Skip to main content
Log in

Risk of resistance and cross-resistance development to selection with imidacloprid and level of heritability in Oxycarenus hyalinipennis Costa (Hemiptera: Lygaeidae): a potential pest of cotton

  • Original Article
  • Published:
Phytoparasitica Aims and scope Submit manuscript

Abstract

Imidacloprid is a widely used neonicotinoid and provide successful control of different crop pests. Its excessive and frequent use nevertheless is leading to resistance in different insect pests across various geographical regions. In this study, we examined the risk of resistance development to imidacloprid, probability of cross-resistance and realized heritability (h2) to imidacloprid, nitenpyram, chlorpyrifos and cypermethrin in a sucking cotton pest Oxycarenus hyalinipennis. After 19 generations of continuous selection with imidacloprid, 146-fold increase in resistance was observed against this insecticide and its realized heritability was 0.21. Imidacloprid resistance selection did not mediate any cross-resistance to cypermethrin but it induced a low level of cross-resistance to nitenpyram and chlorpyrifos. According to the estimated imidacloprid resistance heritability, 12 and 5 generations would be required for a 10-fold LC50 increase at 30% and 70% selection pressure, respectively. The observed lack of cross-resistance with cypermethrin suggests its rotational use with imidacloprid to slow down the imidacloprid resistance in O. hyalinipennis.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abbas, N., Shad, S. A., & Razaq, M. (2012). Fitness cost, cross resistance and realized heritability of resistance to imidacloprid in Spodoptera litura (Lepidoptera: Noctuidae). Pesticide Biochemistry and Physiology, 103(3), 181–188.

    CAS  Google Scholar 

  • Afzal, M. B. S., Abbas, N., & Shad, S. A. (2015). Inheritance, realized heritability and biochemical mechanism of acetamiprid resistance in the cotton mealybug, Phenacoccus solenopsis Tinsley (Homoptera: Pseudococcidae). Pesticide Biochemistry and Physiology, 122, 44–49.

    CAS  PubMed  Google Scholar 

  • Ahmad, M., & Arif, M. I. (2009). Resistance of Pakistani field populations of spotted bollworm Earias vittella (Lepidoptera: Noctuidae) to pyrethroid, organophosphorus and new chemical insecticides. Pest Management Science, 65(4), 433–439.

    CAS  PubMed  Google Scholar 

  • Ahmad, M., Sayyed, A. H., Crickmore, N., & Saleem, M. A. (2007). Genetics and mechanism of resistance to deltamethrin in a field population of Spodoptera litura (Lepidoptera: Noctuidae). Pest Management Science, 63(10), 1002–1010.

    CAS  PubMed  Google Scholar 

  • Akbar, W., Gowda, A., Ahrens, J. E., Stelzer, J. W., Brown, R. S., Bollman, S. L., Greenplate, J. T., Gore, J., Catchot, A. L., Lorenz, G., Stewart, S. D., Kerns, D. L., Greene, J. K., Toews, M. D., Herbert, D. A., Reisig, D. D., Sword, G. A., Ellsworth, P. C., Godfrey, L. D., & Clark, T. L. (2019). First transgenic trait for control of plant bugs and thrips in cotton. Pest Management Science, 75(3), 867–877.

    CAS  PubMed  Google Scholar 

  • Akram, M., Asi, M. R., Mehfooz-ul-Haq, M. A., & Saleem, M. S. (2013). Bioefficacy of organophosphates, pyrethroids and new chemistry insecticides against a field population of dusky cotton bug, Oxycarenus spp.(Hemiptera: Oxycarenidae) in Bt cotton ecosystem. Pakistan Journal of Life Social Sciences, 11, 48–52.

    Google Scholar 

  • Alexandratos, N., & Bruinsma, J. (2012). World agriculture towards 2030/2050: The 2012 revision. Rome: ESA Working paper FAO.

