Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aldrich JR (1988) Chemical ecology of the Heteroptera. Annu Rev Entomol 33:211–238

    Article  Google Scholar 

  • 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 318–363

    Chapter  Google Scholar 

  • 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 13:1031–1036

    Article  CAS  Google Scholar 

  • Aldrich JR, Lusby WR, Marron BE, Nicolaou KC, Hoffmann MP, Wilson LT (1989) Pheromone blends of green stink bugs and possible parasitoid selection. Naturwissenschaften 76:173–175

    Article  CAS  Google Scholar 

  • Aldrich JR, Oliver JE, Shifflet T, Smith CL, Dively GP (2007) Semiochemical investigations of the insidiosus flower bug, Orius insidiosus (Say). J Chem Ecol 33:1477–1493

    Article  CAS  PubMed  Google Scholar 

  • Andow DA (1990) Characterization of predation on egg masses of Ostrinia nubilalis (Lepidoptera: Pyralidae). Ann Entomol Soc Am 83:482–486

    Article  Google Scholar 

  • 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 103:10509–10513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 43:47–54

    Google Scholar 

  • 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 103:109–117

    Article  Google Scholar 

  • Colautti RI, Ricciardi A, Grigorovich IA, MacIsaac HJ (2004) Is invasion success explained by the enemy release hypothesis? Ecol Lett 7:721–733

    Article  Google Scholar 

  • 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 16:310–317

    Article  Google Scholar 

  • 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 30:945–964

    Article  CAS  PubMed  Google Scholar 

  • Colazza S, Cusumano A, Giudice DL, Peri E (2014) Chemo-orientation responses in hymenopteran parasitoids induced by substrate-borne semiochemicals. BioControl 59:1–17

    Article  CAS  Google Scholar 

  • De Boer JG, Dicke M (2004) The role of methyl salicylate in prey searching behavior of the predatory mite Phytoseiulus persimilis. J Chem Ecol 30:255–271

    Article  PubMed  Google Scholar 

  • De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlonson JH, Paré PW (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573

    Article  Google Scholar 

  • 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 37:1854–1865

    Article  PubMed  Google Scholar 

  • 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 30:1257–1269

    Article  CAS  PubMed  Google Scholar 

  • 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 63:48–55

    Article  CAS  Google Scholar 

  • 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 32:1035–1044

    Article  Google Scholar 

  • 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:e0140876

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 11:895–903

    Article  Google Scholar 

  • Herring JL (1966) The genus Orius of the western hemisphere (Hemiptera: Anthocoridae). Ann Entomol Soc Am 59:1093–1109

    Article  Google Scholar 

  • 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 40:193–198

    CAS  Google Scholar 

  • 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 105:225–237

    Google Scholar 

  • Iglinsky W, Rainwater CF (1950) Orius insidiosus, an enemy of a spider mite on cotton. J Econ Entomol 43:567–568

    Article  Google Scholar 

  • James DG (2003) Synthetic herbivore-induced plant volatiles as field attractants for beneficial insects. Environ Entomol 32:977–982

    Article  CAS  Google Scholar 

  • James DG (2005) Further field evaluation of synthetic herbivore-induced plan volatiles as attractants for beneficial insects. J Chem Ecol 31:481–495

    Article  CAS  PubMed  Google Scholar 

  • James DG, Price TS (2004) Field-testing of methyl salicylate for recruitment and retention of beneficial insects in grapes and hops. J Chem Ecol 30:1613–1628

    Article  CAS  PubMed  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Kelly JL, Hagler JR, Kaplan I (2014) Semiochemical lures reduce emigration and enhance pest control services in open-field predator augmentation. Biol Control 71:70–77

    Article  CAS  Google Scholar 

  • Khan ZR, James DG, Midega CAO, Pickett JA (2008) Chemical ecology and conservation biological control. Biol Control 45:210–224

    Article  CAS  Google Scholar 

  • 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 77:1708–1717

    Article  CAS  PubMed  Google Scholar 

  • Kou R, Tang DS, Chow YS (1989) Alarm pheromone of pentatomid bug, Erthesina fullo Thunberg (Hemiptera: Pentatomidae). J Chem Ecol 15:2695–2702

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Lattin JD (1990) Bionomics of the Anthocoridae. Annu Rev Entomol 44:207–231

