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Analysis of seasonal and annual field-evolved insecticide resistance in populations of Thrips hawaiiensis in banana orchards

  • Buli FuEmail author
  • Haiyan Qiu
  • Qiang Li
  • Liangde Tang
  • Dongqiang Zeng
  • Kui LiuEmail author
  • Yulin Gao
Original Paper
  • 75 Downloads

Abstract

Every season over the past decade, efficacious thrips insecticides have been commonly applied for control of Thrips hawaiiensis on banana crops in China. For effective thrips control, some insecticides have been used extensively against the thrips in numerous banana plantations. This study aims to examine the current resistance status and the dynamics regarding the changing frequencies of resistance in the field T. hawaiiensis populations. A total of 13 field samples from banana orchards (Chengmai, Lingao, Dongfang and Ledong located in Hainan Province, China) were collected monthly in 2014 to 2017, and selected individuals were used in bioassays assessing insecticide resistance and metabolic enzyme activity compared to a laboratory-susceptible strain. In 2014, the initial resistance survey found that all sampled populations were susceptible to spirotetramat and cyantraniliprole, while Lingao and Chengmai population showed a moderate resistance to imidacloprid, acetamiprid, abamectin and spinetoram. Further, seasonal and annual analysis of resistance dynamics with imidacloprid, abamectin and spinetoram demonstrated that resistance in field populations of T. hawaiiensis developed quickly within a season (from April to August 2016), but resistance was unstable over subsequent seasons (April 2015, 2016 and 2017). Moreover, synergism experiments using enzyme inhibitors together with metabolic enzyme assays revealed that field-evolved insecticide resistance in T. hawaiiensis was closely associated with the elevated metabolic enzymes. The observed resistance increase within a season was attributed mainly to the intense use of these insecticides and short generation time of thrips. These findings suggest that a rotation system using efficacious thrips insecticides should be implemented for sustainable thrips control to reduce the potential of resistance development.

Keywords

Thrips hawaiiensis Insecticide resistance Synergism Metabolic enzymes Pest control 

Notes

Acknowledgements

We are grateful to Shanguang Li, Xiya Xia, Yantang Sun and Haifeng Jin for their help with the collection of the field population and their assistance in the bioassays. This research was supported by the National Key Research and Development Program of China (Project No. 2017YFD0202100) and partly supported by the Special Fund for Basic Scientific Research of Central Public Research Institutes of China (Project Nos. 1630042017010 and 1630042019007). We would also like to acknowledge the anonymous reviewers for their constructive and valuable comments.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Research involving human participants and/or animals

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

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

10340_2019_1112_MOESM1_ESM.docx (15 kb)
Supplementary material 1 (DOCX 15 kb)

