Abstract
The isolates of Rhipicephalus microplus collected from Madhya Pradesh (MP), Punjab (PJB) and Uttar Pradesh (UP) states of India were characterized using laboratory standardized adult immersion test (AIT) against macrocyclic lactone (ivermectin), synthetic pyrethroids (cypermethrin and deltamethrin), organophosphates (coumaphos and diazinon) and phenylpyrazole compounds (fipronil). Out of the six isolates tested, five isolates except MTH were resistant to deltamethrin and cypermethrin at level II with RF ranging from 16.4 to 24.02 and 7.05 to 13.2, respectively. In case of organophosphates, coumaphos was less effective showing resistance level II (RF 8.52–11.2) in all the six populations compared with diazinon to which three isolates (MHW, RWA and AGS) were resistant at level II. Except MTH, other five isolates were categorized at level I with RF ranging from 1.53 to 3.02 against ivermectin. The phenylpyrazole compound however was found effective, and none of the isolates could survive at a discriminating concentration. The possible strategy for the management of multi-acaricide-resistant ticks in the surveyed districts was discussed in the present study.
Similar content being viewed by others
References
Adehan, S.B., Biguezoton, A., Adakal, H., Assogba, M.N., Zoungrana, S.E., Gbaguidi, A.M., Tonouhewa, A., Kandé, S., Achi, L., Kagone, H. and Adehan, R., 2016. Acaricide resistance of R. microplus ticks in Benin. African Journal of Agricultural Research, 11, 1199–1208
Ahanger, R.R., Godara, R., Katoch, R., Yadav, A., Bhutyal, A.D., Katoch, M., Singh, N.K. and Bader, M.A., 2015. Deltamethrin resistance in field populations of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) in Jammu and Kashmir, India. Experimental and Applied Acarology, 67, 467–475
Benavides, O.E., Romero, N,A., Rodriguez, J.L. and Silva, Z.J., 1999. Evidencia preliminar de la aparicion de resistenciaa lactonas macrociclicas en cepas de garrapata Boophilus microplus en Colombia. Memorias IV Seminarios Internacional de Parasitologia, Puerto Vallarta, Jalisco, Mexico, 20, 20–22
Brito, L.G., Barbieri, F.S., Rocha, R.B., Oliveira, M.C.S. and Elisana, E.S., 2011. Evaluation of the efficacy of acaricides used to control the cattle tick, Rhipicephalus microplus, in dairy herds raised in the Brazilian south western amazon. Veterinary Medicine International, 201, 2–13
Buttar, B.S., Rai, H.S., Singh, N.K., Jyoti, Haque, M. and Rath, S.S., 2012. Emergence of anthelmintic resistance in an organized sheep farm in Punjab. Journal of Veterinary Parasitology, 26, 69–71
Castro-Janer, E., Rifran, L., González, P., Piaggio, J., Gil, A. and Schumaker, T.T., 2010a. Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) resistance to fipronil in Uruguay evaluated by in vitro bioassays. Veterinary Parasitology, 169, 172–177
Castro-Janer, E., Martins, J.R., Mendes, M.C., Namindome, A., Klafke, G.M. and Schumaker, T.T.S., 2010b. Diagnoses of fipronil resistance in Brazilian cattle ticks (Rhipicephalus (Boophilus) microplus) using in vitro larval bioassays. Veterinary Parasitology, 173, 300–306
Chigure, G.M., Sharma, A.K., Kumar, S., Fular, A., Sagar, S.V., Nagar, G., Upadhaya, D., Saravanan, B.C., Kumar, R. and Ghosh, S., 2018. Role of metabolic enzymes in conferring resistance to synthetic pyrethroids, organophosphates, and phenylpyrazole compounds in Rhipicephalus microplus. International Journal of Acarology, 44, 28–34
Cutullé, C., Lovis, L., D’Agostino, B.I., Balbiani, G.G., Morici, G., Citroni, D., Reggi, J. and Caracostantogolo, J.L., 2013. In vitro diagnosis of the first case of amitraz resistance in Rhipicephalus microplus in Santo Tomé (Corrientes), Argentina. Veterinary Parasitology, 192, 296–300
