Development of Thrips Repellents, and Their Combined Application with Aggregation Pheromones in a Push–Pull Strategy to Control Frankliniella occidentalis
Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Test Insects and Plants
2.2. Chemicals
2.3. Oviposition Selection in Cage Experiments
2.4. Control Efficacy in Field Trials
2.5. Push–Pull Strategy with Thrips Repellents and Aggregation Pheromone Lures
2.6. Data Analysis
3. Results
3.1. The Effects of Repellent Sprays on F. occidentalis Oviposition
3.2. Control Efficacy of Repellent Sprays in Field Trials
3.3. Control Efficacy of Push–Pull Strategy with Thrips Repellents and Aggregation Pheromone Lures
4. Discussion
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Reitz, S.R.; Gao, Y.L.; Kirk, W.D.J.; Hoddle, M.S.; Leiss, K.A.; Funderburk, J.E. Invasion biology, ecology, and management of western flower thrips. Annu. Rev. Entomol. 2020, 65, 17–37. [Google Scholar] [CrossRef]
- Mound, L.A. Thysanoptera: Diversity and interactions. Annu. Rev. Entomol. 2005, 50, 247–269. [Google Scholar] [CrossRef]
- Whitfield, A.E.; Ullman, D.E.; German, T.L. Tospovirus-thrips interactions. Annu. Rev. Phytopathol. 2005, 43, 459–489. [Google Scholar] [CrossRef]
- Broughton, S.; Herron, G.A. Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) chemical control: Insecticide efficacy associated with the three consecutive spray strategy. Aust. J. Entomol. 2007, 46, 140–145. [Google Scholar] [CrossRef]
- Funderburk, J. Management of the western flower thrips (Thysanoptera: Thripidae) in fruiting vegetables. Fla. Entomol. 2009, 92, 1–6. [Google Scholar] [CrossRef]
- Wu, S.; Tang, L.; Fang, F.; Li, D.; Yuan, X.; Lei, Z.; Gao, Y. Screening, efficacy and mechanisms of microbial control agents against sucking pest insects as thrips. Adv. Insect Physiol. 2018, 55, 201–219. [Google Scholar] [CrossRef]
- Wang, Z.-H.; Gong, Y.-J.; Jin, G.-H.; Li, B.-Y.; Chen, J.-C.; Kang, Z.-J.; Zhu, L.; Gao, Y.-L.; Reitz, S.; Wei, S.-J. Field-evolved resistance to insecticides in the invasive western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) in China. Pest. Manag. Sci. 2016, 72, 1440–1444. [Google Scholar] [CrossRef] [PubMed]
- Gao, Y.L.; Lei, Z.R.; Reitz, S.R. Western flower thrips resistance to insecticides: Detection, mechanisms and management strategies. Pest. Manag. Sci. 2012, 68, 1111–1121. [Google Scholar] [CrossRef]
- Li, D.; Shang, X.; Reitz, S.; Nauen, R.; Lei, Z.; Lee, S.H.; Gao, Y. Field resistance to spinosad in western flower thrips Frankliniella occidentalis (Thysanoptera: Thripidae). J. Integr. Agr. 2016, 15, 2803–2808. [Google Scholar] [CrossRef]
- Cloyd, R.A. Western flower thrips (Thysanoptera: Thripidae) and insecticide resistance: An overview and strategies to mitigate insecticide resistance development. J. Entomol. Sci. 2016, 51, 257–273. [Google Scholar] [CrossRef]
- Dudareva, N.; Negre, F.; Nagegowda, D.A.; Orlova, I. Plant volatiles: Recent advances and future perspectives. Crit. Rev. Plant Sci. 2006, 25, 417–440. [Google Scholar] [CrossRef]
