Skip to main content
SpringerLink
Log in

Emergence of fipronil resistant Rhipicephalus microplus populations in Indian states

  • Published:
Experimental and Applied Acarology Aims and scope Submit manuscript

Abstract

The intensive usage of chemical acaricides for the control of the cattle tick Rhipicephalus microplus has resulted in the development and establishment of multi-acaricide resistant populations. Fipronil, a phenylpyrazole insecticide, is currently marketed in India for the management of this important veterinary tick species. Here, we tested Indian isolates of R. microplus which have developed multi-acaricide resistance, for their susceptibility to fipronil. Twenty-five field isolates from five agro-climatic zones of the country were collected and tested by adult immersion test (AIT) and larval packet test (LPT). Sixteen isolates with resistance factor (RF) in the range of 1.56–10.9 were detected using LPT, whereas only 11 isolates with RF ranging from 1.05 to 4.1 were detected using AIT. A significant variation of RF between both tests was found, which raises doubt about the suitability of larva-based assays in screening of fipronil resistance. The data indicated possible cross-resistance between groups of acaricides in fipronil-resistant tick populations.

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

Similar content being viewed by others

References

  • Abbas RZ, Zaman MA, Colwell DD, Gilleard J, Iqbal Z (2014) Acaricide resistance in cattle ticks and approaches to its management: the state of play. Vet Parasitol 203(1–2):6–20

    CAS  PubMed  Google Scholar 

  • Abbas N, Ijaz M, Shad SA, Binyameen M (2016) Assessment of resistance risk to fipronil and cross resistance to other insecticides in the Musca domestica L. (Diptera: Muscidae). Vet Parasitol 223:71–76

    CAS  PubMed  Google Scholar 

  • Adehan SB, Biguezoton A, Adakal H, Assogba MN, Zoungrana S, Gbaguidi AM, Tonouhewa A, Kandé S, Achi L, Kagone H, Adehan R, Mensah GA, De Deken R, Madder M, Farougou S (2016) Acaricide resistance of Rhipicephalus microplus ticks in Benin. Afr J Agric Res 11(14):1199–1208

    CAS  Google Scholar 

  • Alberti H, Alberti ALL, Rinaldi PLF, Lamberti DDG, Rodríguez LG, Lima GL (2001) Avaliac¸ ão da eficácia do fipronil e da deltametrina, formulac¸ ão “pour-on”, no control da Haematobia irritans, parasitandobovinosem regime de campo, naregiãooeste do Estado de São Paulo. A-Hora-Vet 20:48–51

    Google Scholar 

  • Anadon A, Gupta RC (2012) Fipronil. In: Gupta RC (ed) Veterinary toxicology. Academic Press, Amsterdam, pp 604–608

    Google Scholar 

  • Andreotti R, Guerrero FD, Soares MA, Barros JC, Miller RJ, Léon APD (2001) Acaricide resistance of Rhipicephalus (Boophilus) microplus in state of MatoGrosso do Sul, Brazil. Rev Bras Parasitol 20(2):127–133

    Google Scholar 

  • Angus BM (1996) The history of the cattle tick Boophilus microptus in Australia and achievements in its control. Int J Parasitol 26(12):1341–1355

    CAS  PubMed  Google Scholar 

  • Becker S, Webster A, Doyle RL, Martins JR, Reck J, Klafke GM (2019) Resistance to deltamethrin, fipronil and ivermectin in the brown dog tick, Rhipicephalus sanguineus sensu stricto, Latreille (Acari: Ixodidae). Ticks Tick Dis 10(5):1046–1050

    Google Scholar 

  • Blagburn BL, Vaughan JL, Lindsay DS, Tebbitt GL (1994) Efficacy dosage titration of lufenuron against developmental stages of fleas (Ctenocephalides felis felis) in cats. Am J Vet Res 55(1):98–101

    CAS  PubMed  Google Scholar 

  • Bloomquist JR (2003) Chloride channels as tools for developing selective insecticides. Arch Insect Biochem Physiol 54(4):145–156

    CAS  PubMed  Google Scholar 

  • Castro-Janer E, Rifran L, Piaggio J, Gil A, Miller RJ, Schumaker TTS (2009) In vitro tests to establish LC50 and discriminating concentrations for fipronil against Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) and their standardization. Vet Parasitol 162(1–2):120–128