Devaney, E. and Devaney, E., 2013. Genetic and genomic approaches to understanding drug resistance in parasites. Parasitology, 140, 1451
Drummond, R.E., Ernst, S.E., Trevino, J.L., Gladney, W.J. and Graham, O.H., 1973. Boophilus annulatus and B. microplus: laboratory tests of insecticides. Journal of Economic Entomology, 66, 130–133
Dutta, S., Godara, R., Katoch, R., Yadav, A., Katoch, M. and Singh, N.K., 2017. Detection of amitraz and malathion resistance in field populations of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) in Jammu region of India. Experimental and Applied Acarology, 71, 291–301
FAO., 2004. Resistance management and integrated parasite control in ruminants. Guidelines. Animal Production and Health Division, Rome: FAO, p. 25–77
Fernández-Salas, A., Rodríguez-Vivas, R.I. and Alonso-Díaz, M.A., 2012. First report of a R. micorplus tick population multi-resistant to acaricides and ivermectin in the Mexican tropics. Veterinary Parasitology, 183, 338–342
Finney, D.J., 1962. Probit Analysis – A Statistical Treatment of the Response Curve. Cambridge University Press, Cambridge, pp.1–318
Fular, A, Sharma, A.K., Kumar, S., Nagar, G., Chigure, G., Ray, D.D. and Ghosh, S., 2018. Establishment of a multi-acaricide resistant reference tick strain (IVRI-V) of Rhipicephalus microplus. Ticks and Tick-borne Diseases, https://doi.org/10.1016/j.ttbdis.2018.04.014
Ghosh, S. and Azhahianambi, P., 2007. Laboratory rearing of Theileria annulata – free Hyalomma anatolicum anatolicum ticks. Experimental and Applied Acarology, 43, 137–146
Ghosh, S., Azhahianambi, P. and Yadav, M.P., 2007. Upcoming and future strategies of tick control: a review. Journal of Vector Borne Diseases, 44, 79–89
Ghosh, S., Kumar, R., Nagar, G., Kumar, S., Sharma, A,K., Srivastava, A., Kumar, S., Kumar, K.A. and Saravanan, B.C., 2015. Survey of acaricides resistance status of Rhipiciphalus (Boophilus) microplus collected from selected places of Bihar, an eastern state of India. Ticks and Tick-borne Diseases, 6, 668–675
Graf, J.F., Gogolewski, R., Leach-, N., Sabatini, G.A., Molento, M.B., Bordin, E.L. and Arantes, G.J., 2004. Tick control: an industry point of view. Parasitology, 129, S427-S442
Higa, L.O.S., Garcia, M.V., Barros, J.C., Koller, W.W. and Andreotti, R., 2015. Acaricide Resistance Status of the Rhipicephalus microplus in Brazil: A Literature Overview. Medical Chemistry, 5, 326–333
Jonsson, N.N., and Hope, M., 2007. Progress in the epidemiology and diagnosis of amitraz resistance in the cattle tick Boophilus microplus. Veterinary Parasitology, 146, 193–198
Jonsson, N.N., Miller, R.J. and Robertson, J.L., 2007. Critical evaluation of the modified-adult immersion test with discriminating dose bioassay for Boophilus microplus using American and Australian isolates. Veterinary Parasitology, 146, 307–315
Jyothimol, G., Ravindran, R., Juliet, S., Ajith Kumar, K.G., Suresh, N.N., Vimalkumar, M.B., Lenka, D.R., Varghese, S. and Ghosh, S. 2014. Low level deltamethrin resistance in ticks from cattle of Kerala, a south Indian state. Veterinary Parasitology, 204, 433–438
Khangembam, R., Singh, H., Rath, S.S. and Singh N.K., 2018. Effect of synergists on ivermectin resistance in field populations of Rhipicephalus (Boophilus) microplus from Punjab districts, India. Ticks and Tick-borne Diseases, 9, 682–686
Klafke, G.M., Castro-Janer, E., Mendes, M.C., Namindome, A. and Schumaker, T.T.S., 2012. Applicability of in vitro bioassays for the diagnosis of ivermectin resistance in R. microplus (Acari: Ixodidae). Veterinary Parasitology, 184, 212–220