    Article  Google Scholar 

  • 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 111:237–242

    Google Scholar 

  • 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 23:218–226

    Article  Google Scholar 

  • 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 2012:1–14

    Article  Google Scholar 

  • 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 97:120–130

    Article  Google Scholar 

  • 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 32:1131–1138

    Article  Google Scholar 

  • Nielsen AL, Hamilton GC (2009) Life history of the invasive species Halyomorpha halys (Hemiptera: Pentatomidae) in northeastern United States. Ann Entomol Soc Am 102:608–616

    Article  Google Scholar 

  • Ninkovic V, Al Abassi S, Pettersson J (2001) The influence of aphid-induced plant volatiles on ladybird beetle searching behavior. Biol Control 21:191–195

    Article  Google Scholar 

  • Northeastern IPM Center (2016) Where is BMSB? http://www.stopbmsb.org/where-is-bmsb/. Accessed 15 Oct 2016

  • 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 201:195–201

    Google Scholar 

  • Peiffer M, Felton GW (2014) Insights into the saliva of the brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae). PLoS ONE 9(2):e88483

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 52:273–288

    Article  Google Scholar 

  • 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 28:131–143

    Article  CAS  PubMed  Google Scholar 

  • Reid CD, Lampman RL (1989) Olfactory responses of Orius insidiosus (Hemiptera: Anthocoridae) to volatiles of corn silks. J Chem Ecol 15:1109–1115

    Article  CAS  PubMed  Google Scholar 

  • 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 5:1–13

    Article  Google Scholar 

  • 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 35:163–175

    Article  CAS  PubMed  Google Scholar 

  • 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 59:294–303

    Article  CAS  Google Scholar 

  • 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 

  • 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 265–276

    Google Scholar 

  • 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 44:1581–1589

    Article  CAS  PubMed  Google Scholar 

  • 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 63:1264–1269

    Article  CAS  PubMed  Google Scholar 

  • Teerling CR, Gillespie DR, Borden JH (1993) Utilization of western flower thrips alarm pheromone as a prey-finding kairomone by predators. Can Entomol 125:431–437

    Article  Google Scholar 

  • Thaler JS (1999) Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature 399:686–688

    Article  CAS  Google Scholar 

  • 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 3–25

    Chapter  Google Scholar 

  • Tillman PG (2011) Natural biological control of stink bug (Heteroptera: Pentatomidae) eggs in corn, peanut, and cotton farmscapes in Georgia. Environ Entomol 40:303–314

    Article  Google Scholar 

  • 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 98:1114–1126

    Article  Google Scholar 

  • Turlings TC, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253

    Article  CAS  PubMed  Google Scholar 

  • 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 30:69–89

    Article  PubMed  Google Scholar 

  • 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 55:401–416

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Fonseca DM, Hamilton GC, Hoelmer KA, Nielsen AL (2014) Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biol Invasions 16:153–166

    Article  CAS  Google Scholar 

  • 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 37:1410–1415

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Park KC (2005) Methyl salicylate, a soybean aphid-induced plant volatile attractive to the predator Coccinella septempunctata. J Chem Ecol 31:1733–1746

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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.

Funding

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.

Author information

Authors and Affiliations

  1. Department of Entomology, Rutgers University, 96 Lipman Drive, New Brunswick, NJ, 08901, USA

    Diego F. Fraga, George C. Hamilton, Anne L. Nielsen & Cesar Rodriguez-Saona

  2. Departamento de Fitossanidade, UNESP/FCAV, km 5 Via de Acesso Professor Paulo Donato Castellane, Jaboticabal, SP, 14884-900, Brazil

    Diego F. Fraga & Antonio C. Busoli

  3. United States Department of Agriculture, National Institute of Food and Agriculture, 1400 Independence Ave., Washington, DC, 20250, USA

    Joyce Parker

Authors
  1. Diego F. Fraga
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joyce Parker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Antonio C. Busoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. George C. Hamilton
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anne L. Nielsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cesar Rodriguez-Saona
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Diego F. Fraga.

Ethics declarations

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.

Additional information

Communicated by T. Haye.

Special Issue: The brown marmorated stink bug Halyomorpha halys an emerging pest of global concern.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fraga, D.F., Parker, J., Busoli, A.C. et al. Behavioral responses of predaceous minute pirate bugs to tridecane, a volatile emitted by the brown marmorated stink bug. J Pest Sci 90, 1107–1118 (2017). https://doi.org/10.1007/s10340-016-0825-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-016-0825-9

Keywords

Search

Navigation