    CAS  PubMed  Google Scholar 

  • Castro-Janer E, Martins JR, Mendes MC, Namindome A, Klafke GM, Schumaker TTS (2010) Diagnoses of fipronil resistance in Brazilian cattle ticks (Rhipicephalus (Boophilus) microplus) using in vitro larval bioassays. Vet Parasitol 173(3–4):300–306

    CAS  PubMed  Google Scholar 

  • Castro-Janer E, Rifran L, Gonzalez P, Niell C, Piaggio J, Gil A, Schumaker TTS (2011) Determination of the susceptibility of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) to ivermectin and fipronil by Larval Immersion Test (LIT) in Uruguay. Vet Parasitol 178(1–2):148–155

    CAS  PubMed  Google Scholar 

  • Castro-Janer E, Klafke GM, Capurro MDL, Schumaker TTS (2015) Cross-resistance between fipronil and lindane in Rhipicephalus (Boophilus) microplus. Vet Parasitol 210(1–2):77–83

    CAS  PubMed  Google Scholar 

  • Chigure GM, Sharma AK, Kumar S, Fular A, Sagar SV, Nagar G, Upadhaya D, Saravanan BC, Kumar R, Ghosh S (2018) Role of metabolic enzymes in conferring resistance to synthetic pyrethroids, organophosphates, and phenylpyrazole compounds in Rhipicephalus microplus. Int J Acarol 44(1):28–34

    Google Scholar 

  • Cole LM, Nicholson RA, Casida JE (1993) Action of phenylpyrazole insecticides at the GABA-gated chloride channel. Est Biochem Physiol 46:47–54

    CAS  Google Scholar 

  • Cuore U, Solari MA (2014) Multiresistant population of Rhipicephalus (Boophilus) microplus ticks in Uruguay. Veterinaria (Montevideo) 50(193):4–13

    Google Scholar 

  • Cuore U, Trelles A, Sanchı´s J, Gayo V, Solari MA (2007) Primer diagno´ stico de resistencia al Fipronil en la garrapatacomu´ n del Ganado Boophilus microplus. Veterinaria (Montevideo) 42:35–41

    Google Scholar 

  • Cutullé C, Lovis L, D’Agostino BI, Balbiani GG, Morici G, Citroni D, Reggi J, Caracostantogolo JL (2013) In vitro diagnosis of the first case of amitraz resistance in Rhipicephalus microplus in Santo Tomé (Corrientes), Argentina. Vet Parasitol 192(1–3):296–300

    PubMed  Google Scholar 

  • Davari B, Vatandoost H, Oshaghi MA, Ladonni H, Enayati AA, Shaeghi M, Basseri HR, Rassi Y, Hanafi-Bojd AA (2007) Selection of Anopheles stephensi with DDT and dieldrin and cross-resistance spectrum to pyrethroids and fipronil. Pestic Biochem Physiol 89(2):97–103

    CAS  Google Scholar 

  • Drummond REA, Ernst SE, Trevino JL, Gladney WJ, Graham OH (1973) Boophilus annulatus and B. microplus: laboratory tests of insecticides. J Econ Entomol 66(1):130–133

    CAS  PubMed  Google Scholar 

  • Dunley JE, Brunner JF, Doerr MD, Beers H (2006) Resistance and cross-resistance in populations of the leaf rollers, Choristoneura rosaceana and Pandemis pyrusana, in Washington apples. J Insect Sci 6(1):14

    PubMed Central  Google Scholar 

  • Durham EW, Scharf ME, Siegfried BD (2001) Toxicity and neurophysiologic effects of fipronil and its oxidative sulfone metabolite on European corn borer larvae (Lepidoptera: Crambidae). Pestic Biochem Physiol 71:97–106

    CAS  Google Scholar 

  • Dutta S, Godara R, Katoch R, Yadav A, Katoch M, Singh NK (2017) Detection of amitraz and malathion resistance in field populations of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) in Jammu region of India. Exp Appl Acarol 71(3):291–301

    CAS  PubMed  Google Scholar 

  • Finney DJ (1962) Probit analysis; a statistical treatment of the sigmoid response curve. Cambridge University Press, New York, pp 1–318