Kumar, S., Paul, S., Sharma, A.K., Kumar, R., Tewari, S.S., Chaudhuri, P., Ray, D.D., Rawat, A.K.S. and Ghosh, S., 2011. Diazinon resistant status in Rhipicephalus (Boophilus) microplus collected from different agro-climatic regions of India. Veterinary Parasitology, 181, 274–281
Kumar, Rinesh, Nagar, G., Sharma, A.K., Kumar, S., Ray, D.D., Chaudhuri, P. and Ghosh, S., 2013. Survey of pyrethroids resistance in Indian isolates of Rhipicephalus (Boophilus) microplus: identification of C190A mutation in the domain II of the para-sodium channel gene. Acta Tropica, 125, 237–245
Kumar, S., Sharma, A.K., Nagar, G. and Ghosh, S., 2015. Determination and establishment of discriminating concentrations of malathion, coumaphos, fenvalerate and fipronil for monitoring acaricide resistance in ticks infesting animals. Ticks and Tick-borne Diseases, 6, 383–387
Kumar, S., Sharma, A.K., Nagar, G., Rawat, S.S., Tiwari, S.S., Kumar, R., Dhakad, M.L., Sharma, R.K., Saxana, R.K., Mehraniya, R.S. and Singh, R.S., 2016. Characterization of acaricide resistance in tick isolates collected from Rajasthan, India. Indian Journal of Animal Sciences, 86, 14–23
Lenka, D.R., Ravindran, R., Jyothimol, G., Udaykumar, M., Reddy, P.M.T., Sathish, N., Palla, I., Chandramohan, B., Ajithkumar, K.G., Nair, S.N. and Chandrasekhar, L., 2016. Deltamethrin resistance in south Indian isolates of Rhipicephalus (Boophilus) microplus. Veterinary Parasitology (Amst), 5, 37–41
Lovis, L., Mendes, M.C., Perret, J.L., Martins, J.R., Bouvier, J., Betschart, B. and Sager, H., 2013. Use of the Larval Tarsal Test to determine acaricide resistance in Rhipicephalus (Boophilus) microplus Brazilian field populations. Veterinary Parasitology, 191, 323–331
Martins, J.R. and Furlong, J., 2001. Avermectin resistance of the cattle tick Boophilus microplus in Brazil. The Veterinary Record, 149, 64–64
Minjauw, B. and McLeod, A., 2003. In: Tick-borne diseases and poverty: the impact of ticks and tick-borne diseases on the livelihoods of small-scale and marginal livestock owners in India and eastern and southern Africa. 24
Nandi, A., Singh, H., Singh, N.K. and Rath, S.S., 2016. Fenvalerate resistance status in Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) from Punjab, India. Journal of Parasitic Diseases, 40, 694–698
Nandi, A., Sagar, S.V., Chigure, G., Fular, A., Sharma, A.K., Nagar, G., Kumar, S., Saravanan, B.C. and Ghosh, S., 2018. Determination and validation of discriminating concentration of ivermectin against Rhipicephalus microplus. Veterinary Parasitology, 250, 30–34
Perez-Cogollo, L.C., Rodriguez-Vivas, R.I., Ramirez-Cruz, G.T. and Miller, R.J., 2010. First report of the cattle tick Rhipicephalus microplus resistant to ivermectin in Mexico. Veterinary Parasitology, 168, 165–169
Pradeep, B.S., Renukaprasad, C. and Souza, P.E., 2012. Evaluation of the commonly used acaricides against different stages of the cattle tick Boophilus microplus by using different in vitro tests. Indian Journal of Animal Research, 46, 248–252
Ravindran, R., Ajith Kumar, K.G., Suresh, N.N., Amithamol, K.K., Sunil, A.R., Adarshkrishna, T.P., Chithra, N.D., Jyothimol, G., Ghosh, S. and Juliet, S., 2014. Acaricidal effects of fenvalerate and cypermethrin against Rhipicephalus (Boophilus) annulatus. Tropical Biomedicine, 31, 449–455
Rodríguez-Vivas, R.I., Pérez-Cogollo, L.C., Rosado-Aguilar, J.A., Ojeda-Chi, M.M., Trinidad-Martinez, I., Miller, R.J., Li, A.Y., de León, A.P., Guerrero, F. and Klafke, G., 2014. Rhipicephalus (Boophilus) microplus resistant to acaricides and ivermectin in cattle farms of Mexico. Revista Brasileira de Parasitologia Veterinária, 23, 113–122
