Upcoming of the integrated tick control program of ruminants with special emphasis on livestock farming system in India

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Upcoming of the integrated tick control program of ruminants with special emphasis on livestock farming system in India D.B. Mondal ∗ , K. Sarma, M. Saravanan Division of Medicine, Indian Veterinary Research Institute, Izatnagar 243 122, UP, India

a r t i c l e

i n f o

Article history: Received 8 December 2011 Received in revised form 9 May 2012 Accepted 29 May 2012 Keywords: Acaricide Control Integrated Livestock Tick

a b s t r a c t Ticks and tick-borne diseases are a global problem and considered as a major obstacle in the health and product performance of animals which reflects impact on the livelihood of resource-poor farming communities. Tick control is practiced in a variety of methods including vaccination involving different livestock system. At present, periodic application of chemical acaricides is the most commonly used method of tick control especially among the small and marginal farmers of India. Resistance to existing chemical acaricides is widespread, and newer classes of acaricides have tended to be significantly more expensive. Presently, there is increasing concern about the use of chemicals in all forms of agriculture as well as livestock management by their potential environmental hazard and presence in food products. The use of herbal preparations among the rural folks is gaining importance because of their strong belief for folded benefits. Integrated control of ticks is the combination of a series of complementary control measures to make the best use of each without placing too much reliance on any single component. Alternative integrated approaches involve the use of eco-friendly cost effective sustainable methods in a strategic integrated manner. © 2012 Elsevier GmbH. All rights reserved.

Introduction Livestock production plays a very significant role for the upliftment of the rural masses and thus in national economy through generating income with their livestock. It provides livelihood security through provision of employment and sustainable household nutrition to poor and pro-poor rural masses of the countries like India. Loss of productivity from the livestock sector is of multifactorial nature. Parasitic diseases, particularly endo- and ectoparasites, are a global problem and considered a major obstacle in the health and product performance of animals. Among ectoparasites, ticks, mites, flies, fleas, midges etc. are very important and harmful as blood sucking parasites of mammals, birds, and reptiles throughout the world (Furman and Loomis, 1984). During the 19th century, as the number of cattle in the world was increased to feed the growing human populations of recently industrialized nations, there was a growing awareness of the relationship between infestations of cattle with ticks and disastrous epizootics of disease in herds of cattle. Since the mid-19th century, when the cattle industry was developing in many tropical and subtropical countries, ticks became a major economic

∗ Corresponding author. E-mail address: [email protected] (D.B. Mondal).

impediment due to cross-boundary spreading of tick infestation (Shaw, 1969). Economic impact of ticks and tick-borne diseases Globally, ticks and tick-borne diseases (TTBDs) continue to be a major constraint on profitable livestock production and productivity. Recently, TTBDs were again ranked high globally in terms of their impact on the livelihood of resource-poor farming communities in developing countries including India (Minjauw and McLeod, 2000). Ticks are rarely associated with high mortality, but decrease the output of animal products, by-products, manure etc. which contribute to production and productivity losses. TTBDs have been recognized as a major cause of production loss predominantly in tropical and subtropical countries of the world (De Castro, 1997). According to FAO (2004), 80% of the world’s cattle population is exposed to tick infestation and has estimated the impact of 7.3 US $/head/year. As per the 1997 estimates, the global production loss caused by TTBDs amounts to 13.9–18.7 billion US $ annually (De Castro, 1997). A recent estimate calculated the costs of control of TTBDs affecting Indian livestock as 498.7 million US $ per annum (Minjauw and McLeod, 2003). In India, almost all the livestock species suffer from tick infestations. Minjauw and McLeod (2003) have estimated the costs caused by T. annulata to be 384.3 million US $ and by tick worry to be 57.2 million US $ in India.

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The economic effect cannot be accurately calculated, but these cases can severely impact farm profitability, community cohesion, and can also be considered a public health issue. Reduced lactation as a result of TTBDs causes an economic loss which would be a serious proposition for a livestock-dependent system (Ghosh et al., 2006). Beside the reduction in milk production, the direct effect of tick infestation has a tremendous impact on the leather industry due to its significant damage to the hide by continuous tick piercing (Biswas, 2003; Jongejan and Uilenberg, 2004). As per leather industry report, the leather sector of India is suffering from a huge shortfall of 3000 million pieces of hide and skin per year (Anonymous, 2002) and causing 20–30% depreciation in normal value in the market (Biswas, 2003). It has been estimated that India produces only 9.8%, 63.3%, 9.2%, and 6.0% of world cattle, buffalo, goat, and sheep hides, respectively, although the country possesses the highest livestock population (Anonymous, 2002). Threats by ticks and tick-borne diseases Multiple effects of TTBDs on animal production (Fig. 1) can be classified as either primary, which the ticks affect directly, such as effects on growth or milk yield, or secondary effects such as effects on feed intake, reproduction, meat production, calf weaning weight etc., which are consequences of primary effects. Younger animals are particularly at risk since stress can interfere with early weight gain, resulting in a negative effect on productivity or growth over their lifetime. Tick bites reduce feed intake of animals due to irritation caused by feeding activities influencing the host’s metabolism. Each tick sucks not less than 30 drops of blood to complete its life cycle. Loss of blood results in retarded growth and lowered body weight. Loss of appetite in heavily tick-infested cattle was found to be responsible for 65% of the body weight reduction (Seebeck et al., 1971) considering the facts of growth rate depression equivalent to at least 450 g a year on an average due to the bites of ticks (Seebeck et al., 1971). The remaining 35% were attributable to interference with the growth process, possibly through the mediation of a tick toxin which could come from the saliva known to be injected into the host. The variation in body weight growth of the infested cattle was due to the variable effect of feeding ticks on the appetite of the cattle. The salivary glands of Dermacentor spp. produce a toxin that affects the nervous system of the host. Larvae and nymphs secrete small quantities of this toxin when they feed, but it is the larger amount injected by adult females that most commonly causes paralysis. The toxin causes changes in the terminal part of the motor nerve fiber responsible for failure of animal mobilization (Donat and Donat, 1987). Tick paralysis is chemically induced by the ticks and therefore usually only continues in its presence. Once the ticks are removed, symptoms usually diminish rapidly. However, in some cases, profound paralysis can develop and even become fatal before anyone becomes aware of a tick’s presence. The weakness of the host sets in about 5 days after attachment of the tick. The toxin appears to be excreted or metabolized rapidly, usually 12–24 h after its removal.

