Skip to main content
SpringerLink
Log in

Impact of sequential exposure of Beauveria bassiana and imidacloprid against susceptible and resistant strains of Musca domestica

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

Insecticide resistance in the housefly Musca domestica is hampering pest management. However, entomopathogens, possibly in combination with insecticides, may have control potential against resistant houseflies. This study investigates the combination of the entomopathogenic fungus Beauveria bassiana and the neonicotinoid insecticide, imidacloprid against a susceptible and a resistant housefly strain, respectively under laboratory conditions. The fungus and insecticide were tested alone and in combinations at LC30. Significant and synergistic interactions between B. bassiana and imidacloprid were observed with increased mortality rates of the combined treatment as compared to individual treatment in housefly strains 772a (susceptible) and 766b (resistant). Significant differences in the GST and P450 activities for both strains were found. Female 766b flies caused 15- to 237-fold increases in gene expression of xenobiotic response genes for B. bassiana and 23- to 120-fold changes for imidacloprid. The combination of B. bassiana and imidacloprid caused significant synergistic interaction when applied against two housefly strains irrespective of order of application. The effect was highest when the insecticide was applied first. The resistant housefly strain had elevated detoxification enzymes and higher expression of detoxification genes, but showed the same level of susceptibility to the combined fungus/insecticide treatment as the susceptible strain.

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

Similar content being viewed by others

References

  • Abbott W (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    Article  CAS  Google Scholar 

  • Agnew P, Berticat C, Bedhomme S, Sidobre C, Michalakis Y, Elena S (2004) Parasitism increases and decreases the costs of insecticide resistance in mosquitoes. Evolution 58:579–586

    Article  PubMed  CAS  Google Scholar 

  • Alizadeh A, Samih MA, Khezri M, Riseh RS (2007) Compatibility of Beauveria bassiana (Bals) Vuill. with several pesticides. Int J Agric Biol 9:31–34

    Google Scholar 

  • Aufauvre J, Biron DG, Vidau C, Fontbonne R, Roudel M, Diogon M, Viguès B, Belzunces LP, Delbac F, Blot N (2012) Parasite-insecticide interactions: a case study of Nosema ceranae and fipronil synergy on honeybee. Sci Rep 2:326

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bitsadze N, Jaronski S, Khasdan V, Abashidze E, Abashidze M, Latchininsky A, Samadashvili D, Sokhadze I, Rippa M, Ishaaya I (2013) Joint action of Beauveria bassiana and the insect growth regulators diflubenzuron and novaluron, on the migratory locust, Locusta migratoria. J Pest Sci 86:293–300

    Article  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Busvine JR (1980) Insects and hygiene. Chapman and Hall, New York

    Book  Google Scholar 

  • Cohen D, Green M, Block C, Slepon R, Ambar R, Wasserman SS, Levine MM (1991) Reduction of transmission of shigellosis by control of houseflies (Musca domestica). Lancet 337:993–997

    Article  PubMed  CAS  Google Scholar 

  • Constantinescu F, Sicuia OA, Fătu C, Dinu MM, Andrei AM, Mincea C (2014) In vitro compatibility between chemical and biological products used for seed treatment. Sci Pap Ser A, Agron 57:146–151

    Google Scholar 

  • Emerson PM, Lindsay SW, Walraven GE, Faal H, Bøgh C, Lowe K, Bailey RL (1999) Effect of fly control on trachoma and diarrhoea. Lancet 353:1401–1403

    Article  PubMed  CAS  Google Scholar 

  • Enayati AA, Ranson H, Hemingway J (2005) Insect glutathione transferases and insecticide resistance. Insect Mol Biol 14:3–8

    Article  PubMed  CAS  Google Scholar 

  • Ericsson JD, Kabaluk JT, Goettel MS, Myers JH (2007) Spinosad interacts synergistically with the insect pathogen Metarhizium anisopliae against the exotic wireworms Agriotes lineatus and Agriotes obscurus (Coleoptera: elateridae). J Econ Entomol 100:31–38

    Article  PubMed  Google Scholar 

  • Fan J, Xie Y, Xue J, Liu R (2013) The effect of Beauveria brongniartii and its secondary metabolites on the detoxification enzymes of the pine caterpillar, Dendrolimus tabulaeformis. J Insect Sci 13:44