    Google Scholar 

  • Ali, M. A., Farooq, J., Batool, A., Zahoor, A., Azeem, F., Mahmood, A., & Jabran, K. (2019). Cotton production in Pakistan. Cotton Production, 249.

  • Alyokhin, A., Dively, G., Patterson, M., Castaldo, C., Rogers, D., Mahoney, M., & Wollam, J. (2007). Resistance and cross-resistance to imidacloprid and thiamethoxam in the Colorado potato beetle Leptinotarsa decemlineata. Pest Management Science, 63(1), 32–41.

    CAS  PubMed  Google Scholar 

  • Arshad, M., Suhail, A., & Zain-ul-Abdin, G. M. (2011). Efficacy of transgenic Bt cotton against Helicoverpa armigera (Lepidoptera: Noctuidae) in the Punjab, Pakistan. Pakistan Entomologist, 33, 119–123.

    Google Scholar 

  • Atta, B., Gogi, M., Arif, M., Mustafa, F., Raza, M., Hussain, M., et al. (2015). Toxicity of some growth regulators (IGRs) against different life stages of ducky cotton bug Oxycarenus hyalinipennis Costa (Hemiptera: Lygaeidae: Oxycareninae). Bulgarian Journal of Agricultural Science, 21(2), 367–371.

    Google Scholar 

  • Bachman, P. M., Ahmad, A., Ahrens, J. E., Akbar, W., Baum, J. A., Brown, S., et al. (2017). Characterization of the activity spectrum of MON 88702 and the plant-incorporated protectant Cry51Aa2. 834_16. PloS one, 12(1).

  • Bala, S. C., Nihal, R., & Sarkar, A. (2019). Population dynamics of whitefly (Bemisia tabaci, Genn.) and Thrips (Scirtothrips dorsalis, Hood.) in Bt cotton. Journal of Entomology and Zoology Studies, 7(2), 1020-1024.

  • Ban, L., Zhang, S., Huang, Z., He, Y., Peng, Y., & Gao, C. (2012). Resistance monitoring and assessment of resistance risk to pymetrozine in Laodelphax striatellus (Hemiptera: Delphacidae). Journal of Economic Entomology, 105(6), 2129–2135.

    PubMed  Google Scholar 

  • Banazeer, A., Afzal, M. B. S., Shad, S. A. (2020a) Characterization of dimethoate resistance in Oxycarenus hyalinipennis (Costa): Resistance selection, cross-resistance to three insecticides and mode of inheritance. Phytoparasitica, 1–9.

  • Banazeer, A., Shad, S. A., & Afzal, M. B. S. (2020b). Laboratory induced bifenthrin resistance selection in Oxycarenus hyalinipennis (Costa)(Hemiptera: Lygaeidae): Stability, cross-resistance, dominance and effects on biological fitness. Crop Protection, 132, 105107.

    CAS  Google Scholar 

  • Bass, C., Denholm, I., Williamson, M. S., & Nauen, R. (2015). The global status of insect resistance to neonicotinoid insecticides. Pesticide Biochemistry and Physiology, 121, 78–87.

    CAS  PubMed  Google Scholar 

  • Bilal, M., Freed, S., Ashraf, M. Z., & Rehan, A. (2018). Resistance and detoxification enzyme activities to bifenthrin in Oxycarenus hyalinipennis (Hemiptera: Lygaeidae). Crop Protection, 111, 17–22.

    CAS  Google Scholar 

  • Brookfield, J. F. (2012). Heritability. Current Biology, 22(7), R217–R219.

    CAS  PubMed  Google Scholar 

  • Casida, J. E., & Durkin, K. A. (2013). Neuroactive insecticides: Targets, selectivity, resistance, and secondary effects. Annual Review of Entomology, 58, 99–117.

    CAS  PubMed  Google Scholar 

  • Castellanos, N. L., Haddi, K., Carvalho, G. A., de Paulo, P. D., Hirose, E., Guedes, R. N. C., Smagghe, G., & Oliveira, E. E. (2019). Imidacloprid resistance in the Neotropical brown stink bug Euschistus heros: Selection and fitness costs. Journal of Pest Science, 92(2), 847–860.