- Shrivastava, G.; Rogers, M.; Wszelaki, A.; Panthee, D.R.; Chen, F. Plant volatiles-based insect pest management in organic farming. Crit. Rev. Plant Sci. 2010, 29, 123–133. [Google Scholar] [CrossRef]
- Beck, J.J.; Torto, B.; Vannette, R.L. Eavesdropping on plant-insect-microbe chemical communications in agricultural ecology: A virtual issue on semiochemicals. J. Agric. Food Chem. 2017, 65, 5101–5103. [Google Scholar] [CrossRef]
- Deletre, E.; Schatz, B.; Bourguet, D.; Chandre, F.; Williams, L.; Ratnadass, A.; Martin, T. Prospects for repellent in pest control: Current developments and future challenges. Chemoecology 2016, 26, 127–142. [Google Scholar] [CrossRef]
- Teulon, D.A.J.; Davidson, M.M.; Perry, N.B.; Nielsen, M.C.; Castañé, C.; Bosch, D.; Riudavets, J.; van Tol, R.W.H.M.; de Kogel, W.J. Methyl isonicotinate—A non-pheromone thrips semiochemical—And its potential for pest management. Int. J. Trop. Insect Sci. 2017, 37, 50–56. [Google Scholar] [CrossRef]
- Davidson, M.M.; Perry, N.B.; Larsen, L.; Green, V.C.; Butler, R.C.; Teulon, D.A.J. 4-Pyridyl carbonyl compounds as thrips lures: Effectiveness for western flower thrips in Y-tube bioassays. J. Agric. Food Chem. 2008, 56, 6554–6561. [Google Scholar] [CrossRef] [PubMed]
- Koschier, E.H. Essential oil compounds for thrips control—A review. Nat. Prod. Commun. 2008, 3, 1171–1182. [Google Scholar] [CrossRef]
- Teulon, D.A.J.; Castane, C.; Nielsen, M.C.; Elsayed, A.M.; Davidson, M.M.; Gardnergee, R.; Poulton, J.; Kean, A.M.; Hall, C.; Butler, R.C. Evaluation of new volatile compounds as lures for western flower thrips and onion thrips in New Zealand and Spain. N. Z. Plant Prot. 2014, 67, 175–183. [Google Scholar] [CrossRef]
- Steenbergen, M.; Abd-El-Haliem, A.; Bleeker, P.; Dicke, M.; Escobar-Bravo, R.; Cheng, G.; Haring, M.A.; Kant, M.R.; Kappers, I.; Klinkhamer, P.G.L.; et al. Thrips advisor: Exploiting thrips-induced defences to combat pests on crops. J. Exp. Bot. 2018, 69, 1837–1848. [Google Scholar] [CrossRef] [PubMed]
- Kirk, W.D.J.; de Kogel, W.J.; Koschier, E.H.; Teulon, D.A.J. Semiochemicals for thrips and their use in pest management. Annu. Rev. Entomol. 2021, 66, 101–119. [Google Scholar] [CrossRef] [PubMed]
- Koschier, E.H.; De Kogel, W.J.; Visser, J.H. Assessing the attractiveness of volatile plant compounds to western flower thrips Frankliniella occidentalis. J. Chem. Ecol. 2000, 26, 2643–2655. [Google Scholar] [CrossRef]
- Chermenskaya, T.D.; Burov, V.N.; Maniar, S.P.; Pow, E.M.; Roditakis, N.; Selytskaya, O.G.; Shamshev, I.V.; Wadhams, L.J.; Woodcock, C.M. Behavioural responses of western flower thrips, Frankliniella occidentalis (Pergande), to volatiles from three aromatic plants. Insect Sci. Appl. 2001, 21, 67–72. [Google Scholar] [CrossRef]
- Avellaneda, J.; Díaz, M.; Coy-Barrera, E.; Rodríguez, D.; Osorio, C. Rose volatile compounds allow the design of new control strategies for the western flower thrips (Frankliniella occidentalis). J. Pest. Sci. 2021, 94, 129–142. [Google Scholar] [CrossRef]
- Du, J.; Song, X.Y.; Shi, X.B.; Tang, X.; Chen, J.B.; Zhang, Z.H.; Chen, G.; Zhang, Z.; Zhou, X.G.; Liu, Y.; et al. NSs, the silencing suppressor of Tomato Spotted Wilt Orthotospovirus, interferes with JA-regulated host terpenoids expression to attract Frankliniella occidentalis. Front. Microbiol. 2020, 11, 590451. [Google Scholar] [CrossRef]