reached 31.6% in 2008–2009 (CSO, 2010). The agricultural sectors of India contain a variety of farming systems, including smallholder dairy, crop–livestock, and livestock-dependent. Cross-bred or exotic cattle and indigenous animals are important components of these systems. TTBDs are considered as one of the most important bottleneck in economical livestock rearing in the country. Approximately 106 tick species belonging to the families Ixodidae and Argasidae are reported to infest domestic, wild, and other animals (Geevarghese et al., 1997). Among the reported species of ticks, Amblyomma testudinarium, Dermacentor auratus, Haemaphysalis bispinosa, Haem. spinigera, Haem. intermedia, Hyalomma anatolicum anatolicum, Hyal. marginatum isaaci, Hyal. hussaini, Hyal. detritum, Hyal. kumari, Boophilus microplus, Ixodes acutitarsus, I. ovatus, Nosomma monstrosum, Rhipicephalus haemaphysaloides, and R. turanicus have been considered the most widely distributed tick species infesting cattle, buffalo, sheep, and goats (Ghosh et al., 2006). Hyal. anatolicum anatolicum, Hyal. marginatum isaaci, B. microplus, and R. haemaphysaloides are reported from almost all the states of India (Fig. 2) infesting livestock population (Ghosh et al., 2006). Reports of I. acutitarsus and I. ovatus are mostly available from the eastern and northeastern zones of India. Of the three predominant Haemaphysalis species, Haem. bispinosa is prevalent throughout India except Uttar Pradesh, while Haem. spinigera is restricted to southern states, central zones, Orissa of the eastern zone, and Meghalaya of the northeastern zone (Ghosh et al., 2007a,b). They are responsible for transmitting theileriosis, babesiosis, anaplasmosis, and ehrlichiosis, predominant health and management hazards of livestock of India (Table 1) as well as farming communities of Asia, Africa, and Latin America (Jongejan and Uilenberg, 2004; De la Fuente and Kocan, 2006). Boophilus microplus, a one-host tick (Soulsby, 1982), presently known as Rhipicephalus (Boophilus) microplus (CFSPH, 2007) is the most prevalent cattle tick in various agroclimatic zones of India infesting all age groups of cattle, horse, sheep, goat, deer (Ghosh et al., 2007a,b), and even camel (Singh and Chhabra, 1999), mithun (Rajkhowa et al., 2005), yak (Mondal, 2006), and wild herbivores (Singh et al., 1978). A high prevalence of B. microplus is reported from Tamilnadu (Kaushal et al., 2002), Chattishgarh (Das and Shrivastava, 2002), Haryana (Sangwan et al., 2000; Singh and Chhabra, 1999), the Vidarbha region of Maharashtra (MH) (Maske et al., 1998), the Marathwada region of Maharashtra (Shastri et al., 1983), and the Bombay region of Maharashtra (Raote, 1983). It has also been reported from the Central Himalayan region (Bhattacharya et al., 1996), from Assam (Deka et al., 1995; Lahkar et al., 1994), Tripura (Das, 1993), Terai of UP, Pantnagar (Das, 1994), Deharadun (Kumar et al., 1994), West Bengal (Basu et al., 1989), the Dharwad region of Karnataka (Kamble and Hiregoudar, 1988), Jammu and Kashmir (Kaul et al., 1990), Bhubaneshwar (Pratap et al., 1991), Chotanagpur and Santhal Parganas of Bihar (Kumar et al., 1989), Andaman (Khan, 1986), Tirunelveli (Sundaram et al., 1986), North Karnataka (Hiregoudar and Hirlapur, 1988), Kallar and Buliar areas of Nilgiri hills (TN) (Saxena and Rahman, 1985), Andhra Pradesh (Sivasankar and Rao, 1984), Bangalore (Jagannath et al., 1979), northeastern India (Miranpuri and Jasmer, 1978), Punjab (Gill and Gill, 1977), Delhi (Raizada and Nagar, 1979), Kashmir (Sharma and Sharma, 1976) etc.

Tick species in India and their distribution Indian farming mostly depends on income from agriculture by keeping animals for milk, meat, wool, and hide production and also for various farm operations. India accounts for a significant share of world’s livestock resources with nearly 57% of world’s buffaloes, 16.5% of cattle, 16.3% of goats, and 5.7% of sheep (FAO, 2004). The livestock sector accounted for 26.84% of agricultural gross domestic product (GDP) and about 5.21% of total GDP in 2008–2009. The share of livestock in the gross value of agricultural outputs has

Common tick control strategy Tick control is practiced in a variety of ways involving different livestock systems. Treatment of hosts with acaricides to kill attached larvae, nymphs, and adults has been the most widely used control method. In the first half of the past century, the main chemical acaricide was arsenic trioxide and subsequently organochlorines, organophosphates, carbamates,

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HIDE QUALITY

TICKS

TRANSMISSION OF DISEASES

DISRUPTION OF METABOLISM FOOD

GROWTH

ENERGY + INTAKE+CONVERSION

PROTEIN

SURVIVAL HIDE WEIGHT MEAT REPRODUCTION

LACTATION

CONCEPTION

CALVING WEANING MILK YIELD

Fig. 1. Multiple effects of tick feeding and tick-borne diseases (TTBDs) on animal production.

Fig. 2. Distribution of predominant ixodid tick species of ruminants in India.

amidines, pyrethroids, ivermectins etc. in different parts of the world. The introduction of new chemical compounds has been necessary because of the development of resistance in tick populations. Initially, the main uses of acaricides were aimed at eradication along with prevention and control of TTBDs. The eradication programs using acaricides were not successful in the ecologically more favorable tropical areas like Asia. In the areas where eradication was

not achieved, the costs for maintaining intensive tick control programs have become prohibitive. Control of TTBDs is mainly focused on tick control which is difficult because ticks have many natural hosts. Tick control or even eradication is not realistic in a country like India because in general, the farmers have small holdings, and conventional methods of tick control using chemical acaricides are popular only among progressive dairy farmers with large herds

Table 1 Tick-associated diseases in India. Disease

Pathogen or causative agent

Tick vector

References

Tropical theileriosis Bovine theileriosis Babesiosis Anaplasmosis Ehrlichiosis

Theileria annulata T. buffeli, T. lestoquardi Babesia bigemina, B. bovis Anaplasma marginale Ehrlichia bovis, E. phagocytophilum

Hyal. anatolicum anatolicum Hyal. anatolicum anatolicum B. microplus Rhipicephalus spp., Hyalomma spp., and Boophilus spp. Rhipicephalus spp.

Gautam (1974); Jongejan and Uilenberg (2004) Ghosh et al. (2006) Prasad (1989) Garg et al. (2004) Sreekumar et al. (2000)

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and even with irregular application. Many farmers are reluctant to change the generic chemical compounds which ultimately create resistance against that specific chemical. Grooming There are other common tick control strategies in practice. Grooming, the manual removal of ticks, is widely used in the developing world, although it is rare in extensive systems (Masika et al., 1997). Cattle enjoy manual removal of ticks. When removing ticks manually, consideration should be given to the possible hazard to humans from pathogens present in these ticks and the most important and deadly human pathogen that has been recognized is Crimean–Congo hemorrhagic fever (CCHF) virus, usually associated with ticks of the genus Hyalomma. Several outbreaks of this disease have been reported from Pakistan (Athar et al., 2005). Pasture management Environmental management systems like burning pasture to control ticks varies considerably among locations, tick species, local geography, pasture, and soil types and are widely practiced in South Africa, North America, and Australia. Burning pasture is a named component of the integrated tick management program (Cordoves et al., 1986). Elimination or exclusion of wildlife hosts of particular tick species has also been recommended to control ticks. Young et al. (1988) reduced tick and tick-borne disease burdens by separating buffalo from cattle in Kenya, and the same principle has been used for I. scapularis and white-tailed deer (Odocoileus virginianus) (Stafford et al., 2003). Clearing of scrub that provides a suitable environment for small native mammals is widely considered by veterinarians to be helpful for reducing ticks. Pasture spelling (depopulating pastures while free-living ticks die because of a shortage of available hosts) is well known as a means to control ticks (Johnston et al., 1968). Biological control Biological control refers to situations where humans attempt to use naturally occurring species of living organisms as antagonists to reduce pest populations (Gronvold et al., 1996). Hence, augmenting populations of existing antagonists (predators, parasites, parasitoids, and pathogens) or importing exotic antagonists are included in this definition. Practically, biological control is intended to reduce the density of a pest population to an equilibrium level low enough to avoid appreciable economic or clinical effects (Gronvold et al., 1996). A successful agent of biological control would be expected to be highly specific to the target organism, with no detrimental effects on antagonist or benign species. For ticks of livestock, candidate methods include ants (Chagas et al., 2002), predatory mites (Holm and Wallace, 1989), chickens (Kohn and Norval, 1994; Dreyer et al., 1997), parasitoid wasps (Hu et al., 1998), Bacillus thuringiensis (Zhioua et al., 1999), entomopathogenic nematodes (Samish and Glazer, 2001), and oxpeckers, Buphagus africanus (Mooring and Mundy, 1996). There are many natural predators of ticks, primarily attacking them in the free-living phase like birds, arthropods, parasitoids, infertile hybrids etc. Biopesticides Biopesticides have been used in various ways. Copping and Menn (2000) reported microbial agents and their secondary metabolites (including antibiotics), entomopathogenic nematodes, plant-derived pesticides (botanicals), arthropod pheromones, genetic modification for resistance among biopesticides and entomopathogenic fungi. Ticks have numerous natural enemies, but