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Farenhorst M, Mouatcho JC, Kikankie CK, Brooke BD, Hunt RH, Thomas MB, Koekemoer LL, Knols BG, Coetzee M (2009) Fungal infection counters insecticide resistance in African malaria mosquitoes. Proc Natl Acad Sci USA 106:17443–17447

    Article  PubMed  PubMed Central  Google Scholar 

  • Farenhorst M, Knols BG, Thomas MB, Howard AF, Takken W, Rowland M, N’Guessan R (2010) Synergy in efficacy of fungal entomopathogens and permethrin against West African insecticide-resistant Anopheles gambiae mosquitoes. PLoS ONE 5(8):e12081

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Farooq M, Freed S (2016) Combined effects of Beauveria bassiana (Hypocreales: Clavicipitaceae) and insecticide mixtures on biological parameters of Musca domestica (Diptera: Muscidae). Pak J Zool 48:1465–1476

    Google Scholar 

  • Feng MG, Pu XY (2005) Time–concentration–mortality modeling of the synergistic interaction of Beauveria bassiana and imidacloprid against Nilaparvata lugens. Pest Manag Sci 61:363–370

    Article  PubMed  CAS  Google Scholar 

  • Feng MG, Pu XY, Ying SH, Wang YG (2004) Field trials of an oil-based emulsifiable formulation of Beauveria bassiana conidia and low application rates of imidacloprid for control of false-eye leafhopper Empoasca vitis on tea in southern China. Crop Prot 23:489–496

    Article  CAS  Google Scholar 

  • Feyereisen R (1995) Molecular biology of insecticide resistance. Toxicol Lett 82:83–90

    Article  PubMed  Google Scholar 

  • Feyereisen R (2005) Insect cytochrome P450. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science. Elsevier, Oxford, pp 1–77

    Google Scholar 

  • Feyereisen R (2012) Insect CYP genes and P450 enzymes. Insect Mol Biol 8:236–316

    Google Scholar 

  • ffrench-Constant R (1999) Target site mediated insecticide resistance: what questions remain? Insect Biochem Mol Biol 29:397–403

    Article  CAS  Google Scholar 

  • Furlong M, Groden E (2001) Evaluation of synergistic interactions between the Colorado potato beetle (Coleoptera: Chrysomelidae) pathogen Beauveria bassiana and the insecticides, imidacloprid, and cyromazine. J Econ Entomol 94:344–356

    Article  PubMed  CAS  Google Scholar 

  • Højland DH, Kristensen M (2017) Analysis of differentially expressed genes related to resistance in spinosad- and neonicotinoid-resistant Musca domestica L (Diptera: Muscidae) strains. PLoS ONE 12(1):e0170935

    Article  PubMed  PubMed Central  Google Scholar 

  • Højland DH, Jensen KMV, Kristensen M (2014a) Adaptation of Musca domestica L field population to laboratory breeding causes transcriptional alterations. PLoS ONE 9(1):e85965

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Højland DH, Jensen KMV, Kristensen M (2014b) Expression of xenobiotic metabolizing cytochrome P450 genes in a spinosad-resistant Musca domestica L strain. PLoS ONE 9(8):e103689

    Article  PubMed  PubMed Central  Google Scholar 

  • Højland DH, Vagn Jensen KM, Kristensen M (2014c) A comparative study of P450 gene expression in field and laboratory Musca domestica L strains. Pest Manag Sci 70:1237–1242

    Article  PubMed  CAS  Google Scholar 

  • Hovda LR, Hooser SB (2002) Toxicology of newer pesticides for use in dogs and cats. Vet Clin N Am 32:455–467

    Article  Google Scholar 

  • Hussain D, Akram M, Iqbal Z, Ali A, Saleem M (2010) Effect of some insecticides on Trichogramma chilonis Ishii (Trichogrammatidae: Hymenoptera) immature and adult survival. J Agric Res 48:531–537

    Google Scholar 

  • Jia M, Cao G, Li Y, Tu X, Wang G, Nong X, Whitman DW, Zhang Z (2016) Biochemical basis of synergism between pathogenic fungus Metarhizium anisopliae and insecticide chlorantraniliprole in Locusta migratoria (Meyen). Sci Rep 6:28424

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Joffe T, Gunning RV, Allen GR, Kristensen M, Alptekin S, Field LM, Moores GD (2012) Investigating the potential of selected natural compounds to increase the potency of pyrethrum against houseflies Musca domestica (Diptera: Muscidae). Pest Manag Sci 68:178–184