- Wu, X.; Xu, S.; Zhao, P.; Zhang, X.; Yao, X.; Sun, Y.; Fang, R.; Ye, J. The Orthotospovirus nonstructural protein NSs suppresses plant MYC-regulated jasmonate signaling leading to enhanced vector attraction and performance. PLoS Pathog. 2019, 15, e1007897. [Google Scholar] [CrossRef]
- Sadeh, D.; Nitzan, N.; Shachter, A.; Ghanim, M.; Dudai, N. Rosemary-whitefly interaction: A continuum of repellency and volatile combinations. J. Econ. Entomol. 2019, 112, 616–624. [Google Scholar] [CrossRef]
- Hori, M. Repellency of rosemary oil against Myzus persicae in a laboratory and in a screenhouse. J. Chem. Ecol. 1998, 24, 1425–1432. [Google Scholar] [CrossRef]
- Hori, M.; Komatsu, H. Repellency of rosemary oil and its components against onion aphid, Neotoxoptera formosana (Takahashi) (Homoptera: Aphididae). Appl. Entomol. Zool. 1997, 32, 303–310. [Google Scholar] [CrossRef]
- Dardouri, T.; Gomez, L.; Schoeny, A.; Costagliola, G.; Gautier, H. Behavioural response of green peach aphid Myzus persicae (Sulzer) to volatiles from different rosemary (Rosmarinus officinalis L.) clones. Agr. Forest Entomol. 2019, 21, 336–345. [Google Scholar] [CrossRef]
- Zhang, Z.-Q.; Sun, X.-L.; Xin, Z.-J.; Luo, Z.-X.; Gao, Y.; Bian, L.; Chen, Z.-M. Identification and field evaluation of non-host volatiles disturbing host location by the tea geometrid, Ectropis obliqua. J. Chem. Ecol. 2013, 39, 1284–1296. [Google Scholar] [CrossRef]
- Zhang, Z.; Luo, Z.; Gao, Y.; Bian, L.; Sun, X.; Chen, Z. Volatiles from non-host aromatic plants repel tea green leafhopper Empoasca vitis. Entomol. Exp. Appl. 2014, 153, 156–169. [Google Scholar] [CrossRef]
- Li, X.; Zhang, Z.; Hafeez, M.; Huang, J.; Zhang, J.; Wang, L.; Lu, Y. Rosmarinus officinialis L. (Lamiales: Lamiaceae), a promising repellent plant for thrips management. J. Econ. Entomol. 2021, 114, 131–141. [Google Scholar] [CrossRef]
- Cook, S.M.; Khan, Z.R.; Pickett, J.A. The use of push-pull strategies in integrated pest management. Annu. Rev. Entomol. 2007, 52, 375–400. [Google Scholar] [CrossRef] [PubMed]
- Hassanali, A.; Herren, H.; Khan, Z.R.; Pickett, J.A.; Woodcock, C.M. Integrated pest management: The push-pull approach for controlling insect pests and weeds of cereals, and its potential for other agricultural systems including animal husbandry. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008, 363, 611–621. [Google Scholar] [CrossRef]
- van Tol, R.W.H.M.; James, D.E.; Kogel, W.J.d.; Teulon, D.A.J. Plant odours with potential for a push-pull strategy to control the onion thrips, Thrips tabaci. Entomol. Exp. Appl. 2007, 122, 69–76. [Google Scholar] [CrossRef]
- Kim, C.Y.; Khan, F.; Kim, Y. A push-pull strategy to control the western flower thrips, Frankliniella occidentalis, using alarm and aggregation pheromones. PLoS ONE 2023, 18, e0279646. [Google Scholar] [CrossRef]
- Hamilton, J.G.C.; Hall, D.R.; Kirk, W.D.J. Identification of a male-produced aggregation pheromone in the western flower thrips Frankliniella occidentalis. J. Chem. Ecol. 2005, 31, 1369–1379. [Google Scholar] [CrossRef] [PubMed]