    Google Scholar 

  • Fujii T, Sanada-Morimura S, Oe T, Ide M, Than DV, Chie HV, Tuon PV, Lo P, Cuong LQ, Liu ZW, Zhu ZR (2019) Long‐term field insecticide susceptibility data and laboratory experiments reveal evidence for cross resistance to other neonicotinoids in the imidacloprid‐resistant brown plant hopper Nilaparva talugens. Pest Manag Sci. doi:https://doi.org/10.1002/ps.5533

    Article  PubMed  Google Scholar 

  • Fular A, Sharma AK, Kumar S, Nagar G, Chigure G, Ray DD, Ghosh S (2018) Establishment of a multi-acaricide resistant reference tick strain (IVRI-V) of Rhipicephalus microplus. Ticks Tick Borne Dis 9(5):1184–1191

    PubMed  Google Scholar 

  • George JE (2000) Present and future technologies for tick control. Ann NY Acad Sci 916(1):583–588

    CAS  PubMed  Google Scholar 

  • Ghosh S, Azhahianambi P (2007) Laboratory rearing of Theileria annulata-free Hyalomma anatolicum anatolicum ticks. Exp Appl Acarol 43(2):137–146

    CAS  PubMed  Google Scholar 

  • Ghosh S, Bansal GC, Gupta SC, Ray DD, Khan MQ, Irshad H, Shahiduzzaman MD, Seitzer U, Ahmed JS (2007) Status of tick distribution in Bangladesh, India and Pakistan. Parasitol Res 101(2):207–216

    Google Scholar 

  • Ghosh S, Kumar R, Nagar G, Kumar S, Sharma AK, Srivastava A, Kumar S, Kumar KA, Saravanan BC (2015) Survey of acaricides resistance status of Rhipiciphalus (Boophilus) microplus collected from selected places of Bihar, an eastern state of India. Ticks Tick Dis 6(5):668–675

    Google Scholar 

  • Ghosh S, Gupta S, Kuma KA, Sharma AK, Kumar S, Nagar G, Kumar R, Paul S, Fular A, Chigure G, Nandi A (2017) Characterization and establishment of a reference deltamethrin and cypermethrin resistant tick line (IVRI-IV) of Rhipicephalus (Boophilus) microplus. Pestic Biochem Physiol 138:66–70

    CAS  PubMed  Google Scholar 

  • Guerrero FD, Lovis L, Martins JR (2012) Acaricide resistance mechanisms in Rhipicephalus (Boophilus) microplus. Rev Bras Parasitol Vet 21(1):1–6

    PubMed  Google Scholar 

  • Guerrero FD, Pérez de León A, Rodríguez-Vivas RI, Jonsson N, Miller RJ, Andreotti R (2014) Acaricide research and development, resistance and resistance monitoring. In: Sonenshine DE, Roe RR (eds) Biology of ticks, 2nd ed. Oxford University Press, New York, pp 353–381

    Google Scholar 

  • Guglielmone AA, Volpogni MM, Mangold AJ, Anziani OS, Castelli MC (2000) Evaluación de unaformulacióncomercial “pour on” con fipronil al 1% para el control de Haematob iairritans en vaquillonas Holando natural mentein festadas. Veterinaria (Argentina) 17:108–113

    Google Scholar 

  • Klafke GM, Sabatini GA, Thais A, Martins JR, Kemp DH, Miller RJ, Schumaker TT (2006) Larval immersion tests with ivermectin in populations of the cattle tick Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) from State of Sao Paulo, Brazil. Vet Parasitol 142(3–4):386–390

    CAS  PubMed  Google Scholar 

  • Klafke G, Webster A, Agnol BD, Pradel E, Silva J, de La Canal LH, Becker M, Osório MF, Mansson M, Barreto R, Scheffer R (2017) Multiple resistance to acaricides in field populations of Rhipicephalus microplus from Rio Grande do Sul state, Southern Brazil. Ticks Tick Dis 8(1):73–80

    Google Scholar 

  • Kostromytska OS, Wu S, Koppenhöfer AM (2018) Diagnostic dose assays for the detection and monitoring of resistance in adults from listronotus maculicollis (Coleoptera: Curculionidae) populations. J Econ Entomol 111(5):2329–2339