    Article  PubMed  CAS  Google Scholar 

  • Kaufman PE, Gerry AC, Rutz DA, Scott JG (2006) Monitoring susceptibility of house flies (Musca domestica L) in the United States to imidacloprid. J Agric Urban Entomol 23:195–200

    CAS  Google Scholar 

  • Kaufman PE, Nunez SC, Mann RS, Geden CJ, Scharf ME (2010) Nicotinoid and pyrethroid insecticide resistance in houseflies (Diptera: Muscidae) collected from Florida dairies. Pest Manag Sci 66:290–294

    Article  PubMed  CAS  Google Scholar 

  • Koppenhöfer AM, Cowles RS, Cowles EA, Fuzy EM, Baumgartner L (2002) Comparison of neonicotinoid insecticides as synergists for entomopathogenic nematodes. Biol Control 24:90–97

    Article  Google Scholar 

  • Kristensen M (2005) Glutathione S-transferase and insecticide resistance in laboratory strains and field populations of Musca domestica. J Econ Entomol 98:1341–1348

    Article  PubMed  CAS  Google Scholar 

  • Kristensen M, Jespersen JB (2008) Susceptibility to thiamethoxam of Musca domestica from Danish livestock farms. Pest Manag Sci 64:126–132

    Article  PubMed  CAS  Google Scholar 

  • Kristensen M, Jespersen JB, Knorr M (2004) Cross-resistance potential of fipronil in Musca domestica. Pest Manag Sci 60:894–900

    Article  PubMed  CAS  Google Scholar 

  • Kristensen M, Huang J, Qiao CL, Jespersen JB (2006) Variation of Musca domestica L. acetylcholinesterase in Danish housefly populations. Pest Manag Sci 62:738–745

    Article  PubMed  CAS  Google Scholar 

  • Li J, Wang Q, Zhang L, Gao X (2012) Characterization of imidacloprid resistance in the housefly Musca domestica (Diptera: Muscidae). Pestic Biochem Physiol 102:109–114

    Article  CAS  Google Scholar 

  • Malik A, Singh N, Satya S (2007) House fly (Musca domestica): a review of control strategies for a challenging pest. J Environ Sci Health B 42:453–469

    Article  PubMed  CAS  Google Scholar 

  • Markussen MD, Kristensen M (2010) Cytochrome P450 monooxygenase-mediated neonicotinoid resistance in the house fly Musca domestica L. Pestic Biochem Physiol 98:50–58

    Article  CAS  Google Scholar 

  • Matsuda K, Shimomura M, Kondo Y, Ihara M, Hashigami K, Yoshida N, Raymond V, Mongan NP, Freeman JC, Komai K (2000) Role of loop D of the α7 nicotinic acetylcholine receptor in its interaction with the insecticide imidacloprid and related neonicotinoids. Br J Pharmacol 130:981–986

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McGraw-Hill C (2008) Statistix 8.1 Analytical software, Tallahassee, Florida

  • Nardini L, Blanford S, Coetzee M, Koekemoer LL (2014) Effect of Beauveria bassiana infection on detoxification enzyme transcription in pyrethroid resistant Anopheles arabiensis: a preliminary study. Trans R Soc Trop Med Hyg 108:221–227

    Article  PubMed  CAS  Google Scholar 

  • Nedal MF, Hassan FD (2009) Changes in detoxifying enzymes and carbohydrate metabolism associated with spinetoram in two field-collected strains of Spodoptera littoralis (Biosd.). Egypt Acad J Biolog Sci 1:15–26

    Google Scholar 

  • Neves PM, Hirose E, Tchujo PT, Moino A Jr (2001) Compatibility of entomopathogenic fungi with neonicotinoid insecticides. Neotrop Entomol 30:263–268

    Article  CAS  Google Scholar 

  • Paula AR, Carolino AT, Paula CO, Samuels RI (2011) The combination of the entomopathogenic fungus Metarhizium anisopliae with the insecticide imidacloprid increases virulence against the dengue vector Aedes aegypti (Diptera: Culicidae). Parasit Vectors 4:8

    Article  PubMed  PubMed Central  Google Scholar 

  • Polo-PC (1987) User’s guide to probit or logit analysis. LeOra Software, Berkeley