    Google Scholar 

  • Dhillon, M. K., Gujar, G. T., & Kalia, V. (2011). Impact of Bt cotton on insect biodiversity in cotton ecosystem in India. Pakistan Entomologist, 33(2), 161–165.

    Google Scholar 

  • Edwards, K. T., Caprio, M. A., Allen, K. C., & Musser, F. R. (2013). Risk assessment for Helicoverpa zea (Lepidoptera: Noctuidae) resistance on dual-gene versus single-gene corn. Journal of Economic Entomology, 106(1), 382–392.

    PubMed  Google Scholar 

  • El-Rahim, A., Gamal, H., & Amro, M. (2015). Population fluctuations of Oxycarenus hyalinipennis and effect of certain compounds on its population on okra in Asyut governorate. Egyptian Journal of Agricultural Research, 9, 25–34.

    Google Scholar 

  • Elzaki, M. E. A., Pu, J., Zhu, Y., Zhang, W., Sun, H., Wu, M., & Han, Z. (2018). Cross-resistance among common insecticides and its possible mechanism in Laodelphax striatellus Fallén (Hemiptera: Delphacidae). Oriental Insects, 52(1), 2–15.

    Google Scholar 

  • Falconer, D. S. (1981). Introduction to quantitative genetics (Vol. Ed. 2): Longman.

  • Falconer, D. S., & Mackay, T. F. C. (1996). Introduction to quantitative Genetics,4th edition. New York: Longman.

    Google Scholar 

  • Feyereisen, R., Dermauw, W., & Van Leeuwen, T. (2015). Genotype to phenotype, the molecular and physiological dimensions of resistance in arthropods. Pesticide Biochemistry and Physiology, 121, 61–77.

    CAS  PubMed  Google Scholar 

  • Firkoi, M. J., & Hayes, J. L. (1990). Quantitative genetic tools for insecticide resistance risk assessment: Estimating the heritability of resistance. Journal of Economic Entomology, 83(3), 647–654.

    Google Scholar 

  • Garrood, W. T., Zimmer, C. T., Gorman, K. J., Nauen, R., Bass, C., & Davies, T. G. (2016). Field evolved resistance to imidacloprid and ethiprole in populations of brown planthopper Nilaparvata lugens collected from across south and East Asia. Pest Management Science, 72(1), 140–149.

    CAS  PubMed  Google Scholar 

  • Gassmann, A. J., Carrière, Y., & Tabashnik, B. E. (2009). Fitness costs of insect resistance to Bacillus thuringiensis. Annual Review of Entomology, 54(1), 147–163.

    CAS  PubMed  Google Scholar 

  • Gorman, K., Devine, G., Bennison, J., Coussons, P., Punchard, N., & Denholm, I. (2007). Report of resistance to the neonicotinoid insecticide imidacloprid in Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). Pest Management Science, 63(6), 555–558.

    CAS  PubMed  Google Scholar 

  • Gorman, K., Slater, R., Blande, J. D., Clarke, A., Wren, J., McCaffery, A., & Denholm, I. (2010). Cross resistance relationships between neonicotinoids and pymetrozine in Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science, 66(11), 1186–1190.

    CAS  PubMed  Google Scholar 

  • Graham, S. H., & Stewart, S. D. (2018). Field study investigating Cry51Aa2. 834_16 in cotton for control of thrips (Thysanoptera: Thripidae) and tarnished plant bugs (Hemiptera: Miridae). Journal of Economic Entomology, 111(6), 2717–2726.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo, T., Ma, Y., Ding, R., Zhou, J., Li, G., Cai, X., et al. (2014). Selection and realized heritability analysis of resistance to imidacloprid in cotton aphid (Aphis gossypii). Acta Entomologica Sinica, 57(3), 330–334.