References

  1. Atakan E, Olculu M, Pehlivan S, Satar S (2015) A new thrips species recorded in Turkey: Thrips hawaiiensis (Morgan, 1913) (Thysanoptera: Thripidae). Turk Entomol Bult 2:77–84Google Scholar
  2. Bao WX, Narai Y, Nakano A, Kaneda T, Murai T, Sonoda S (2014) Spinosad resistance of melon thrips, Thrips palmiis conferred by G275E mutation in α6 subunit of nicotinic acetylcholine receptor and cytochrome P450 detoxification. Pestic Biochem Physiol 112:51–55CrossRefGoogle Scholar
  3. Bao WX, Kataoka Y, Fukada K (2015) Imidacloprid resistance of melon thrips, Thrips palmi, is conferred by CYP450-mediated detoxification. J Pestic Sci 40:65–68CrossRefGoogle Scholar
  4. Bielza P (2008) Insecticide resistance management strategies against the western flower thrips, Frankliniella occidentalis. Pest Manag Sci 64:1131–1138CrossRefGoogle Scholar
  5. Bielza P, Guillén J (2015) Cyantraniliprole: a valuable tool for Frankliniella occidentalis (Pergande) management. Pest Manag Sci 71(8):1068–1074CrossRefGoogle Scholar
  6. Bielza P, Quinto V, Contreras J, Torne M, Martin A, Espinosa PJ (2007) Resistance to spinosad in the western flower thrips, Frankliniella occidentalis (Pergande), in greenhouses of south-eastern Spain. Pest Manag Sci 63(7):682–687CrossRefGoogle Scholar
  7. Cao Y, Zhi JR, Zhang RZ, Li C, Liu Y, Lv ZY, Gao YL (2017) Different population performance of Frankliniella occidentalis and Thrips hawaiiensis on flowers of two horticultural plants. J Pest Sci 3:1–13Google Scholar
  8. Chen X, Yuan L, Du Y, Zhang Y, Wang J (2011) Cross-resistance and biochemical mechanisms of abamectin resistance in the western flower thrips, Frankliniella occidentalis. Pestic Biochem Physio 101:34–38CrossRefGoogle Scholar
  9. Espinosa PJ, Bielza P, Contreras J, Lacasa A (2002a) Insecticide resistance in field populations of Frankliniella occidentalis (Pergande) in Murcia (south-east Spain). Pest Manag Sci 58:967–971CrossRefGoogle Scholar
  10. Espinosa PJ, Bielza P, Contreras J, Lacasa A (2002b) Field and laboratory selection of Frankliniella occidentalis (Pergande) for resistance to insecticides. Pest Manag Sci 58: 920-927CrossRefGoogle Scholar
  11. Fu BL, Tang LD, Qiu HY, Liu JF, Zeng DQ, Xie YX, Zeng DQ, Liu K (2016) Screening of high effect and low toxicity insecticides for controlling Thrips hawaiiensis (Morgan). Chinese Journal of Fruit Science 33:257–267Google Scholar
  12. Fu BL, Li Q, Xia XY, Tang LD, Qiu HY, Xie YX, Zeng DQ, Liu K (2017) Moderate resistance to spinetoram reduces the fitness of Thrips hawaiiensis (Thysanoptera: Thripidae). Acta Entomol Sin 60(2):180–188Google Scholar
  13. Fu BL, Li Q, Qiu HY, Tang LD, Zeng DQ, Liu K, Gao YL (2018a) Resistance development, stability, cross-resistance potential, biological fitness and biochemical mechanisms of spinetoram resistance in the Thrips hawaiiensis (Thysanoptera: Thripidae). Pest Manag Sci 74:1564–1574CrossRefGoogle Scholar
  14. Fu BL, Li Q, Qiu HY, Tang LD, Zeng DQ, Liu K, Gao YL (2018b) Oviposition, feeding preference and biological performance of Thrips hawaiiensis on four host plants with and without supplemental foods. Arthropod-Plant Inte.  https://doi.org/10.1007/s11829-018-9647-4 Google Scholar
  15. Gao YL, Reitz SR, Wang J, Tamez-Guerra P, Wang ED, Xu XN, Lei ZR (2012a) Potential use of the fungus Beauveria bassiana against the western flower thrips Frankliniella occidentalis without reducing the effectiveness of its natural predator Orius sauteri (Hemiptera: Anthocoridae). Biocontrol Sci Technol 22(7):803–812CrossRefGoogle Scholar
  16. Gao YL, Lei ZR, Reitz SR (2012b) Western flower thrips resistance to insecticides: detection, mechanisms, and management strategies. Pest Manag Sci 68:1111–1121CrossRefGoogle Scholar