only a few species of entomopathogenic fungi have been evaluated as tick control agents. Some laboratory results suggest that several bacteria are pathogenic to ticks, but their mode of action and their potential value as tick control agents remain to be determined. Entomopathogenic nematodes that are pathogenic to ticks can potentially control ticks, but improved formulations and selection of novel nematode strains are needed (Samish et al., 2004). Fungi are capable of infecting a wide range of living organism including insects and ticks. Spore suspension of mold Aspergillus terreus at different concentrations decreases the egg conversion factor by arresting oviposition of Hyal. anatolicum anatolicum and may play a substantial role in tick control programs (Suliman and Mahammed, in press). Spraying of aqueous and oil-based entomogenous fungal formulation (109 conidia/ml) depicted an 80–90% and a 40–50% mortality in adult ticks (R. appendiculatus and Amblyomma variegatum), respectively (Kaaya and Hassan, 2000). Research on a biopesticide derived from a strain of naturally occurring soil fungus Metarhizium anisopliae has confirmed the effectiveness with 100% tick mortality of the most common variety of tick within two days in laboratory condition (Leemon and Jonsson, 2008). Current control strategies for ticks rely heavily on extensive chemical treatments (acaricides) which are inundated with the problems of tick resistance and residues in meat and milk. Fungal biopesticides have emerged as realistic non-chemical control options for a range of pests in agriculture. Therefore one option for tick control is the use of a fungal biopesticides (Leemon, 2011). Two formulations using a mixture of spores of M. anisopliae isolates ARI-M52 and ARI-M63 in two different dose levels provided reasonable tick control on animals which were kept below 34 ◦ C for significant time periods each day (Leemon et al., 2008). One of the advantages of fungal biopesticides over other biological control agents is the ease with which they can be cultured on simple artificial media like rice or other cereals with minimal specialized equipment. Other advantages are that fungal biopesticides can be applied to the target using more or less conventional acaricide fluid application systems such as hand sprays or spray races, and the fungal conidia that are applied to the target can be mixed with water or oil or water and oil mixtures. To date, little is known of the pathogenesis of fungal biopesticides for ticks of livestock, and the selection of strains for bioassays has been largely on the basis of trial and error. Biopesticides will likely play a substantial role in future tick control programs because of the diversity of ticks. Considerable research is required to select appropriate strains, to develop them as biopesticides, to establish their effectiveness, and to devise production strategies to bring them in practical use. Genetic manipulation Development of ‘cattle lines’ or a breed with enhanced, genetically based disease resistance is an especially attractive prospect (De Castro and Newson, 1993). Good examples of exploiting genetic resistance to livestock diseases in general and parasites in particular, have been described for resistance of B. indicus to cattle ticks. Advances in molecular genetics should offer opportunities for identifying markers for parasite resistance. It is known that in many subtropical and semi-arid environments, indigenous dual-purpose breeds are highly resistant to ticks, resulting in low infestation rates that cause insignificant direct losses. Massive losses caused by TTBDs occur in susceptible breeds of cattle if unprotected. Moreover, local indigenous cattle kept completely tick-free become equally susceptible. The phenomena of host resistance to ticks and enzootic stability to tick-borne diseases are well documented (Latif and Pegram, 1992). In cattle, resistance levels may vary greatly between breeds and between animals. Host resistance is stable, heritable, long lasting, and the most important factor affecting the economics of tick control. It is a low-cost

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permanent solution requiring no extra resources nor incurring any additional costs. High host resistance is advantageous in any tick control program. However, its improvement has been almost entirely neglected in Asia (Frisch, 1999) including India. In India, cattle breeds of Ongole/Nellore, Sahiwal, Ponwar hill cattle, and buffaloes are recorded in the literature as resistant to tick infestation (Gaur et al., 2002). Most of the times, the tick resistance status of these animals was attributed to the physical characters and behavior of these animals. The genetic or molecular basis of host resistance to ticks and tick-borne diseases is unknown. Vaccination Vaccination has been incorporated into integrated control programs for ticks in two ways. Firstly, for many years, vaccines of variable efficacy against tick-borne diseases have been used, often resulting in a reduced need for using acaricides. Secondly, in more recent years, vaccines against tick gut glycoprotein have become commercially available, directly reducing the need for using acaricides. Vaccines so far commercially available were developed to be effective against B. microplus and are based on the tick midgut protein Bm86. However, current research suggests that the target might be conserved in a number of tick species, resulting in some successes against B. annulatus (Pipano et al., 2003), Hyal. anatolicum anatolicum, and Hyal. dromedarii (De Vos et al., 2001). A commercial product based on the Bm86 antigen is TickGARDPLUS. Bm86 is a concealed antigen, and repeated inoculations are required to provide continuing immunity because the presence of feeding ticks does not boost the immune response of cattle. Efficacy studies with the vaccine developed from Bm86 account for the fact that the vaccine has an effect on the number of females engorging, the number of eggs they produce, the viability of the eggs, and the larvae that hatch from them and thus resulting in an overall effect of 90% on the reproductive performance of the tick (Willadsen et al., 1995). Other potential vaccine candidates for B. microplus are Bm91 (Riding et al., 1994), b-N-acetylhexosaminidase (del Pino et al., 1998), vitellin (Tellam et al., 2002), trypsin inhibitors (Andreotti et al., 2002), and SBm7462 (Patarroyo et al., 2002). A serine proteinase inhibitor (serpin) from Haem. longicornis has also been investigated as a potential vaccine candidate (Sugino et al., 2003). Serpins of R. appendiculatus have been identified, cloned and characterized, but their protective effects have not been tested yet (Mulenga et al., 2003). Trimnell et al. (2002) reported that cloned putative cement proteins from R. appendiculatus were able to achieve 48% mortality of nymphs feeding on vaccinated guinea pigs. Progress on the development of vaccines against ticks in India can be divided into two broad categories: work done on laboratory animals as well as on natural hosts using crude and partially purified antigens and the experimentation using purified antigens followed by testing as vaccine candidates. Immunization of animals against targeted tick species using crude and partially purified antigens had been initiated in India in the early 1990s to develop immune-prophylactic measure that would be more effective against local tick strains (Manohar and Banerjee, 1992a,b; Thakur et al., 1992). But the results obtained in preliminary studies have not been confirmed in natural hosts. A group of scientists from Haryana Agriculture University, Hissar (India), reported crossprotective efficacy of midgut extracts of Hyal. dromedarii following immunization of rabbits (Kumar and Kumar, 1995, 1996). However, the challenge dose (n = 10 pairs of ticks) used for the crossprotection study was not sufficient to establish the cross-protective potentiality of the antigen tested. Common cross-reactive proteins of 66 kDa were detected in the salivary gland extracts of Hyal. anatolicum anatolicum and in B. microplus (Parmar and Grewal, 1996; Parmar et al., 1996). Similarly, Ghosh and Khan (1998) reported six immunodominant proteins of 97.4, 85, 66, 47.3, 42, and 31 kDa in all

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the stages of Hyal. anatolicum anatolicum. Subsequently, Ghosh and Khan (2000) reported common proteins of 68, 57.5, 50.8, 47.3, 43, and <43 kDa in all the stages of B. microplus and Hyal. anatolicum anatolicum. In comparison to the work done on three-host ticks, experiments conducted for immunization of cattle against the onehost tick, B. microplus, are very limited. Crude extracts of partially fed adults and unfed larvae of B. microplus for the immunization of cross-bred calves and proteins of 105.4 and 92.2 kDa were recognized as immunodominant proteins present in adults and in larvae of the tick species (Ghosh and Khan, 1996, 1997a,b,c). However, further work for exploitation of the identified antigens is required. By purification of antigens and their testing as vaccine candidates, crude larval and nymphal extracts of Hyal. anatolicum anatolicum were used for the immunization of New Zealand white rabbits (Ghosh and Khan, 1998). In another study, Ghosh and Khan (1999) depicted that unfed larvae of Hyal. anatolicum anatolicum provide a relatively easily available source of antigen for immunization of cattle against both larvae and nymphs of this tick species. In their experiment, crude extracts of Hyal. anatolicum anatolicum anti-larval immunoglobulin ligands purified at the level of 93.3%, a protein of 39 kDa was isolated which was found effective in conferring protection by reducing 71.6% of larval and 77.3% of nymphal infestations (Ghosh et al., 1999). In continuation, the nymphal antigens were purified by immunoaffinity chromatographic technique, and a protein of the same molecular weight was isolated and tested against experimental challenge infestations and found protective (Sharma et al., 2001). Later, the antigen has been included in the list of identified tick vaccine candidates (Willadsen, 2004). As a concealed antigen approach, larval gut antigens’ screening depicted three proteins of 100, 59.4 and 37 kDa which conferred protection by reducing larval, nymphal, and adult infestations by 70.6%, 54.5%, and 61.9%, respectively (Das et al., 2000). Using chromatographic affinity testing, a protein of 68 kDa was identified from adult extracts of Hyal. anatolicum anatolicum which conferred protection against tick challenge (Das et al., 2003). Further, Singh and Ghosh (2003) specifically isolated two glycol proteins of 34 and 29 kDa from the larvae of Hyal. anatolicum anatolicum and B. microplus, respectively, conferring protection against both tick species for up to 30 weeks (Ghosh et al., 2005). As an important component of vaccine formulation, the comparative immunopotentiating properties of incomplete Freund’s adjuvant (IFA) and saponin in combination with the 39 kDa larval antigen of Hyal. anatolicum anatolicum achieved a better effect with IFA than saponin during immunization of cross-bred cattle against infestation of Hyal. anatolicum anatolicum (Ghosh et al., 2002). Work on crossprotection and cloning of the desired antigen may evolve effective immune protection against Hyal. anatolicum anatolicum infestation in India. Chemical acaricides Periodic application of acaricides (agents used to kill ticks and mites) is the most widely used method to control ticks and may be directed against the free-living stages of ticks in the environment or against the parasitic stages on the host. At present, tick control is based on large-scale repeated use of synthetic acaricides, viz. cypermethrin, deltamethrin, fenvelerate, diazinon, amitraz, flumethrin, and ivermectin, a macrocyclic lactone. Acaricides used to control ticks on livestock or in the environment should be applied in such a manner that the ticks will be killed. The treatments do not harm livestock or applicators, treated animals do not contain high residues, and the environment is not adversely affected. The most widely used method for the control of ticks is the direct application of acaricides to host animals. Acaricides can be applied by dipping, washing, spraying, pour-on, spot-on, or by injections. Insecticide ear tags are commercially available in

