Identification and Characterization of the Pheromones in the Minute Pirate Bug Orius sauteri (Heteroptera: Anthocoridae)

Abstract

The flower bug Orius sauteri is a generalist predator that occurs throughout Japan, and is a promising indigenous natural enemy for micro-pests such as thrips, aphids, and spider mites. We aimed to manipulate the attraction, dispersal, and settlement behavior of Orius bugs using natural chemical substances emitted by the bugs themselves. To identify potential candidates, we screened components in the whole-body extract of O. sauteri based on antennal response and then determined their chemical structure. A gas chromatograph electroantennographic detector (GC/EAD) indicated that the antennae of males responded to two components in the extract of females. GC/mass spectrometry (MS) showed that these two components were octenal and octadienal. Derivatization or GC-FT-IR analysis identified these components as (E)-2-octenal and (E)-2,7-octadienal. To assess the effect of these components on O. sauteri behavior, we conducted two assays. A field bioassay demonstrated that a blend of the two components functioned as a sex pheromone, and a dispersal assay showed that (E)-2-octenal generated a dose-dependent dispersal response. Our study will provide baseline information for enhancing the retention of O. sauteri on important commercial crops to prey on pest species.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

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

    Article  Google Scholar 

  2. Aldrich JR, Oliver JE, Taghizadeh T, Ferreira JTB, Liewehr D (1999) Pheromones and colonization: reassessment of the milkweed bug migration model (Heteroptera: Lygaeidae: Lygaeinae). Chemoecol 9:63–71

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  4. Blum MS (1961) The presence of 2-hexenal in the scent gland of the pentatomid Brochymena quadripustulata. Ann Entomol Soc Am 54:410–412

    CAS  Article  Google Scholar 

  5. Blum MS, Crain RD, Chidester JB (1961) Trans-2-hexenal in the scent gland of the hemipteran Acanthocephala femorata. Nature 189:245–246

    CAS  Article  Google Scholar 

  6. Borges M, Aldrich JR (1992) Instar-specific defensive secretions of stink bugs (Heteroptera: Pentatomidae). Experientia 48:893–896

    CAS  Article  Google Scholar 

  7. Buser HR, Arn H, Guerin P, Rauscher S (1983) Determination of double bond position in mono-unsaturated acetates by mass spectrometry of dimethyl disulfide adducts. Anal Chem 55:818–822

    CAS  Article  Google Scholar 

  8. Carvalho LM, Bueno VHP, Castane C (2011) Olfactory response towards its prey Frankliniella occidentalis of wild and laboratory-reared Orius insidiosus and Orius laevigatus. J Appl Entomol 135:177–183

    Article  Google 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

    CAS  Article  Google Scholar 

  10. Crawley MJ (2005) Statistics, an introduction using R. John Wiley, New York

    Book  Google Scholar 

  11. Furihata S, Tabuchi K, Okudera S, Takahashi A, Hinomoto N, Shimoda M, Yamaguchi T (2019) An efficient method for monitoring predatory minute pirate bug Orius spp. (Hemiptera: Anthocoridae) populations using blue-colored sticky traps. Environ Entomol 48:426–433

    Article  Google Scholar 

  12. Gunawardena NE, Bandumathie MK (1993) Defensive secretion of rice bug, Leptocorisa oratorius Fabricius, (Hemiptera: Coreidae): a unique chemical combination and its toxic, repellent, and alarm properties. J Chem Ecol 19:851–861

    CAS  Article  Google Scholar 

  13. Hock V, Chouinard G, Lucas É, Cormier D, Leskey T, Zhang A (2017) Olfactometer responses of plum curculio Conotrachelus nenuphar (Herbst)(Coleoptera: Curculionidae) to host plant volatiles, synthetic grandisoic acid, and live conspecifics. J Insect Behav 30:475–494. https://doi.org/10.1007/s10905-017-9634-0

    Article  Google Scholar 

  14. Hughes MA, Martini X, Kuhns E, Colee J, Mafra-Neto A, Stelinski LL, Smith JA (2017) Evaluation of repellents for the redbay ambrosia beetle, Xyleborus glabratus, vector of the laurel wilt pathogen. J Appl Entomol 141:653–664