  17. Goldarazena A (2011) First record of Thrips hawaiiensis (Morgan, 1913) (Thysanoptera: Thripidae), an Asian pest thrips in Spain. OEPP/EPPO Bulletin 41:170–173CrossRefGoogle Scholar
  18. Herron GA, Langfield BJ, Tomlinson TM, Mo J (2014) Dose-response testing of Australian populations of onion thrips. Aust Entomol 50:418–423CrossRefGoogle Scholar
  19. Hou W, Liu Q, Tian L, Wu Q, Zhang Y, Xie W, Wang S, Miguel KS, Funderburk J, Scott JG (2014) The α6 nicotinic acetylcholine receptor subunit of Frankliniella occidentalis is not involved in resistance to spinosad. Pestic Biochem Physiol 111:60–67CrossRefGoogle Scholar
  20. Huseth A, Chappell T, Langdon K, Morsello S, Martin S, Greene J, Herbert A, Jacobson A, Reay-Jones F, Reed T, Reisig D, Roberts P, Smith R, Kennedy G (2016) Frankliniella fusca resistance to neonicotinoid insecticides: an emerging challenge for cotton pest management in the eastern United States. Pest Manag Sci 72:1934–1945CrossRefGoogle Scholar
  21. Immaraju JA, Paine TD, Bethke JA, Robb KL, Newman JP (1992) Western flower thrips (Thysanoptera: Thripidae) resistance to insecticides in coastal California greenhouses. J Econ Entomol 85(1):9–14CrossRefGoogle Scholar
  22. Jensen SE (1998) Acetylcholinesterase activity associated with methiocarb resistance in a strain of western flower thrips, Frankliniella occidentalis (Pergande). Pestic Biochem Physiol 61:191–200CrossRefGoogle Scholar
  23. Jensen SE (2000) Mechanisms associated with methiocarb resistance in Frankliniella occidentalis (Thysanoptera: Thripidae). J Econ Entomol 93:464–471CrossRefGoogle Scholar
  24. Meng X, Xie Z, Zhang N, Ji C, Dong F, Qian K, Wang J (2018) Molecular cloning and characterization of GABA receptor and GluCl subunits in the western flower thrips, Frankliniella occidentalis. Pestic Biochem Physiol.  https://doi.org/10.1016/j.pestbp Google Scholar
  25. Mouden S, Sarmiento KF, Klinkhamer PG, Leiss K (2017) Integrated pest management in western flower thrips: past, present and future. Pest Manag Sci 73(5):813–822CrossRefGoogle Scholar
  26. Mound LA (2005) Thysanoptera: diversity and interaction. Annu Rev Entomol 50:247–269CrossRefGoogle Scholar
  27. Murai T (2001) Development and reproductive capacity of Thrips hawaiiensis (Thysanoptera: Thripidae) and its potential as a major pest. Bull Entomol Res 91:193–198Google Scholar
  28. Nazemi A, Khajehali J, Van Leeuwen T (2016) Incidence and characterization of resistance to pyrethroid and organophosphorus insecticides in Thrips tabaci (Thysanoptera: Thripidae) in onion fields in Isfahan, Iran. Pestic Biochem Physiol 129:28–35CrossRefGoogle Scholar
  29. Puinean AM, Lansdell SJ, Collins T, Bielza P, Millar NS (2013) A nicotinic acetylcholine receptor transmembrane point mutation (G275E) associated with resistance to spinosad in Frankliniella occidentalis. J Neurochem 124(5):590–601CrossRefGoogle Scholar
  30. Rahman T, Spafford H, Broughton S (2012) Use of spinosad and predatory mites for the management of Frankliniella occidentalis in low tunnel-grown strawberry. Entomol Exp Applic 142(3):258–270CrossRefGoogle Scholar
  31. Reitz SR, Gao YL, Lei ZR (2011) Thrips: pests of concern to China and the United States. J Integr Agr 10:867–892Google Scholar
  32. Reynaud P, Balmes V, Pizzo J (2008) Thrips hawaiiensis (Morgan, 1913) (Thysanoptera: Thripidae), an Asian pest thrips now established in Europe. OEPP/EPPO Bulletin 38:155–160CrossRefGoogle Scholar
  33. Rinkevich FD, Chen M, Shelton AM, Scott JG (2010) Transcripts of the nicotinic acetylcholine receptor subunit gene Pxla6 with premature stop codons are associated with spinosad resistance in diamond back moth, Plutella xylostella. Invert Neurosci 10:25–33CrossRefGoogle Scholar