- Broughton, S.; Cousins, D.A.; Rahman, T. Evaluation of semiochemicals for their potential application in mass trapping of Frankliniella occidentalis (Pergande) in roses. Crop Prot. 2015, 67, 130–135. [Google Scholar] [CrossRef]
- Sampson, C.; Kirk, W.D.J. Can mass trapping reduce thrips damage and is it economically viable? Management of the western flower thrips in strawberry. PLoS ONE 2013, 8, e80787. [Google Scholar] [CrossRef]
- Covaci, A.; Oltean, I.; Pop, A. Evaluation of pheromone lure as mass-trapping tools for western flower thrips. Bull. UASVM Agric. 2012, 69, 333–334. [Google Scholar] [CrossRef]
- Li, X.; Geng, S.; Zhang, Z.; Zhang, J.; Li, W.; Huang, J.; Lin, W.; Bei, Y.; Lu, Y. Species-specific aggregation pheromones contribute to coexistence in two closely related thrips species. Bull. Entomol. Res. 2019, 109, 119–126. [Google Scholar] [CrossRef] [PubMed]
- Lin, Q.-C.; Chen, H.; Babendreier, D.; Zhang, J.-P.; Zhang, F.; Dai, X.-Y.; Sun, Z.-W.; Shi, Z.-P.; Dong, X.-L.; Wu, G.-A.; et al. Improved control of Frankliniella occidentalis on greenhouse pepper through the integration of Orius sauteri and neonicotinoid insecticides. J. Pest. Sci. 2021, 94, 101–109. [Google Scholar] [CrossRef]
- Schroeder, R.; Hilker, M. The relevance of background odor in resource location by insects: A behavioral approach. Bioscience 2008, 58, 308–316. [Google Scholar] [CrossRef]
- Koschier, E.H.; Nielsen, M.C.; Spangl, B.; Davidson, M.M.; Teulon, D.A.J. The effect of background plant odours on the behavioural responses of Frankliniella occidentalis to attractive or repellent compounds in a Y-tube olfactometer. Entomol. Exp. Appl. 2017, 163, 160–169. [Google Scholar] [CrossRef]
- Mercier, B.; Prost, J.; Prost, M. The essential oil of turpentine and its major volatile fraction (α- and β-pinenes): A review. Int. J. Occup. Med. Environ. Health 2009, 22, 331–342. [Google Scholar] [CrossRef]
- Haselton, A.T.; Acevedo, A.; Kuruvilla, J.; Werner, E.; Kiernan, J.; Dhar, P. Repellency of α-pinene against the house fly, Musca domestica. Phytochemistry 2015, 117, 469–475. [Google Scholar] [CrossRef]
- Koc, S.; Cengiz, A.; Polat, B.; Kahraman Kokten, S.; Gultekin, Z.N.; Caliskan, C.; Tufan-Cetin, O.; Cetin, H. Evaluating the repellent effects of major essential oil components (Lamiaceae) on brown dog tick Rhipicephalus sanguineus sensu lato using the larval repellent activity test. Vet. Parasitol. 2025, 333, 110361. [Google Scholar] [CrossRef]
- Feng, Y.-X.; Lu, X.-X.; Du, Y.-S.; Zhang, J.-W.; Almaz, B.; Zeng, D.; Du, S.-S. Synergized potential, insecticidal and repellent activity of essential oils from two Rhododendron species against three stored product insects. J. Essent. Oil Res. 2023, 35, 91–101. [Google Scholar] [CrossRef]
- Lv, J.Y.; Meng, Z.J.; Deng, Y.N.; Li, Y.Y.; Li, X.S.; Yan, S.C. Screening and identification of two repellent active volatiles to Hyphantria cunea. J. Pest. Sci. 2025, 98, 1305–1316. [Google Scholar] [CrossRef]