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some countries for the control of ear ticks. Dipping is an expensive operation, but it is desirable when a large number of animals are to be treated or a tick eradication program is in place. Frequency of dipping depends upon the involved tick species. The strategic (or most effective) use of acaricides for the control of ticks will depend upon a number of factors including the kind of life cycle of the tick species to be controlled, its seasonal activity, and the urgency of the need in terms of disease transmission. Certainly, a given acaricide must be directed against the susceptible stage(s) of the tick. In the case of B. microplus, dipping regularly on every 21st day is recommended to break the life cycle because 18 days is the least time from the dropping off of an engorged female to the time when the resultant larvae can be ready for infestation, and the dip gives protection for three days (Hungerford, 1990). The construction of a dipping tank varies according to the kind and number of animals required to be dipped. In tropical and subtropical countries, it is preferable to cover the tank with a roof to avoid excessive concentration of insecticides by evaporation or dilution by rain. Commonly used acaricides and their efficacy in India have been summarized (Table 2). Besides various indirect effects of synthetic acaricides on the environment generally due to their large-scale use, there is an emerging problem of development of resistance in ticks to these acaricides. Resistance of ticks to synthetic acaricides has already been reported worldwide (FAO, 1984; WHO, 1992). It results from repeated exposure of tick populations to chemical acaricides and ongoing survival and reproduction of ticks that are less affected by the acaricides. However, no studies are available on the probable development of resistance to herbal acaricides if any for which research about the molecular basis of action of herbal acaricides might be helpful. Herbal approach As per the report published by FAO (2004), the tick population in India has developed resistance against all the commonly available acaricides, and there have been only limited research activities to develop newer classes of acaricides due to the enormous costs involved. The synthetic acaricides are being used in concentrations many times higher than the prescribed doses. This contributes to the increased consumption of insecticides in Indian agriculture. The control of tick populations in the absence of effective acaricides will be difficult if not impossible in the future. Little attention has been paid to explore the huge potential of medicinal plants available in India with acaricidal property. Presently, there is increasing concern about the use of chemicals in all forms of agriculture as well as in livestock management by their potential environmental hazard and presence in food products. Exploration of the possibilities to use botanical acaricides for the control of TTBDs has been identified as one of the future options. About 80% of the worldwide populations are dependent on medicinal plants for their primary health care (Farnsworth et al., 1985). India is one of the world’s 12 regions having the largest biodiversity and possesses 15,000–20,000 plant species with proven medicinal value (Kumar, 1996). In the World Trade Organization (WTO) regime, when countries are competing in the patent rights, it is high time to take immediate measures and programs to save these natural assets before they are lost forever. The use of herbal preparations among the rural folks specifically in India is gaining importance because of their therapeutic value, their local availability, and cost effectiveness. The latest trend in utilization of herbal preparations along with modern biochemicals have added advantage of providing effective therapy and in some cases may reduce the dose of allopathic/chemical drug in combination therapy. Considering the facts, there is an urgent need to find out cost-effective therapeutic regimes with medicinal plants alone or in combination with some

chemical acaricides for a synergetic action against tick infestation on livestock or for reducing future tick populations. The ethno-veterinary and medicinal plant knowledge offers a range of plant materials to be evaluated for their acaricidal properties. Plant materials are known to possess insecticidal, growth inhibiting, anti-molting, and repellent activities. A number of reports is available on the effect of different plant materials on tick species such as Jatropha curcas (Adebowale and Adedire, 2006), Annona squamosa (Khalequzzaman and Sultana, 2006), Polyalthia longifolia, Ageratum conyzoides, Tagetes errecta, Tagetes minuta, Cymbopogan spp., Mentha piperita, Ocimum sanctum, Dalbergia sisoo Roxb., Azadirachta indica, Eucalyptus maculate, Citrus spp., Ferronia elephantum, Solanum nigrum Linn., Lantana camara (ICMR, 2003). Different plant materials were also been tested earlier by many workers (Narang et al., 1988; Kalakumar et al., 2000; Handule et al., 2002; Chagas et al., 2008; Choudhury et al., 2004) to find out their acaricidal effects. But in all the events, the data were generated following application of the plant materials on the naturally infested animals. No such control study with a distinct number of ticks of a given species in a specific life stage and with a defined concentration of specific plant extracts has been tried earlier. Extracts of some plants are also effective against certain tick species (Maske et al., 1996; Banerjee, 1997; Vatsya and Singh, 1997; Shrivastava and Sinha, 1990; Hazzari and Misra, 1989). The feasibility of these plant extracts for tick control under field conditions has not been adequately studied, yet. Khudrathulla and Jagannath (2000) studied the effect of a methanolic extract of Styloxanthes scabra on ixodid ticks. The leaves of tobacco (N. tabacum) were found effective against R. haemaphysaloides (Choudhury et al., 2004). Methanolic extracts of neem (Azadirachta indica) leaves and bark were tested for the acaricidal effects (Pathak et al., 2004). Essential oil of Azadirachta indica and Ocimum suave has shown acaricidal and repellent properties against the larvae of Amblyomma variegatum and all stages of Hyal. anatolicum excavatum and R. appendiculatus (Ndumu et al., 1999; Kaaya and Hassan, 2000). An acaricidal activity of the essential oil of Melaleuca alterifolia Cheel (tea tree oil) against nymphs of Ixodes ricinus was demonstrated (Iori et al., 2005). Attempts have also been made to isolate the active fraction(s) or active component(s) of those plant materials containing the acaricidal property, but the efficacy of the fractions was solely evaluated through in vitro study (Narang et al., 1988). In a comprehensive bioassay trial, Chungsamarnyart et al. (1988) tested the ethanolic extracts of 44 plant species for their larvicidal activity, but they did not test the acaricidal properties of those plant extracts against adult ticks, the most resistant stage. Despite a plethora of reports on the acaricidal activity of plant extracts, some of the plant products have been reported to possess excellent therapeutic potential as concluded through moderately scientific testing protocols on traditional medicine of the individual researchers including questionnaires to practitioners, poorly designed field trails, and very limited laboratory tests. Testing of promising plant materials by laboratory trials through identification, isolation, and purification of the active ingredients and finding efficacy against a defined stage of a given tick species in a controlled study (with tick barrier) will definitely be helpful. The development of field-tested, cost-effective, and easily available quality herbal acaricides to control ticks and to prevent the spread of TTBDs without any significant adverse effects on the environment has become the basic need of the hour. In the recent past, work has been initiated in India on a similar line with properly designed scientific protocols by a group of workers (Srivastava et al., 2008; Magadum et al., 2009; Ghosh et al., 2010; Mondal, 2012) with identified plant extracts and their combinations having strong acaricidal activities to substitute synthetic acaricides. Emphasis has been given on the importance of detailed study