Sabatini, G.A., Kemp, D.H., Hughes, S., Nari, A. and Hansen, J., 2001. Test to determine LC50 and discriminating doses for macrocyclic lactones against the cattle tick Rhipicephalus (Boophilus) microplus. Veterinary Parasitology, 95, 53–62
Sharma, A.K., Kumar, R., Kumar, S., Nagar, G., Singh, N.K., Rawat, S.S., Dhakad, M.L., Rawat, A.K.S., Ray, D.D. and Ghosh, S., 2012. Deltamethrin and cypermethrin resistance status of Rhipicephalus (Boophilus) microplus collected from six agro-climatic regions of India. Veterinary Parasitology, 188, 337–345
Shyma, K.P., Kumar, S., Sangwan, A.K., Sharma, A.K., Nagar, G., Ray, D.D. and Ghosh, S., 2013. Acaricide resistance status of Rhipicephalus (Boophilus) microplus and Hyalomma anatolicum collected from Haryana. Indian Journal of Animal Sciences, 83, 591–594
Singh, N.K. and Rath, S.S. 2014. Esterase mediated resistance against synthetic pyrethroids in field populations of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) in Punjab districts of India. Veterinary Parasitology, 204, 330–338
Singh, N.K., Haque, M. and Jyoti, S.S., 2010. Studies on acaricide resistance in Rhipicephalus (Boophilus) microplus against synthetic pyrethroids by adult immersion test with a discriminating dose. Journal of Veterinary Parasitology, 24, 207–208
Singh, N.K., Haque, M., Singh, H., Rath, S.S. and Ghosh, S., 2014. A comparative study on cypermethrin resistance in Rhipicephalus (Boophilus) microplus and Hyalomma anatolicum from Punjab (India). Ticks and Tick-borne Diseases, 5, 90–94
Singh, N.K., Singh, H., Prerna, M. and Rath, S.S. 2015a. First report of ivermectin resistance in field populations of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) in Punjab districts of India. Veterinary Parasitology, 214, 192–194
Singh, N.K., Gelot, I.S., Singh, V. and Rath, S.S, 2015b. Detection of amitraz resistance in Rhipicephalus (Boophilus) microplus from North Gujarat, India. Journal of Parasitic Diseases, 39, 49–52
Vatsya, S. and Yadav, C.L., 2011. Evaluation of acaricide resistance mechanisms in field populations of Rhipicephalus (Boophilus) microplus collected from India. International Journal of Acarology, 37, 405–410
Vudriko, P., Okwee-Acai, J., Tayebwa, D.S., Byaruhanga, J., Kakooza, S., Wampande, E. and Suzuki, H., 2016. Emergence of multi-acaricide resistant Rhipicephalus ticks and its implication on chemical tick control in Uganda. Parasites & Vectors, 9, 4
Wharton, R.H., 1974. Ticks with Special Emphasis on Boophilus Microplus. In: Pal R., Wharton R.H. (eds) Control of Arthropods of Medical and Veterinary Importance. Springer, Boston, MA
Funding
The authors received funding from the Indian Council of Agricultural Research, New Delhi, through the National Agricultural Science Fund (Grant number NASF/ABA-6015/2016-17/357 and NFBDFARA/BSA-4004/2013-14) and Department of Science and Technology, New Delhi (DST-SERB-PDF/2016/001816).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Necessary permission to use large animals for tick feeding was taken from the regulatory authority: Committee for the Purpose of Control and Supervision of Experimentation on Animals (CPCSEA).
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Sagar, S.V., Saini, K., Sharma, A.K. et al. Acaricide resistance in Rhipicephalus microplus collected from selected districts of Madhya Pradesh, Uttar Pradesh and Punjab states of India. Trop Anim Health Prod 52, 611–618 (2020). https://doi.org/10.1007/s11250-019-02048-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11250-019-02048-0