    CAS  Article  Google Scholar 

  15. Imura T, Kamikawa S (2012) Possibility of Tagetes patula L. for banker plants of Orius spp. Ann Rept Kansai Pl Prot 54:163–165

    Article  Google Scholar 

  16. Ishiwatari T (1974) Studies on the scent stink bug (Hemiptera: Pentatomidae) I. alarm pheromone activity. Appl Entomol Zool 9:153–158

    CAS  Article  Google Scholar 

  17. Ishiwatari T (1976) Studies on the scent of stink bugs (Hemiptera: Pentatomidae): II. Aggregation pheromone activity. Appl Entomol Zool 11:38–44

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  19. 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

    CAS  Article  Google Scholar 

  20. Kugel M (1977) The time course of the electroretinogram of compound eyes in insects and its dependence on special recording conditions. J Exp Biol 71:1–6

    CAS  PubMed  Google Scholar 

  21. Leal WS, Kuwahara Y, Matsuyama S, Suzuki T, Ozawa T (1992) GC-FTIR potential for structure elucidation. J Braz Chem Soc 3:25–29

    CAS  Article  Google Scholar 

  22. Levinson HZ, Ilan ARB (1971) Assembling and alerting scents produced by the bedbug Cimex lectularius L. Experientia 27:102–103

    CAS  Article  Google Scholar 

  23. Li S, Tan X, Desneux N, Benelli G, Zhao J, Li X, Zhang F, Gao X, Wang S (2015) Innate positive chemotaxis to pollen from crops and banker plants in predaceous biological control agents: towards new field lures? Sci Rep 5. https://doi.org/10.1038/srep12729

  24. Maeda T, Fujiwara-Tsujii N, Yasui H, Matsuyama S (2016) Female sex pheromone in trails of the minute pirate bug, Orius minutus (L). J Chem Ecol 42:433–443

    CAS  Article  Google Scholar 

  25. Mochizuki M, Yano E (2007) Olfactory response of the anthocorid predatory bug Orius sauteri to thrips-infested eggplants. Entomol Exp Appl 123:57–62

    Article  Google Scholar 

  26. Nagai K (1990) Suppressive effect of Orius sp. (Hemiptera: Anthocoridae) on the population density of Thrips palmi Karny (Thysanoptera: Thripidae) in eggplant in an open field. Jpn J Appl Ent Zool 34:109–114

    Article  Google Scholar 

  27. Nakashima Y, Hirose Y (1999) Trail sex pheromone as a cue for searching mates in an insect predator Orius sauteri. Ecol Entomol 24:115–117

    Article  Google Scholar 

  28. Njihia TN, Torto B, Murungi LK, Irungu J, Mwenda DM, Babin R (2017) Identification of kairomones of second instar nymphs of the variegated coffee bug Antestiopsis thunbergii (Heteroptera: Pentatomidae). Chemoecology 27:239–248

    CAS  Article  Google Scholar 

  29. Noge K (2015) Studies on chemical ecology of the heteropteran scent gland components. J Pestic Sci 40:143–145

    CAS  Article  Google Scholar 

  30. Noge K, Prudic KL, Becerra JX (2012) Defensive roles of (E)-2-alkenals and related compounds in Heteroptera. J Chem Ecol 38:1050–1056

    Article  Google Scholar 

  31. Ogino T, Uehara T, Muraji M, Yamaguchi T, Ichihashi T, Suzuki T, Kainoh Y, Shimoda M (2016) Violet LED light enhances the recruitment of a thrip predator in open fields. Sci Rep 6. https://doi.org/10.1038/srep32302

  32. Ohno K, Takemoto H (1997) Species composition and seasonal occurrence of Orius spp. (Heteroptera: Anthocoridae), predacious natural enemies of Thrips palmi (Thysanoptera: Thripidae), in eggplant fields and surrounding habitats. Appl Entomol Zool 32:27–35