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Table 2 Commonly used acaricides and their efficacy in India. Acaricide class

Compounds

Application

Common tick species

Efficacy (%)

References

Pyrethroids

Cypermethrin Cyperkill Deltamethrin

B. microplus Hyal. anatolicum anatolicum B. microplus

100 96–100 96–100

Khan (1996) Pathan et al. (2003) Gupta et al. (1998)

Flumethrin Permethrin

Dip Dip Spray Dip Pour-on Dip

B. microplus Hyal. anatolicum anatolicum

90–100 90–100

Kumar et al. (2001) Kumar et al. (2001)

Organophosphates

Fenvalerate Hexafen Coumaphos

Dip Sponging Sponging

B. microplus Haem. bispinosa Hyal. dromedarii

90–100 90 95–100

Khan (1996) Khan (1996) Talukdar et al. (1998)

Carbamates

Diazinon Carbaryl

Dip Spray

Haem. bispinosa B. microplus

97–100 100

Shahardar et al. (2002) Basu and Haldar (1997)

Macrocyclic lactones

Ivermectin

Injection

B. microplus, R. haemaphysaloides

100

Maske et al. (1992)

to evaluate the efficacy of acaricides of plant origin both in vitro as well as in vivo along with the characterization of the active chemical components to identify the active fractions of those plant materials responsible for acaricidal efficacy. They also revealed the ability of some identified plant components to affect the reproductive performance of ticks and to reduce tick populations even in the next progeny by reducing hatchability or molting success.

Integrated control strategy In the current system of livestock production in developing countries like India, tick control cannot be imagined without the use of chemical acaricides despite the increasing resistance of tick populations, environmental contamination, and even contamination of milk and meat products with drug residues (Graf et al., 2004). Chemical acaricides are widely used among medium- and largescale farmers in India (Beniwal et al., 1997). Resistance to existing acaricides of many chemical classes is widespread and increasing (Willadsen, 2004). Resistance against all classes of acaricides from different parts of world (FAO, 1984; WHO, 1992) has been reported. The high speed with which this has occurred after the release of each new class of chemicals is clearly a deterrent to companies which develop such compounds for parasite control. Resistance results from exposure of tick populations to acaricides, and the ongoing survival and reproduction of ticks that are less affected by a given acaricide. Monitoring and early detection of acaricide resistance is one of the essential components for successful integrated pest management (IPM). Such acaricide resistance screening tests should be available for all acaricides which are being used in the field. The problem of increasingly resistant strains of ticks and health hazards due to tick resistance invites a serious think over a sustainable alternative approach for controlling TTBDs in eco-friendly manner. Development of new acaricides is a long and expensive process which reinforces the need for alternative approaches of tick control (Graf et al., 2004). It has been estimated that on an average the development costs of a new insecticide is about 230 million US $ (De la Fuente et al., 1995). Moreover, the multinational companies are not interested in funding insecticide research since the targeted arthropods are developing resistance faster than the economic return of the input. In this situation, the global livestock production community may not be in a position to have soon a new-generation insecticide to control ticks. For this reason, newer methodologies like combinational chemistry and computational biology along with high throughput screening against a target would yield new-generation acaricides. New-generation acaricides targeting previously not-explored metabolic pathways or biomolecules’ synthesis pathways should be generated, and these acaricides should be kept in reserve for any emergency situations

expected to arrive by multi-acaricide-resistant tick populations in the future. In the post WTO scenario, it is essential to have livestock products free of any harmful elements, and therefore research efforts have been directed toward the development of alternative strategies for controlling tick infestations (Graf et al., 2004). It has been postulated globally that IPM or integrated tick management (ITM) is the only suitable option for a sustainable control of TTBDs. However, IPM/ITM emphasizes the use of series of complementary control measures following the consideration of economic factors, epidemiology, resistance status, and the production and management structure in place without relying much on any single measures (Nari, 1995). This includes the use of chemical acaricides, vaccines, pasture spelling, resistance animal development, biological control, and herbal remedies (ethno veterinary practices) to control TTBDs in a geographical area. As a component of ITM, the use of eco-friendly, cost-effective botanical acaricides along with other available methods can be an appropriate sustainable method in a strategic integrated manner. Besides the environment-friendly nature of herbal acaricides, the speed of development of resistance can be slowed down since herbs having insecticidal property will contain more than one active acaricide component, so single-point mutations in ticks will not be sufficient to render a herbal insecticide/acaricide ineffective. On the contrary, it is a common phenomenon when using chemical acaricides that due to a single-point mutation in the targeted molecule most of the pesticide becomes ineffective (WHO, 1992; Benavides et al., 2000). Therefore, it is imperative to identify plant components with acaricidal properties and to use the easily adoptable tick control components singly or in combination with other available approaches in a strategic way to reduce tick populations and to combat TTBDs in livestock.

Conclusions TTBDs rank high in terms of their impact on the livelihood of resource-poor farming communities like India. Decreased outputs of animal products, by-products, manure etc. contribute to production and productivity losses. Control of ticks so far mainly rests on the continuous use of acaricides both on and off host. Longterm use of these chemicals leads to the development of resistance, residual effects on livestock products and the environment. Newer classes of acaricides have tended to be significantly more expensive. Due to high costs involved in treating tick infestations, most of the small and marginal farmers are utilizing indigenous method to get rid of tick infestations. Structural changes in the provision of veterinary services, economic and social changes in livestock production systems, increased costs of acaricides combined with the increasing incidence of acaricide resistance in ticks have led