    CAS  PubMed  Google Scholar 

  • Kristensen M, Jespersen JB, Knorr M (2004) Cross-resistance potential of fipronil in Musca domestica. Pest Manag Sci 60(9):894–900

    CAS  PubMed  Google Scholar 

  • Kristensen M, Hansen KK, Jensen KMV (2005) Cross-resistance between dieldrin and fipronil in German cockroach (Dictyoptera: Blattellidae). J Econ Entomol 98(4):1305–1310

    CAS  PubMed  Google Scholar 

  • Kumar S, Sharma AK, Nagar G, Ghosh S (2015) Determination and establishment of discriminating concentrations of malathion, coumaphos, fenvalerate and fipronil for monitoring acaricide resistance in ticks infesting animals. Ticks Tick Dis 6(3):383–387

    Google Scholar 

  • Lew-Tabor AE, Valle MR (2016) A review of reverse vaccinology approaches for the development of vaccines against ticks and tick borne diseases. Ticks Tick Dis 7(4):573–585

    CAS  Google Scholar 

  • Liu N, Yue X (2000) Insecticide resistance and cross-resistance in the house fly (Diptera: Muscidae). J Econ Entomol 93(4):1269–1275

    CAS  PubMed  Google Scholar 

  • Lorini I, Galley D (2001) The cross-resistance spectrum in deltamethrin resistance strains of Rhyzopertha dominica (F.) (Coleoptera: Bostrychidae). Neotrop Entomol 30(2):321–325

    CAS  Google Scholar 

  • Lovis L, Perret JL, Bouvier J, Fellay JM, Kaminsky R, Betschart B, Sager H (2011) A new in vitro test to evaluate the resistance level against acaricides of the cattle tick, Rhipicephalus (Boophilus) microplus. Vet Parasitol 182(2–4):269–280

    CAS  PubMed  Google Scholar 

  • Lovis L, Reggi J, Berggoetz M, Betschart B, Sager H (2013) Determination of acaricide resistance in Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) field populations of Argentina, South Africa, and Australia with the larval tarsal test. J Med Entomol 50(2):326–335

    CAS  PubMed  Google Scholar 

  • Martins JR, Furlong J (2001) Avermectin resistance of the cattle tick Boophilus microplus in Brazil. Vet Rec 149(2):64–64

    CAS  PubMed  Google Scholar 

  • Martins JR, Doyle RL, Gonzales JC (2006) Principais resultados de testes carrapaticidas in vitro empregando-se o teste de imersão de adultos no IPVDF, Eldorado do Sul, RS. In: Anais do 14◦ Congresso Brasileiro de ParasitologiaVeterinária, RibeirãoPreto, SP, Brazil 218

  • Miller RJ, Davey RB, George JE (2005) First report of organophosphate-resistant Boophilus microplus (Acari: Ixodidae) within the United States. J Med Entomol l42(5):912–917

    Google Scholar 

  • Miller RJ, Almazán C, Ortíz Estrada M, Davey RB, George JE, Pérez de León A (2013) First report of fipronil resistance in Rhipicephalus (Boophilus) microplus of Mexico. Vet Parasitol 191:97–10

    CAS  PubMed  Google Scholar 

  • Nandi A, Sagar SV, Chigure G, Fular A, Sharma AK, Nagar G, Kumar S, Saravanan BC, Ghosh S (2018) Determination and validation of discriminating concentration of ivermectin against Rhipicephalus microplus. Vet Parasitol 250:30–34

    CAS  PubMed  Google Scholar 

  • Reck J, Klafke GM, Webster A, Dall’Agnol B, Scheffer R, Souza UA, Corassini VB, Vargas R, dos Santos JS, de Souza Martins JR (2014) First report of fluazuron resistance in Rhipicephalus microplus: a field tick population resistant to six classes of acaricides. Vet Parasitol 201(1–2):128–136

    CAS  PubMed  Google Scholar 

  • Rodríguez-Vivas RI, Apanaskevich DA, Ojeda-Chi MM, Trinidad-Martínez I, Reyes-Novelo E, Esteve-Gassent MD, de León AP (2016) Ticks collected from humans, domestic animals, and wildlife in Yucatan, Mexico. Vet Parasitol 215:106–113

