla Entomol 98:1114–1126CrossRefGoogle Scholar
  61. Turlings TC, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253CrossRefPubMedGoogle Scholar
  62. Van Den Boom CEM, Van Beek TA, Posthumus MA, De Groot A, Dicke M (2004) Qualitative and quantitative variation among volatile profiles induced by Tetranychus urticae feeding on plants from various families. J Chem Ecol 30:69–89CrossRefPubMedGoogle Scholar
  63. Woods JL, James DG, Lee JC, Gent DH (2011) Evaluation of airborne methyl salicylate for improved conservation biological control of two-spotted spider mite and hop aphid in Oregon hop yards. Exp Appl Acarol 55:401–416CrossRefPubMedGoogle Scholar
  64. Xu J, Fonseca 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
  65. Yu H, Zhang Y, Wu K, Gao XW, Guo YY (2008) Field-testing of synthetic herbivore-induced plant volatiles as attractants for beneficial insects. Environ Entomol 37:1410–1415CrossRefPubMedGoogle Scholar
  66. Zhu J, Park KC (2005) Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J Chem Ecol 31:1733–1746CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of EntomologyRutgers UniversityNew BrunswickUSA
  2. 2.Departamento de FitossanidadeUNESP/FCAVJaboticabalBrazil
  3. 3.United States Department of AgricultureNational Institute of Food and AgricultureWashingtonUSA

Personalised recommendations