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to a demand for more cost-effective and sustainable approaches to control TTBDs. The use of herbal preparations among the rural folks is gaining importance because of their therapeutic value, local availability, and cost effectiveness. The speed of development of resistance against herbal acaricides may be slower as herbs contain more than one effective compound in contrast to chemical acaricides. So single-point mutations of ticks will not be sufficient to render a given herbal acaricide ineffective. Finding new classes of cost-effective, eco-friendly acaricides and their strategic use can be a magic wand and may be a boon for Indian farmers. References Adebowale, K.O., Adedire, C.O., 2006. Chemical composition and insecticidal properties of the underutilized Jatropha curcas seed oil. Afr. J. Biotechnol. 5, 901–906. Andreotti, R., Gomes, A., Malavazi-Piza, K.C., Sasaki, S.D., Sampaio, C.A.M., Tanaka, A.S., 2002. BmTI antigens induce a bovine protective immune response against Boophilus microplus tick. Int. Immunopharmacol. 2, 557–563. Anonymous, 2002. Leather goods sector poised to take on new challenges. Leatherware 16 (10), 10–12. Athar, M.N., Khalid, M.A., Ahmad, A.M., Bashir, N., Baqai, H.Z., Ahmad, M., Balouch, A.H., Bashir, K., 2005. Crimean–Congo hemorrhagic fever outbreak in Rawalpindi, Pakistan, February 2002: contact tracing and risk assessment. Am. J. Trop. Med. Hyg. 72, 471–473. Banerjee, P.S., 1997. Efficacy of herbal ectoparasiticide AV/EPP/14 on some ectoparasites of dogs and cattle. J. Vet. Parasitol. 11, 215–217. Basu, A.K., De, S.K., Sanyal, A.K., 1989. Incidence of ticks (Acari: Ixodidae) associated with cattle and buffalo in West Bengal. Environ. Ecol. 7, 784–786. Basu, A.K., Haldar, D.P., 1997. A note on the effect of continuous use of sevin 50WP on some cattle ticks. Vet. Parasitol. 11, 183–184. Benavides, E., Rodriguez, J.L., Romero, A., 2000. Isolation and partial characterization of the Montecitos strain of Boophilus microplus (Canestrini, 1877) multi-resistant to different acaricides. Ann. N.Y. Acad. Sci. 916, 668–671. Beniwal, R.K., Nichani, A.K., Sharma, R.D., Radka, N.K., Suri, D., Sarup, S., 1997. Responses in animals vaccinated with the T. annulata (Hisar) cell culture vaccine. Trop. Anim. Health Prod. 29, 1095–1138. Bhattacharya, D., Mahesh, C., Laha, R., 1996. Parasites of livestock in central Himalayan region. Indian J. Vet. Res. 5, 51–53. Biswas, S., 2003. Role of veterinarians in the care and management during harvest of skin in livestock species. In: Proc. National Seminar on Leather Industry in Today’s Perspective, Kolkata, India, pp. 62–64. Central Statistics Office (CSO), 2010. Ministry of Statistics and Programme, India. Centre for Food Security and Public Health (CFSPH), 2007. Rhipicephalus (Boophilus) Microplus: Southern Cattle Tick, Cattle Tick. Iowa State University, Iowa, pp. 1–3. Chagas, A.C.S., Furlong, J., Nascimento, C.B., 2002. Predation of Boophilus microplus (Canestrini 1887) (Acari: Ixodidae) tick engorged female by the ant Pachycondyla striata in pastures. Biosci. J. 18, 77–81. Chagas, A.C.S., Vieira, L.S., Freitas, A.R., Araújo, M.R.A., Araújo-Filho, J.A., Araguao, W.R., Navarro, A.M.C., 2008. Anthelmintic efficacy of neem (Azadirachta indica A. Juss) and the homeopathic product Fator Vermes® in Morada Nova sheep. Vet. Parasitol. 151, 68–73. Choudhury, R.T., Vasanthi, C., Latha, B.R., John, L., 2004. In vitro effect of Nicotina tabacum aqueous extract on Rhipicephalus haemaphysaloides ticks. Indian J. Anim. Sci. 74, 730–731. Chungsamarnyart, N.S., Jiwajinda, W., Jansawan, U., Buranasilpin, K.P., 1988. Effective plant crude-extracts on the ticks (Boophilus microplus). Larvicidal action. Kasetsart J. Nat. Sci. Suppl. 22, 37–41. Copping, L.G., Menn, J.J., 2000. Biopesticides: a review of their action, applications and efficacy. Pest Manage. Sci. 56, 651–676. Cordoves, C.O., de la Cruz, J., Tamayo, J., Mesejo, J., Fleites, R., 1986. Experience and perspectives of tick control and eradication in the Republic of Cuba. Rev. Cub. Cienc. Vet. 7, 1–13. Das, G., Ghosh, S., Khan, M.H., Sharma, J.K., 2000. Immunization of crossbred cattle against Hyalomma anatolicum anatolicum by purified antigens. Exp. Appl. Acarol. 24, 645–659. Das, G., Ghosh, S., Sharma, J.K., Khan, M.H., Gupta, S.C., 2003. Attempted immunization of crossbred (Bos indicus and Bos taurus) calves by affinity purified concealed antigens of Hyalomma anatolicum anatolicum. Indian J. Anim. Sci. 73, 713–717. Das, K., Shrivastava, S.K., 2002. Bovine tick, Boophilus microplus Canestrini, infestation in rural Chattisgarh. J. Appl. Zool. Res. 13, 247–248. Das, S.S., 1993. Prevalence of hemoprotozoan infections in domestic animals in Tripura (India). J. Parasitol. Appl. Anim. Biol. 2, 53–56. Das, S.S., 1994. Prevalence of ixodid tick infestation on farm animals in Pantnagar, Terai of Uttar Pradesh. J. Parasitol. Appl. Anim. Biol. 3, 71–73. De Castro, J.J., 1997. Sustainable tick and tickborne disease control in livestock improvement in developing countries. Vet. Parasitol. 71, 77–97. De Castro, J.J., Newson, R.M., 1993. Host resistance in cattle tick control. Parasitol. Today 9, 13–17. De la Fuente, J., Kocan, K.M., 2006. Strategies for development of vaccines for control of ixodid tick species. Parasite Immunol. 28, 275–283. De la Fuente, J., Rodriguez, M., Montero, C., Leonard, R., 1995. Control of Boophilus microplus infestations in cattle vaccinated with a recombinant BM 86 antigen

preparation. Evidences of control of chemical resistance strains and Babesia bovis transmission. In: Seminario, Internacional de parasitologia animals. Resistancia y control en garrapatas y moscas de imporatancia veterenaria, Acapulco, Mexico, pp. 101–111. De Vos, S., Zeinstra, L., Taoufik, O., Willadsen, P., Jongejan, F., 2001. Evidence for the utility from Boophilus microplus in vaccination against other tick species. Exp. Appl. Acarol. 25, 245–261. Deka, D.K., Choudhry, S., Chakraborty, A., 1995. Parasites of domestic animals and birds in Likhimpur (Assam). J. Vet. Parasitol. 9, 21–25. del Pino, F.A.B., Brandelli, A., Gonzáles, J.C., Henriques, J.A.P., Dewes, H., 1998. Effect of antibodies against ␤-N-acetylhexosaminidase on reproductive efficiency of the bovine tick Boophilus microplus. Vet. Parasitol. 79, 247–255. Donat, J.R., Donat, J.F., 1987. Tick paralysis with persistent weakness and electromyographic abnormalities. Arch. Neurol. 38, 59–61. Dreyer, K., Fourie, L.J., Kok, D.J., 1997. Predation of livestock ticks by chickens as a tick control method in a resource-poor urban environment. Onderstepoort J. Vet. Res. 64, 273–276. FAO, 1984. Ticks and Tick-borne Disease Control: A Practical Field Manual. Vol. I. Tick Control. Food and Agriculture Organization of the United Nations, Rome, 299 pp. FAO, 2004. Resistance Management and Integrated Parasite Control in Ruminants: Guidelines. Animal Production and Health Division, Food and Agriculture Organization of the United Nations, Rome, pp. 25–77. Farnsworth, N.R., Akerele, O., Bingel, A.S., Soejarta, D.D., Eno, Z., 1985. Medicinal plants in therapy. Bull. World Health Organ. 63, 965–981. Frisch, J.E., 1999. Towards a permanent solution for controlling cattle ticks. Int. J. Parasitol. 29, 57–71. Furman, D.P., Loomis, E.C., 1984. The Ticks of California (Acari: Ixodida). University of California Publications, Bulletin of the California Insect Survey, vol. 25. University of California Press, California, pp. 1–239. Garg, R., Banerjee, P.S., Yadav, C.L., Garg, A., 2004. Subclinical babesiosis and anaplasmosis in crossbred cattle in an organized farm. J. Vet. Parasitol. 18, 151–153. Gaur, G.K., Kaushik, S.N., Garg, R.C., 2002. Ongole cattle status in India. Anim. Genet. Resour. Inform. 32, 27–34. Gautam, O.P., 1974. Theileriosis in India. In: 3rd Int. Congress Parasite, Munich, West Germany. Geevarghese, G., Fernandes, S., Kulkarni, S.M., 1997. A checklist of Indian ticks (Acari: Ixodidae). Indian J. Anim. Sci. 67, 566–574. Ghosh, S., Azhahianambi, P., de la Fuente, J., 2006. Control of ticks of ruminants, with special emphasis on livestock farming system in India – present and future possibilities for integrated control: a review. Exp. Appl. Acarol. 40, 49–66. Ghosh, S., Azhahianambi, P., Yadav, M.P., 2007a. Upcoming and future strategies of tick control: a review. J. Vector Borne Dis. 44, 79–89. Ghosh, S., Bansal, G.C., Gupta, S.C., Ray, D., Khan, M.Q., Irshad, H., Shahiduzzaman, M.D., Seitzer, U., Ahmed, J.S., 2007b. Status of tick distribution in Bangladesh, India and Pakistan. Parasitol. Res. 101, 207–216. Ghosh, S., Khan, M.H., 1996. Studies on immunological control of ticks. II. Immunization of cattle against Boophilus microplus using tick extract supernatant antigen. J. Vet. Parasitol. 10, 33–37. Ghosh, S., Khan, M.H., 1997a. Cross-bred cattle protected against Boophilus microplus by immunization with antigens from adult and larval ticks. Indian J. Anim. Sci. 67, 183–186. Ghosh, S., Khan, M.H., 1997b. Immunological control of ticks: shared antigens in larval and adult stages of the tick, Boophilus microplus. J. Vet. Parasitol. 11, 149–154. Ghosh, S., Khan, M.H., 1997c. Identification of tick antigen immunogenic in calves. Int. J. Anim. Sci. 12, 248–253. Ghosh, S., Khan, M.H., 1998. Immunization of rabbits against Hyalomma anatolicum anatolicum using homogenate from unfed immature ticks. Indian J. Exp. Biol. 36, 167–170. Ghosh, S., Khan, M.H., 1999. Larval antigen protect cross bred cattle from immature stages of Hyalomma anatolicum anatolicum. Indian J. Exp. Biol. 37, 203–205. Ghosh, S., Khan, M.H., 2000. Isolation of immunoreactive proteins from the larval extracts of Boophilus microplus and Hyalomma anatolicum anatolicum. Indian J. Anim. Sci. 70, 14–18. Ghosh, S., Khan, M.H., Ahmed, N., 1999. Immunization of cattle against H. anatolicum anatolicum using antigen purified by immunoaffinity chromatography. Trop. Anim. Health Prod. 31, 263–273. Ghosh, S., Sharma, A.K., Kumar, S., Tiwari, S.S., Rastogi, S., Srivastava, S., Singh, M., Kumar, R., Paul, S., Ray, D.D., Rawat, A.K.S., 2010. In vitro and in vivo efficacy of Acorus calamus extract against Rhipicephalus (Boophilus) microplus. Parasitol. Res. 108, 361–370. Ghosh, S., Singh, N.K., Das, G., 2005. Assessment of duration of immunity in calves immunized by glycoproteins isolated from the larvae of Hyalomma anatolicum anatolicum and Boophilus microplus. Parasitol. Res. 95, 319–326. Ghosh, S., Singh, N.K., Rawat, P., 2002. Comparative immunopotentiating properties of saponin and incomplete Freund’s adjuvant coupled to affinity purified larval antigen of Hyalomma anatolicum anatolicum. Indian J. Exp. Biol. 40, 1026–1031. Gill, H.S., Gill, B.S., 1977. Ixodid ticks of domestic animals in the Punjab State. Annual Report of Punjab Agricultural University, Ludhiana, India, pp. 69. Graf, J.F., Gogolewski, R., Leach-Bing, N., Sabatini, G.A., Molento, M.B., Bordin, E.L., Arantes, G.J., 2004. Tick control: an industry point of view. Parasitology 129, 427–442. Gronvold, J., Henricksen, S.A., Larsen, M., Nansen, P., Wolstrup, J., 1996. Biological control. Aspects of biological control – with special reference to arthropods, protozoans and helminths of domestic animals. Vet. Parasitol. 64, 47–64.