    Google Scholar 

  • Hofs, J.-L., Schoeman, A., & Vaissayrel, M. (2004). Effect of Bt cotton on arthropod biodiversity in south African cotton fields. Communications in Agricultural and Applied Biological Sciences, 69(3), 191.

    CAS  PubMed  Google Scholar 

  • Ijaz, M., & Shad, S. A. (2018). Inheritance mode and realized heritability of resistance to imidacloprid in Oxycarenus hyalinipennis Costa (Hemiptera: Lygaeidae). Crop Protection, 112, 90–95.

    CAS  Google Scholar 

  • Ijaz, M., Afzal, M. B. S., & Shad, S. A. (2016). Resistance risk analysis to acetamiprid and other insecticides in Acetamiprid selected population of Phenacoccus solenopsis. Phytoparasitica, 44, 177–186.

    CAS  Google Scholar 

  • Jeschke, P., Nauen, R., Schindler, M., & Elbert, A. (2010). Overview of the status and global strategy for neonicotinoids. Journal of Agricultural and Food Chemistry, 59(7), 2897–2908.

    PubMed  Google Scholar 

  • Jeyakumar, P., Tanwar, R., Chand, M., Singh, A., Monga, D., & Bambawale, O. (2008). Performance of Bt cotton against sucking pests. Journal of Biopesticides, 1(2), 223–225.

    Google Scholar 

  • Jutsum, A. R., Heaney, S. P., Perrin, B. M., & Wege, P. J. (1998). Pesticide resistance: Assessment of risk and the development and implementation of effective management strategies†. Pesticide Science, 54(4), 435–446.

    CAS  Google Scholar 

  • Kaufman, P. E., Nunez, S. C., Geden, C. J., & Scharf, M. E. (2010). Selection for resistance to imidacloprid in the house fly (Diptera: Muscidae). Journal of Economic Entomology, 103(5), 1937–1942.

    CAS  PubMed  Google Scholar 

  • Khan, H. A. A., Akram, W., Shehzad, K., & Shaalan, E. A. (2011). First report of field evolved resistance to agrochemicals in dengue mosquito, Aedes albopictus (Diptera: Culicidae), from Pakistan. Parasites & Vectors, 4(1), 146.

    CAS  Google Scholar 

  • Köhler, H.-R., & Triebskorn, R. (2013). Wildlife ecotoxicology of pesticides: Can we track effects to the population level and beyond? Science, 341(6147), 759–765.

    PubMed  Google Scholar 

  • Lai, T., & Su, J. (2011). Assessment of resistance risk in Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) to chlorantraniliprole. Pest Management Science, 67(11), 1468–1472.

    CAS  PubMed  Google Scholar 

  • Li, J., Wang, Q., Zhang, L., & Gao, X. (2012). Characterization of imidacloprid resistance in the housefly Musca domestica (Diptera: Muscidae). Pesticide Biochemistry and Physiology, 102(2), 109–114.

    CAS  Google Scholar 

  • Liu, Y.-H., Chung, Y.-C., & Xiong, Y. (2001). Purification and characterization of a dimethoate-degrading enzyme of Aspergillus Niger ZHY256, isolated from sewage. Applied and Environmental Microbiology, 67(8), 3746–3749.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mansoor-ul-Hasan, U. E., Sagheer, M., & Ghouse, G. (2007). Some studies on the integration of chemical control with biological control for cotton insect pest management. Pakistan Journal of Agricultural Sciences, 44(2), 277–282.

    Google Scholar 

  • Nasir, M., Asif, M. U., & Shamraiz, R. M. (2019). Comparative efficacy of different insecticides against dusky cotton bug (Oxycarenus spp.) under field conditions.

  • Powles, S. B., & Yu, Q. (2010). Evolution in action: Plants resistant to herbicides. Annual Review of Plant Biology, 61, 317–347.

    CAS  PubMed  Google Scholar 

  • Robertson, J., & Preisler, H. (1992). Pesticide bioassays with arthropods. Boca Raton: CRC.