    Article  Google Scholar 

  33. Ohta I, Takeda M (2014) Adult survival of Orius strigicollis (Poppius) on different flowering plants and its development and fecundity on buckwheat flowers. Ann Rept Kansai Pl Prot 56:1–5

    Article  Google Scholar 

  34. R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/

  35. Rahman MM, Lim UT (2017) Evaluation of aggregation and alarm pheromones of Riptortus pedestris (Hemiptera: Alydidae) as a push–pull strategy in soybean fields. Appl Entomol Zool 52:469–479

    CAS  Article  Google Scholar 

  36. Ritz C, Baty F, Streibig JC, Gerhard D (2015) Dose-response analysis using R. PLoS One 10:e0146021

    Article  Google Scholar 

  37. Stepanycheva EA, Petrova MO, Chermenskaya TD, Shamshev IV, Pazyuk IM (2014) The behavioral response of the predatory bug Orius laevigatus Fieber (Heteroptera, Anthocoridae) to synthetic volatiles. Entomol Rev 94:1053–1058

    Article  Google Scholar 

  38. Takai M (1998) Control of insect pests on eggplant using indigenous natural enemies in an open field. I. Seasonal trend of the major insect pests of eggplant and their natural enemies. Bull Kochi Agric Res Cent 7:21–27

    Google Scholar 

  39. Ulrich KR, Feldlaufer MF, Kramer M, Leger RJS (2015) Inhibition of the entomopathogenic fungus Metarhizium anisopliae sensu lato in vitro by the bed bug defensive secretions (E)-2-hexenal and (E)-2-octenal. BioControl 60:517–526

    CAS  Article  Google Scholar 

  40. Ulrich KR, Kramer M, Feldlaufer MF (2016) Ability of bed bug (Hemiptera: Cimicidae) defensive secretions (E)-2-hexenal and (E)-2-octenal to attract adults of the common bed bug Cimex lectularius. Physiol Entomol 41:103–110

    CAS  Article  Google Scholar 

  41. Venables WN, Ripley BD (2002) Modern applied statistics with S. Fourth Edition. Springer, New York. ISBN 0-387-95457-0

    Google Scholar 

  42. Xu X, Enkegaard A (2009) Prey preference of Orius sauteri between western flower thrips and spider mites. Entomol Exp Appl 132:93–98

    Article  Google Scholar 

  43. Yasuda T, Oku K, Higuchi H, Shigehisa S, Okutani-Akamatsu Y, Watanabe T, Takahashi A, Sugeno W, Yamashita M, Fukumoto T, Mochizuki F (2009) Optimization of blends of synthetic sex pheromone components for attraction of the sorghum plant bug Stenotus rubrovittatus (Matsumura)(Heteroptera: Miridae). Appl Entomol Zool 44:611–619

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank Dr. Shigeru Matsuyama at the University of Tsukuba for his kind advice on the synthesis of octadienal and Dr. Nobuyuki Akai and Mr. Masazumi Hayashi at Tokyo University of Agriculture and Technology for supporting the GC/FT-IR analysis. We also thank Mr. Kouhei Terada and Mr. Tomofumi Shibata for supporting the field bioassay. This project was supported by a research grant from the Japan Prize Foundation.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Takuya Uehara.

Electronic supplementary material

Supplementary Fig. 1

Comparison of the attractiveness of 2,7-octadienals synthesized by different pathways. Number of catches were analyzed using the Mann–Whitney U-test (N = 8, P = 0.8282). (PPTX 80 kb)

Supplementary Fig. 2

Schematic diagram of dispersal assay. (PPTX 73 kb)

Supplementary Tables

(PPTX 77 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Uehara, T., Maeda, T., Shimoda, M. et al. Identification and Characterization of the Pheromones in the Minute Pirate Bug Orius sauteri (Heteroptera: Anthocoridae). J Chem Ecol 45, 811–817 (2019). https://doi.org/10.1007/s10886-019-01104-1

Download citation

Keywords

  • Biological control
  • Natural enemy
  • Generalist predator
  • Pesticide
  • Semiochemicals