- Usha Rani, P.; Madhusudhanamurthy, J.; Sreedhar, B. Dynamic adsorption of α-pinene and linalool on silica nanoparticles for enhanced antifeedant activity against agricultural pests. J. Pest. Sci. 2014, 87, 191–200. [Google Scholar] [CrossRef]
- Jaffar, S.; Lu, Y. Toxicity of some essential oils constituents against oriental fruit fly, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Insects 2022, 13, 954. [Google Scholar] [CrossRef] [PubMed]
- Deletre, E.; Matu, F.; Murungi, L.; Mohamed, S. Repellency potential of tomato herbivore-induced volatiles against the greenhouse whitefly (Trialeurodes vaporariorum) (Hemiptera: Aleyrodidae). J. Econ. Entomol. 2022, 115, 565–572. [Google Scholar] [CrossRef] [PubMed]
- Sun, Z.X.; Ma, R.X.; Hu, J.; Chen, Y.P.; Peng, C.; Li, D.G.; Zhang, J.T.; Shen, M.L.; Gui, F.R. Repellent and insecticidal effects of Rosmarinus officinalis and its volatiles on Tuta absoluta. Entomol. Gen. 2024, 44, 297–306. [Google Scholar] [CrossRef]
- Tsuro, M.; Uefune, M.; Iwamoto, A.; Otagaki, S. Transgenic torenia plant emitting 1,8-cineole from petals repels thrips. Vitr. Cell. Dev. Biol.-Plant 2025. [Google Scholar] [CrossRef]
- Lamy, F.C.; Poinsot, D.; Cortesero, A.M.; Dugravot, S. Artificially applied plant volatile organic compounds modify the behavior of a pest with no adverse effect on its natural enemies in the field. J. Pest. Sci. 2017, 90, 611–621. [Google Scholar] [CrossRef]



| Greenhouses | Initial Number per Flower | Number of Thrips per Flower | Control Efficacy (%) | ||||
|---|---|---|---|---|---|---|---|
| Day 1 | Day 2 | Day 3 | Day 1 | Day 2 | Day 3 | ||
| Push–pull strategy | 0.33 ± 0.11 | 0.28 ± 0.11 | 0.35 ± 0.09 | 0.39 ± 0.10 | 81.95 ± 7.06 | 71.08 ± 10.41 | 79.90 ± 8.52 |
| Thrips repellent only | 0.71 ± 0.20 | 1.00 ± 0.76 | 1.29 ± 0.74 | 1.72 ± 0.54 | 77.70 ± 6.71 | 75.07 ± 4.64 | 70.30 ± 4.62 |
| Control | 0.23 ± 0.07 | 1.33 ± 0.20 | 1.82 ± 0.64 | 1.34 ± 0.20 | - | - | - |
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Li, X.; Pan, Y.; Wang, Y.; Wang, Y.; Zhang, Z.; Lu, Y. Development of Thrips Repellents, and Their Combined Application with Aggregation Pheromones in a Push–Pull Strategy to Control Frankliniella occidentalis. Insects 2025, 16, 1137. https://doi.org/10.3390/insects16111137
Li X, Pan Y, Wang Y, Wang Y, Zhang Z, Lu Y. Development of Thrips Repellents, and Their Combined Application with Aggregation Pheromones in a Push–Pull Strategy to Control Frankliniella occidentalis. Insects. 2025; 16(11):1137. https://doi.org/10.3390/insects16111137
Chicago/Turabian StyleLi, Xiaowei, Yiming Pan, Yunxu Wang, Yaru Wang, Zhijun Zhang, and Yaobin Lu. 2025. "Development of Thrips Repellents, and Their Combined Application with Aggregation Pheromones in a Push–Pull Strategy to Control Frankliniella occidentalis" Insects 16, no. 11: 1137. https://doi.org/10.3390/insects16111137
APA StyleLi, X., Pan, Y., Wang, Y., Wang, Y., Zhang, Z., & Lu, Y. (2025). Development of Thrips Repellents, and Their Combined Application with Aggregation Pheromones in a Push–Pull Strategy to Control Frankliniella occidentalis. Insects, 16(11), 1137. https://doi.org/10.3390/insects16111137