    Google Scholar 

  • Rosenheim, J. (1991). Realized heritability estimation for pesticide resistance traits. Entomologia Experimentalis et Applicata, 58(1), 93–97.

    Google Scholar 

  • Sanada Morimura, S., Fujii, T., Chien, H. V., Cuong, L. Q., Estoy Jr., G. F., & Matsumura, M. (2019). Selection for imidacloprid resistance and mode of inheritance in the brown planthopper, Nilaparvata lugens. Pest Management Science, 75(8), 2271–2277.

    CAS  PubMed  Google Scholar 

  • Sanghi, A. H., Aslam, M., & a., & Khalid., L. (2014). Efficacy of different insecticides against dusky cotton bug Oxycarenus hyalinipennis (Hemiptera: Lygaeidae) in ecological zone of Rahim yar khan. International Journal of Comprehensive Research in Biological Sciences, 1, 49–54.

    Google Scholar 

  • Shah, R. M., Abbas, N., Shad, S. A., & Sial, A. A. (2015). Selection, resistance risk assessment, and reversion toward susceptibility of pyriproxyfen in Musca domestica L. Parasitology Research, 114(2), 487–494.

    PubMed  Google Scholar 

  • Shakeel, M., Farooq, M., Nasim, W., Akram, W., Khan, F. Z. A., Jaleel, W., Zhu, X., Yin, H., Li, S., Fahad, S., Hussain, S., Chauhan, B. S., & Jin, F. (2017). Environment polluting conventional chemical control compared to an environmentally friendly IPM approach for control of diamondback moth, Plutella xylostella (L.), in China: a review. Environmental Science and Pollution Research, 24(17), 14537–14550.

    CAS  PubMed  Google Scholar 

  • Slade, G., & Morrison, N. (2014). Developing GM insects for sustainable pest control in agriculture and human health. BMC Proceedings, 8(4), O43 BioMed Central.

    PubMed Central  Google Scholar 

  • Software, L. (2002). Polo plus, a User’s guide to Probit or logic analysis. Berkeley: LeOra Software.

    Google Scholar 

  • Srigiriraju, L., Semtner, P. J., & Bloomquist, J. R. (2010). Monitoring for imidacloprid resistance in the tobacco adapted form of the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae), in the eastern United States. Pest Management Science, 66(6), 676–685.

    CAS  PubMed  Google Scholar 

  • Srinivas, M., & Patil, B. (2010). Quantitative and qualitative loss caused by dusky cotton bug, Oxyacarenus laetus Kirby on cotton. Karnataka Journal of Agricultural Sciences, 17(3).

  • Tabashnik, B. E. (1992). Resistance risk assessment: Realized heritability of resistance to Bacillus thuringiensis in diamondback moth (Lepidoptera: Plutellidae), tobacco budworm (Lepidoptera: Noctuidae), and Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology, 85(5), 1551–1559.

    Google Scholar 

  • Tabashnik, B. E., & McGaughey, W. H. (1994). Resistance risk assessment for single and multiple insecticides: Responses of Indianmeal moth (Lepidoptera: Pyralidae) to bacillus thuringiensis. Journal of Economic Entomology, 87(4), 834–841.

    Google Scholar 

  • Tanaka, Y., & Noppun, V. (1989). Heritability estimates of phenthoate resistance in the diamond-back moth. Entomologia Experimentalis et Applicata, 52(1), 39–47.

    Google Scholar 

  • Tennekes, H. A., & Sanchez-Bayo, F. (2011). Time-dependent toxicity of neonicotinoids and other toxicants: Implications for a new approach to risk assessment. Journal of Environmental & Analytical Toxicology.

  • Tomizawa, M., & Casida, J. E. (2005). Neonicotinoid insecticide toxicology: Mechanisms of selective action. Annual Review of Pharmacology and Toxicology, 45, 247–268.