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Gupta, S.K., Singh, S., Banerjee, D.P., Singh, S., 1998. Evaluation of flumethrin (Bayticol) pour-on against tick infestations on cross-bred cattle and buffaloes. Vet. Parasitol. 12, 79–81. Handule, I.M., Ketavan, C., Geb, S., 2002. Toxic effect of Ethiopian neem oil on larvae of cattle tick, Rhipicephalus pulchellus Gertaeker. Kasetsart J. Nat. Sci. 36, 18–22. Hazzari, M.M., Misra, S.C., 1989. Efficacy of newer acaricides against Boophilus microplus in experimentally infested calves. Indian Vet. J. 66, 1105–1107. Hiregoudar, L.S., Hirlapur, S., 1988. Ticks of cattle and buffaloes in north Karnataka. Indian Vet. J. 65, 18–22. Holm, E., Wallace, M.M.H., 1989. Distribution of some anystid mites (Acari: Anystidae) in Australia and Indonesia and their role as possible predators of the cattle tick Boophilus microplus (Acari: Ixodidae). Exp. Appl. Acarol. 6, 77–83. Hu, R.J., Hyland, K.E., Oliver, J.H., 1998. A review on the use of ixodiphagous wasps (Hymenoptera: Encyrtidae) as natural enemies for the control of ticks (Acari: Ixodidae). Syst. Appl. Acarol. 3, 19–27. Hungerford, T.G., 1990. Hungerford’s Diseases of Livestock, 9th ed. McGraw-Hill Book Co., Sydney, Australia. ICMR, 2003. Prospects of using herbal products in the control of mosquito vectors. ICMR Bull. 33, 1–12. Iori, A., Grazioli, D., Gentile, E., Marano, G., Salvatore, G., 2005. Acaricidal properties of the essential oil of Melaleuca alternifolia Cheel (tea tree oil) against nymphs of Ixodes ricinus. Vet. Parasitol. 129, 173–176. Jagannath, M.S., Muraleedharan, K., Hiregoudar, L.S., 1979. Prevalence of ixodid ticks of cattle at Bangalore. Indian J. Anim. Sci. 49, 890–894. Johnston, L.A.Y., Wharton, R.H., Calaby, J.H., 1968. Eradication of cattle tick (Boophilus microplus) from Magnetic Island, Queensland, in the presence of native fauna. Aust. Vet. J. 44, 403–405. Jongejan, F., Uilenberg, G., 2004. The global importance of ticks. Parasitology 129, 1–12. Kaaya, G.P., Hassan, S., 2000. Entomogenous fungi as promising biopesticides for tick control. Exp. Appl. Acarol. 24, 913–926. Kalakumar, B., Kumar, H.A.S., Kumar, B.A., Reddy, K.S., 2000. Evaluation of custard seed oil and neem oil as acaricides. J. Vet. Parasitol. 14, 171–172. Kamble, C.K., Hiregoudar, L.S., 1988. Prevalence of different species of ticks on domestic animals in Dharwad area of Karnataka. Mysore J. Agric. Sci. 22, 331–333. Kaul, H.N., Shetty, P.S., Ghalsasi, G.R., Dhanda, V., 1990. Survey of ticks (Acarina: Ixodidae) for Crimean haemorrhagic fever virus activity in Jammu & Kashmir State, India. Indian J. Med. Res. A Infect. Dis. 91, 5–8. Kaushal, K., Balakrishanan, N., Rakesh, K., Gill, K.S., 2002. Prevalence of ixodid ticks in Nilgiri district of Tamil Nadu State (India). Indian Vet. J. 21, 177–179. Khalequzzaman, M.Y., Sultana, S., 2006. Insecticidal activity of Annona squamosa L. seed extracts against the red flour beetle, Tribolium castaneum (Herbst). J. Biol. Sci. 14, 107–112. Khan, M.H., 1986. Biology of Boophilus microplus (Can.) in Andamans. Indian J. Anim. Health 25, 7–9. Khan, M.H., 1996. Efficacy of pyrethroids against acarines infesting animals. Indian Vet. J. 73, 1257–1259. Khudrathulla, M., Jagannath, M.S., 2000. Effect of methonolic extract of Stylosanthes scabra on ixodid ticks of animals. Indian J. Anim. Sci. 70, 1057–1058. Kohn, W.K., Norval, R.A.I., 1994. Predation of ticks by chickens in Zimbabwe. Zimbabwe Vet. J. 25, 33–37. Kumar, A., Ansari, M.Z., Basu, A., Sahai, B.N., 1989. Incidence and intensity of tick infestation of cattle and buffaloes in Chotanagpur and Santhal Paragnas Region in Bihar. J. Res. Birsa Agric. Univ. 1, 221–225. Kumar, A., Rawat, B.S., Saxena, A.K., Agarwal, G.P., 1994. Prevalence of ectoparasites on goats in Dehradun (India). Appl. Parasitol. 35, 227–236. Kumar, K.P.R., 1996. Indian medicine industry under the emerging patent regimes. Ancient Sci. Life 15, 161. Kumar, R., Chauhan, P.P.S., Daya Shanker Agarwal, R.D., Kumar, R., Sanker, D., 2001. Efficacy of flumethrin pour-on against tick infestation on cattle and buffaloes. J. Vet. Parasitol. 15, 167–168. Kumar, R., Kumar, R., 1995. Artificial immunization of rabbits, Hyalomma dromedarii tick-derived midgut antigen. Exp. Appl. Acarol. 19, 319–324. Kumar, R., Kumar, R., 1996. Cross resistance to Hyalomma anatolicum anatolicum ticks in rabbits immunized with midgut antigens of Hyalomma dromedarii. Indian J. Anim. Sci. 66, 657–661. Lahkar, B.C., Borkakoty, M.R., Sarmah, P.C., 1994. Incidence pattern of Boophilus microplus (Canestrini, 1887) in cattle in Assam. J. Assam Vet. Counc. 4, 46–49. Latif, A.A., Pegram, R.G., 1992. Naturally acquired host-resistance in tick control in Africa. Insect Sci. Appl. 13, 505–513. Leemon, D., 2011. Fungal Biopesticide for Cattle Tick Control. Meat & Livestock Australia Limited, Locked Bag, pp. 991. Leemon, D.M., Jonsson, N.N., 2008. Laboratory studies on Australian isolates of Metarhizium anisopliae as a biopesticide for the cattle tick Boophilus microplus. J. Invertebr. Pathol. 97, 40–49. Leemon, D.M., Turner, L.B., Jonsson, N.N., 2008. Pen studies on the control of cattle tick [Rhipicephalus (Boophilus) microplus] with Metarhizium anisopliae (Sorokin). Vet. Parasitol. 156, 248–260. Magadum, S., Mondal, D.B., Ghosh, S., 2009. Comparative efficacy of Annona squamosa and Azadirachta indica extracts against B. microplus Izatnagar isolates. Parasitol. Res. 105, 1085–1091. Manohar, G.S., Banerjee, D.P., 1992a. Effects of immunization of rabbits on establishment, survival and reproductive biology of the tick Hyalomma anatolicum anatolicum. J. Parasitol. 78, 77–81.

