Review articleMenace of acaricide resistance in cattle tick, Rhipicephalus microplus in India: Status and possible mitigation strategies
Introduction
India is predominantly an agriculture dominated country. It is home to the world’s largest bovine population of 299.9 million which includes 190.90 million cattle and 108.7 million buffaloes (DAHD, 2015) accounting for 16.2 and 56.9 %, respectively, of the world bovine population. Despite very low productivity per animal, India stands first in the world milk production accounting for 20 % of world output (DAHD, 2018). The livestock sector is significantly contributing to the Indian economy by providing milk, meat, bones and hides. Apart from this, livestock plays a major role in maintaining soil fertility, energy production and rural transportation. The overall contribution of the livestock sector in total GDP is nearly 4.11 % at current prices during 2012–13 (DAHD, 2015). However, this sector is sufferings from many health related problems posed by bacteria, viruses, fungi, and parasites (both endo and ectoparasites). Of the different problems, management of the multidimensional problems created by tick infestations is very challenging. Due to ideal environmental conditions, almost all the economically important livestock species are suffering from ticks and tick-borne diseases (TTBDs) (Ghosh et al., 2007). In a questionnaire survey, the control cost of TTBDs in India has been estimated at the tune of 498.7 million US$/annum (Minjauw and McLeod, 2003).
In India, the problem of TTBDs is particularly relevant because of large-scale maintenance of susceptible crossbred animals to improve and sustain the production of milk and milk products. Despite efforts have been made to develop other non-chemical methods to manage ticks, the use of chemical acaricides is still a predominant approach implemented in the field (Ghosh and Nagar, 2014). Amongst 106 valid tick species reported from India, R. microplus is widely prevalent and is the most damaging species infesting livestock, zoo and wild animals (Ghosh et al., 2007). Due to short and single host life cycle with high fecundity, the R. microplus has been subjected to maximum exposure of acaricides and thus developed a remarkable ability to become resistant to the toxic effect of the chemicals used to manage them. Globally, R. microplus has become resistant to almost all the classes of chemicals that are registered for use against it, for example; against organophosphates and carbamates (Li et al., 2005; Kumar et al., 2011); pyrethroids (Ghosh et al., 2015; Klafke et al., 2017a); amidines (Miller et al., 2002; Klafke et al., 2017b); macrocyclic lactones (Martins and Furlong, 2001; Perez-Cogollo et al., 2010a; Klafke et al., 2017a; Nandi et al., 2018); fipronil (Castro-Janer et al., 2010; Klafke et al., 2017a) and against fluazuron (Reck et al., 2014).
The tick management programme is focused on repeated use of organophosphates, pyrethroids, formamidines and macrocyclic lactones. Uses of formamidines (amitraz) and macrocyclic lactones (ivermectin) are comparatively less but on the rise due to the declining efficiency of organophosphates and pyrethroids acaricide. By a questionnaires survey in sampled population, FAO (2004) predicted the establishment of widespread acaricidal resistance tick populations in India. Later, with the establishment of country specific discriminating concentration (DC) of commonly used acaricides, the reports of resistance and the possible mechanism of development of acaricidal resistance in R. microplus against various types of acaricide are published from different parts of the country (Singh et al., 2010; Kumar et al., 2011; Sharma et al., 2012; Kumar et al., 2013; Jyothimol et al., 2014; Kumar et al., 2014; Singh et al., 2015a; Kumar et al., 2017; Nagar et al., 2018; Sharma et al., 2018; Godara et al., 2019) (Table 3).
The purpose of this review is to appraise the overall acaricide resistance scenario and to provide an overview of the current state of knowledge, research gaps, present and future national initiatives required to combat the menace of the complex problem.
Section snippets
Establishment of a reference tick strains of Rhipicephalus microplus for resistance characterization
Due to non-availability of reference tick strains, no country specific bioassays, biochemical and molecular assays were standardized until 2011 for the assessment of resistance. The systematic work on resistant characterization was started after national initiatives through World Bank funded, National Agricultural Innovation Project (Project No. NAIP/Comp-4/ C2066/2008-09) in the year 2008. In the subsequent years, reference strains, a prerequisite for resistance characterization, were
Acaricide resistance pattern in India
More than half a century ago, Chaudhuri and Naithani (1964) reported that the R. micropluspopulation-infesting cattle stationed at the Latoli kraal of the Indian Veterinary Research Institute, Mukteswar, has developed resistance to benzene hexachloride (BHC). Later, resistance to carbaryl, a broad-spectrum carbamate pesticide, was reported by Basu and Haldar (1997). Sporadic reports of resistance were published time to time but in most of the experiments the efficacy of commercially available
Metabolic detoxification of enzymes
Ticks are using a detoxifying enzyme system to break down or sequester broad spectrum of acaricides due to its wide substrate specificity. Metabolic resistance mediated by detoxifying enzymes such as esterases, glutathione S-transferases (GST) and Cytochrome P450 monoxygenases are reportedly involved in conferring resistance against ticks (Crampton et al., 1999; Jamroz et al., 2000; Enayati et al., 2010; Temeyer et al., 2013). The involvement of the esterases in development of resistance to
Contributing factors in resistance development
Based on the managemental practices and infrastructure, the farm types are classified as organized and unorganized. The animal sheds with poor infrastructural and ventilation facilities provide ample breeding spaces for ticks in cracks and crevices for propagation. Besides, the habit of pilling cow dung cakes, farm machinery, feed, gunny bags, etc. in and around the animal sheds further add to breeding/shelter spaces in the sheds for easy proliferation of tick population.
The climatic conditions
Management of acaricide resistance
India consisting of fifteen agro-climatic zones, the implementation of a specific regime for tick management would neither be possible nor be feasible. In order to design well-structured management programs, there is an emergent need for comprehensive data about the status of acaricide resistance spanning different agro-climatic zones of the country. Therefore, periodic and appropriate monitoring of resistance using established and country specific protocol against commonly used acaricides in
Conclusion
Policy decision regarding uniform tick management strategy is not a realistic target for a country like India because in general, the livestock owners have small holdings, unorganized, with least infrastructure, and minimum knowledge about the gravity of the problem. There is an urgent need for continuous monitoring of acaricide resistance in the field situation through bioassay, biochemical and molecular tools for strategic application of available acaricides and for maintaining the life span
Declaration of Competing Interest
None.
Acknowledgements
The authors are grateful to Indian Council of Agricultural Research, New Delhi for funding through National Agricultural Science Fund [Grant number NASF/ABA-6015/2016-17/357 and NFBSFARA/BSA-4004/2013-14].
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2022, HeliyonCitation Excerpt :FAO (2004) predicted the establishment of widespread acaricide resistance in tick populations in India. Factors contributing to the development of acaricide resistance in India include poor infrastructure and management practices that provide conducive sites for the easy proliferation of ticks and climatic conditions conducive to the growth and survival of ticks throughout the year (Kumar et al., 2020). Furthermore, the liberalisation of the veterinary drug industry has made acaricides easily accessible to farmers, and limited control has led to improper dosing, higher application frequency, limited rotational use of acaricides, and non-adherence to acaricide usage principles.
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Present address: Department of Parasitology, College of Veterinary and Animal Sciences, Rewa, Madhya Pradesh, India.