  34. Rueda M, Shelton AM (2003) Development of a bioassay system for monitoring susceptibility in Thrips tabaci. Pest Manag Sci 59:553–558CrossRefGoogle Scholar
  35. Shen JL, Wu YD (1995) Insecticide resistance in cotton boll worm and its management. China Agriculture Press, Beijing, pp 79–82Google Scholar
  36. Sial AA, Brunner JF, Garczynski SF (2011) Biochemical characterization of chlorantraniliprole and spinetoram resistance in laboratory-selected obliquebanded leafroller, Choristoneurarosaceana (Harris) (Lepidoptera: Tortricidae). Pestic Biochem Physio 99:274–279CrossRefGoogle Scholar
  37. Sparks TC, Nauen R (2015) IRAC: mode of action classification and insecticide resistance management. Pestic Biochem Physio 121:122–128CrossRefGoogle Scholar
  38. Sparks TC, Dripps JE, Watson GB, Paroonagian D (2012) Resistance and cross-resistance to the spinosyns—a review and analysis. PesticBiochem Physio 102:1–10Google Scholar
  39. Thalavaisundaram S, Wilkes MA, Mansfield S, Rose HA, Herron GA (2012) Esterases and glutathione-S-transferases contribute to pyrethroid resistance in western flower thrips, Frankliniella occidentalis. Aust Entomol 51:272–278CrossRefGoogle Scholar
  40. Wan Y, Yuan G, He B, Xu B, Xie W, Wang S, Zhang Y, Wu Q, Zhou X (2018) Foccα6, a truncated nAChR subunit, positively correlates with spinosad resistance in the western flower thrips, Frankliniella occidentalis (Pergande). Insect Biochem Mol Biol 99:1–10CrossRefGoogle Scholar
  41. Wang ZH, Gong YJ, Jin GH, Li BY, Chen JC, Kang ZJ, Zhu L, Reitz SR, Gao YL, Wei SJ (2016) Field-evolved resistance to insecticides in the invasive western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) in China. Pest Manag Sci 72:1440–1444CrossRefGoogle Scholar
  42. Watson GB, Chouinard SW, Cook KR, Geng C, Gifford JM, GustafsonGD Hasler JM, Larrinua IM, Letherer TJ, Mitchell JC, Pak WL, Salgado VL, Sparks TC, Stilwell GE (2010) A spinosyn-sensitive Drosophila melanogaster nicotinic acetylcholine receptor identified through chemical induced target site resistance, resistance gene identification, and heterologous expression. Insect Biochem Mol Biol 40:376–384CrossRefGoogle Scholar
  43. Wu Y, Liu K, Qiu HY, Li FJ, Cao Y (2014) Polymorphic microsatellite markers in Thrips hawaiiensis (Thysanoptera: Thripidae). Appl Entomol Zool 49:619–622CrossRefGoogle Scholar
  44. Wu SY, Gao YL, Smagghe G, Xu XN, Lei ZR (2016) Interactions between the entomopathogenic fungus Beauveria bassiana and the predatory mite Neoseiulus barkeri and biological control of their shared prey/host Frankliniella occidentalis. Biol Control 98:43–51CrossRefGoogle Scholar
  45. Wu SY, Tang LD, Zhang XR, Xing ZL, Lei ZR, Gao YL (2017) A decade of a thrips invasion in China: lessons learned. Ecotoxicology 27(7):1032–1038CrossRefGoogle Scholar
  46. Zhang SY, Kono S, Murai T, Miyata T (2008) Mechanisms of resistance to spinosad in the western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Insect Sci 15:125–132CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.The Ministry of Agriculture and Rural Affairs Key Laboratory of Integrated Pest Management of Tropical Crops, Environment and Plant Protection InstituteChinese Academy of Tropical Agricultural SciencesHaikouChina
  2. 2.State Key Laboratory for Biology of Plant Diseases and Insect Pest, Institute of Plant ProtectionChinese Academy of Agricultural SciencesBeijingChina
  3. 3.Key Laboratory of Agricultural Environment and Agriculture Products SafetyGuangxi UniversityNanningChina

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