    CAS  PubMed  Google Scholar 

  • Tomizawa, M., & Casida, J. E. (2008). Molecular recognition of neonicotinoid insecticides: The determinants of life or death. Accounts of Chemical Research, 42(2), 260–269.

    Google Scholar 

  • Torres-Vila, L., Rodrıguez-Molina, M., Lacasa-Plasencia, A., & Bielza-Lino, P. (2002). Insecticide resistance of Helicoverpa armigera to endosulfan, carbamates and organophosphates: The Spanish case. Crop Protection, 21(10), 1003–1013.

    CAS  Google Scholar 

  • Ullah, S., Shad, S. A., & Abbas, N. (2015). Resistance of dusky cotton bug, Oxycarenus hyalinipennis Costa (Lygaidae: Hemiptera), to conventional and novel chemistry insecticides. Journal of Economic Entomology, 109(1), 345–351.

    PubMed  Google Scholar 

  • Ullah, S., Shah, R. M., & Shad, S. A. (2016). Genetics, realized heritability and possible mechanism of chlorfenapyr resistance in Oxycarenus hyalinipennis (Lygaeidae: Hemiptera). Pesticide Biochemistry and Physiology, 133, 91–96.

    CAS  PubMed  Google Scholar 

  • USDA (2009). Significant Pest bulletin cottonseed bug. United States Department of Agriculture, Animal and Plant Health Inspection Service, 1.

  • Van der Sluijs, J. P., Amaral-Rogers, V., Belzunces, L., Van Lexmond, M. B., Bonmatin, J.-M., Chagnon, M., et al. (2015). Conclusions of the worldwide integrated assessment on the risks of neonicotinoids and fipronil to biodiversity and ecosystem functioning. Environmental Sciences and Pollution Research, 22, 148-154.

  • Wang, Z., Yao, M., & Wu, Y. (2009). Cross resistance, inheritance and biochemical mechanisms of imidacloprid resistance in B biotype Bemisia tabaci. Pest Management Science: formerly Pesticide Science, 65(11), 1189–1194.

    CAS  Google Scholar 

  • Wang, S. Y., Liu, Y., Zhou, X., Zhang, A., Li, L., et al. (2011). Mechanisms of imidacloprid resistance in Frankliniella occidentalis. Chinese Journal of Applied Entomology, 48, 559–565.

    CAS  Google Scholar 

  • Wang, L.-L., Feng, Z. J., Li, T., Lu, X. P., Zhao, J. J., et al. (2015). Inheritance, realized heritability, and biochemical mechanisms of malathion resistance in Bactrocera dorsalis (Diptera: Tephritidae). Journal of Economic Entomology, 109(1), 299–306.

    PubMed  Google Scholar 

  • Zhang, L., Shi, J., & Gao, X. (2008). Inheritance of beta-cypermethrin resistance in the housefly Musca domestica (Diptera: Muscidae). Pest Management Science, 64(2), 185–190.

    CAS  PubMed  Google Scholar 

  • Zhao, J.-Z., Bishop, B. A., & Grafius, E. J. (2000). Inheritance and synergism of resistance to imidacloprid in the Colorado potato beetle (Coleoptera: Chrysomelidae). Journal of Economic Entomology, 93(5), 1508–1514.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We specially thank to Dr. Muhammad Babar Shahzad Afzal, Assistant Research Officer (Entomology), Citrus Research Institute, Sargodha, Punjab, Pakistan to spare his precious time to read the final version of manuscript for English language and sense.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Mamuna Ijaz or Sarfraz Ali Shad.

Ethics declarations

Conflict of interest

No conflict of interest was found among authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ijaz, M., Shad, S.A. Risk of resistance and cross-resistance development to selection with imidacloprid and level of heritability in Oxycarenus hyalinipennis Costa (Hemiptera: Lygaeidae): a potential pest of cotton. Phytoparasitica 49, 287–297 (2021). https://doi.org/10.1007/s12600-020-00842-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12600-020-00842-3

Keywords

Navigation