    Google Scholar 

  • Quintela ED, Mccoy CW (1997) Pathogenicity enhancement of Metarhizium anisopliae and Beauveria bassiana to first instars of Diaprepes abbreviatus (Coleoptera: Curculionidae) with sublethal doses of imidacloprid. Environ Entomol 26:1173–1182

    Article  CAS  Google Scholar 

  • Roslavtseva S (1994) Current views of biochemical mechanisms of resistance. Agrokhimiya 10:143–148

    Google Scholar 

  • Russell CW, Ugine TA, Hajek AE (2010) Interactions between imidacloprid and Metarhizium brunneum on adult Asian longhorned beetles (Anoplophora glabripennis (Motschulsky))(Coleoptera: Cerambycidae). J Invertebr Pathol 105:305–311

    Article  PubMed  CAS  Google Scholar 

  • Serebrov V, Gerber O, Malyarchuk A, Martemyanov V, Alekseev A, Glupov V (2006) Effect of entomopathogenic fungi on detoxification enzyme activity in greater wax moth Galleria mellonella L. (Lepidoptera, Pyralidae) and role of detoxification enzymes in development of insect resistance to entomopathogenic fungi. Biol Bull 33:581–586

    Article  CAS  Google Scholar 

  • Steinkraus DC, Geden CJ, Rutz DA, Kramer JP (1990) First report of the natural occurrence of Beauveria bassiana (Moniliales: Moniliaceae) in Musca domestica (Diptera: Muscidae). J Med Entomol 27:309–312

    Article  Google Scholar 

  • R development core team (2012) R: a language and environment for statistical computing, R foundation for statistical computing, Vienna, Austria. https://www.r-project.org/

  • Watson D, Rutz D, Long S (1996) Beauveria bassiana and sawdust bedding for the management of the housefly, Musca domestica (Diptera: Muscidae) in calf hutches. Biol Control 7:221–227

    Article  Google Scholar 

  • Wilce MC, Parker MW (1994) Structure and function of glutathione S-transferases. Biochim et Biophys Acta (BBA)-Protein Structure Mol Enzymol 1205:1–18

    Article  CAS  Google Scholar 

  • Wu S, Kostromytska OS, Koppenhöfer AM (2017) Synergistic combinations of a pyrethroid insecticide and an emulsifiable oil formulation of Beauveria bassiana to overcome insecticide resistance in Listronotus maculicollis (Coleoptera: Curculionidae). J Econ Entomol 110:1794–1802

    Article  PubMed  Google Scholar 

  • Yaqoob R, Tahir HM, Khan SY, Naseem S (2013) Insecticide resistance in Bactocera zonata (Diptera: Tephritidae) in district, Sargodha, Pakistan. Biochem Pharmacol 2:114

    Article  CAS  Google Scholar 

  • Yu S, Robinson F, Nation J (1984) Detoxication capacity in the honey bee, Apis mellifera L. Pestic Biochem Physiol 22:360–368

    Article  CAS  Google Scholar 

  • Zibaee A, Bandani AR, Tork M (2009) Effect of the entomopathogenic fungus, Beauveria bassiana, and its secondary metabolite on detoxifying enzyme activities and acetylcholinesterase (AChE) of the Sunn pest, Eurygaster integriceps (Heteroptera: Scutellaridae). Biocontrol Sci Technol 19:485–498

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank Claus Dahl, Lars Damberg, Tina Tønnersen for valuable technical assistance. Muzammil Farooq was supported by a Higher Education Commission of Pakistan (HEC) Fellowship.

Author information

Authors and Affiliations

  1. Department of Entomology, Faculty of Agricultural Sciences and Technology, Bahauddin Zakariya University, Multan, Pakistan

    Muzammil Farooq & Shoaib Freed

  2. Department of Agroecology, Aarhus University, 4200, Slagelse, Denmark

    Tove Steenberg, Dorte Heidi Højland & Michael Kristensen

Authors
  1. Muzammil Farooq
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tove Steenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dorte Heidi Højland
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shoaib Freed
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michael Kristensen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael Kristensen.

Additional information

Handling Editor: Helen Roy

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Farooq, M., Steenberg, T., Højland, D.H. et al. Impact of sequential exposure of Beauveria bassiana and imidacloprid against susceptible and resistant strains of Musca domestica. BioControl 63, 707–718 (2018). https://doi.org/10.1007/s10526-018-9892-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-018-9892-6

Keywords

Search

Navigation