    PubMed  Google Scholar 

  • Sabatini GA, Kemp DH, Hughes S, Nari A, Hansen J (2001) Test to determine LC50 and discriminating doses for macrocyclic lactones against the cattle tick Boophilus microplus. Vet Parasitol 95:53–62

    CAS  PubMed  Google Scholar 

  • Sagar SV, Saini K, Sharma AK, Kumar S, Kumar R, Fular A, Shakya M, Upadhaya D, Nagar G, Shanmuganath C, Samanta S (2019) Acaricide resistance in Rhipicephalus microplus collected from selected districts of Madhya Pradesh, Uttar Pradesh and Punjab states of India. Trop Anim Health Prod. doi.https://doi.org/10.1007/s11250-019-02048-0

    Article  PubMed  Google Scholar 

  • Sato ME, Silva MZD, Raga A, Souza Filho MFD (2005) Abamectin resistance in Tetranychus urticae Koch (Acari: Tetranychidae): selection, cross-resistance and stability of resistance. Neotrop Entomol 34(6):991–998

    CAS  Google Scholar 

  • Sharma AK, Kumar R, Kumar S, Nagar G, Singh NK, Rawat SS, Dhakad ML, Rawat AKS, Ray DD, Ghosh S (2012) Deltamethrin and cypermethrin resistance status of Rhipicephalus (Boophilus) microplus collected from six agro-climatic regions of India. Vet Parasitol 188(3–4):337–345

    CAS  PubMed  Google Scholar 

  • Singh NK, Vemu B, Nandi A, Singh H, Kumar R, Dumka VK (2014) Laboratory assessment of acaricidal activity of Cymbopogon winterianus, Vitex negundo and Withania somnifera extracts against deltamethrin resistant Hyalomma anatolicum. Exp Appl Acarol 63(3):423–430

    PubMed  Google Scholar 

  • Sugimoto N, Osakabe M (2014) Cross-resistance between cyenopyrafen and pyridaben in the two spotted spider mite Tetranychus urticae (Acari: Tetranychidae). Pest Manag Sci 70(7):1090–1096

    CAS  PubMed  Google Scholar 

  • Van Wyk RD, Baron S, Maritz-Olivier C (2016) An integrative approach to understanding pyrethroid resistance in Rhipicephalus microplus and R. decoloratus ticks. Ticks Tick Dis 7(4):586–594

    Google Scholar 

  • Wen Z, Scott JG (1999) Genetic and biochemical mechanisms limiting fipronil toxicity in the LPR strain of house fly, Musca domestica. Pestic Sci 55(10):988–992

    CAS  Google Scholar 

  • White WH, Plummer PR, Kemper CJ, Miller RJ, Davey RB, Kemp DH, Hughes S, Smith II, CK, Gutie´ rrez JA (2004) An in vitro larval immersion microassay for identifying and characterizing candidate acaricides. J Med Entomol 41:1034–1042

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Zhang Y, Han Y, Liu B, Yan Q, Guo H, Liu Z, Wang L, Fang J (2017) Resistance monitoring and cross-resistance role of CYP6CW1 between buprofezin and pymetrozine in field populations of Laodelphax striatellus (Fallén). Sci Rep 7(1):14639

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgement

The authors are grateful to the Indian Council of Agricultural Research, New Delhi, for funding through the National Agricultural Science Fund [NASF/ABA-6015/2016-17/357] and Department of Science and Technology, New Delhi (DST-SERB-PDF/2016/001816).

Author information

Authors and Affiliations

  1. Entomology Laboratory, Division of Parasitology, ICAR-Indian Veterinary Research Institute, Izatnagar, Bareilly, U.P., 243122, India

    Mukesh Shakya, Sachin Kumar, Ashutosh Fular, Deepak Upadhaya, Anil Kumar Sharma, Nisha Bisht, Abhijit Nandi & Srikant Ghosh

Authors
  1. Mukesh Shakya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sachin Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ashutosh Fular
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Deepak Upadhaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anil Kumar Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nisha Bisht
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Abhijit Nandi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Srikant Ghosh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Srikant Ghosh.

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

Shakya, M., Kumar, S., Fular, A. et al. Emergence of fipronil resistant Rhipicephalus microplus populations in Indian states. Exp Appl Acarol 80, 591–602 (2020). https://doi.org/10.1007/s10493-020-00481-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10493-020-00481-7

Keywords

Search

Navigation