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Manohar, G.S., Banerjee, D.P., 1992b. Immune response in rabbits immunized against Hyalomma anatolicum anatolicum. Indian J. Anim. Sci. 62, 505–512. Masika, P.J., Sonandi, A., Van Averbeke, W., 1997. Tick control by small-scale cattle farmers in the central Eastern Cape Province, South Africa. J. S. Afr. Vet. Assoc. 68, 45–48. Maske, D.K., Bhilegaonkar, N.G., Jangde, C.R., 1996. Treatment of tick infestation in cattle with pestoban. Ind. J. Indigen. Med. 17, 81–83. Maske, D.K., Bhilegaonkar, N.G., Sardey, M.R., 1998. Evaluation of acaricides. Ind. J. Indigen. Med. 19, 38–44. Maske, D.K., Sardey, M.R., Bhilegaonkar, N.G., 1992. Treatment of tick infestations in cattle with ivermectin. Indian Vet. J. 69, 57–58. Minjauw, B., McLeod, A., 2000. Epidemiology and economics of tick-borne diseases, their effects on the livelihood of poor in east and southern Africa and in India. Consultancy report to the Animal Health Programme (AHP) of the Department for International Development (DOID), Nairobo, Kenya, pp. 94. Minjauw, B., McLeod, A., 2003. Tick-borne diseases and poverty. The impact of ticks and tick-borne diseases on the livelihood of small scale and marginal livestock owners in India and eastern and southern Africa. Research report, DFID Animal Health Programme, Centre for Tropical Veterinary Medicine, University of Edinburgh, UK. Miranpuri, G.S., Jasmer, S., 1978. Ticks and mites from domestic animals in Assam, India, and their possible role in transmission of diseases. Indian J. Parasitol. 2, 11–14. Mondal, D.B., 2006. Health issues in high altitude wildlife and their management. Compendium of Lectures: ICAR summer school on Recent trends in wildlife health management and forensics w.e.f. 8th to 28th September, 2006. Organized by Centre for Wildlife Conservation Management & Disease Surveillance, IVRI, Izatnagar and sponsored by ICAR, pp. 248–257. Mondal, D.B., 2012. Advances in integrated tick control programme for the control of animal diseases. In: Compendium of 30th ISVM Conference w.e.f. 1st to 3rd Feb, 2012. Organized by College of Veterinary Sciences and AH, Central Agricultural University, Selesih, Aizawl, Mizoram, pp. 175–182. Mooring, M.S., Mundy, P.J., 1996. Interactions between impala and oxpeckers at Matobo National Park, Zimbabwe. Afr. J. Ecol. 34, 54–65. Mulenga, A., Tsuda, A., Onuma, M., Sugimoto, C., 2003. Four serine proteinase inhibitors (serpin) from the brown ear tick, Rhipicephalus appendiculatus; cDNA cloning and preliminary characterization. Insect Biochem. Mol. Biol. 33, 267–276. Narang, C., Suganya, M., Chanarang, R., Surat Wadee, J., Weerapol, J., 1988. Effective plant crude extract on tick (B. microphilus)-larvicidal action. Kasetsart J. Nat. Sci 22, 37–41. Nari, A., 1995. Strategies for the control of one-host ticks and relationship with tick-borne diseases in South America. Vet. Parasitol. 57, 153–165. Ndumu, P.A., George, J.P.D., Choudhury, M.K., 1999. Toxicity of neem seed oil (Azadirachta indica) against the larvae of Amblyomma variegatum, a three-host tick in cattle. Phytother. Res. 13, 532–534. Parmar, A., Grewal, A.S., 1996. Characterization of immunogenic components of Hyalomma anatolicum anatolicum: the vector of bovine tropical theileriosis. Curr. Sci. 70, 161–164. Parmar, A., Grewal, A.S., Dhillon, P., 1996. Immunological cross-reactivity between salivary gland proteins of Hyalomma anatolicum anatolicum and Boophilus microplus ticks. Vet. Immunol. Immunopathol. 51, 345–352. Patarroyo, J.H., Portela, R.W., De Castro, R.O., Couto Pimentel, J., Guzman, F., Patarroyo, M.E., Vargas, M.I., Prates, A.A., Dias Mendes, M.A., 2002. Immunization of cattle with synthetic peptides derived from the Boophilus microplus gut protein (Bm86). Vet. Immunol. Immunopathol. 88, 163–172. Pathak, D., Mathur, V.C., Latha, B.R., John, L., 2004. In vitro effect of indigenous plant extract on ixodid ticks of small ruminants. Indian J. Anim. Sci. 74, 616–617. Pathan, A.J., Raote, Y.V., Bharkad, G.P., 2003. Comparative efficacy of deltamethrin (butox) at different concentrations against ixodid tick infestations in cattle. Blue Cross 20, 12–13. Pipano, E., Alekceev, E., Galker, F., Fish, L., Samish, M., Shkap, V., 2003. Immunity against Boophilus annulatus induced by the Bm86 (Tick-GARD) vaccine. Exp. Appl. Acarol. 29, 141–149. Prasad, K.D., 1989. Babesia and babesiosis affecting Indian cattle. In: Compendium of Summer Institute on Arthropod-borne Diseases of Domestic Animals and Birds and Their Control held at Veterinary College Ranchi, May 22 – June 10, pp. 79–88. Pratap, G., Misra, S.C., Panda, M.R., 1991. A note of the incidence of ectoparasites on Black Bengal goats at Bhubaneswar. Indian Vet. J. 68, 92–94. Raizada, R.N., Nagar, S.K., 1979. Observations on the environmental stress on distribution and abundance of Boophilus microplus (Acarina: Ixodidae) and its preference for host and feeding sites in Uttar Pradesh. Indian J. Anim. Sci. 49, 622–628. Rajkhowa, S., Rajkhowa, C., Bujarbaruah, K.M., Hazarika, G.C., 2005. Seasonal dynamics of Boophilus microplus infesting mithum Bos frontalis of Nagaland. Indian J. Anim. Sci. 75, 25–26. Raote, Y.V., 1983. Incidence of parasitic infestation on organized cattle farms in Bombay region. M.V.Sc. thesis submitted to Konkan Krishi Vidyapeeth, Dapoli, Ratnagiri. Riding, G.A., Jarmey, J., McKenna, R.V., Pearson, R., Cobon, G.S., Willadsen, P., 1994. A protective concealed antigen from Boophilus microplus: purification, localization and possible function. J. Immunol. 153, 5158–5166. Samish, M., Glazer, I., 2001. Entomopathogenic nematodes for the biocontrol of ticks. Trends Parasitol. 17, 368–371.

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Samish, M., Ginsberg, H., Glazer, I., 2004. Biological control of ticks. Parasitology 129 (Suppl.), S389–S403. Sangwan, A.K., Sangwan, N., Goel, M.C., 2000. Progressive displacement of Hyalomma ticks by Boophilus microplus in Haryana. J. Parasitic Dis. 24, 95–96. Saxena, V.K., Rahman, S.J., 1985. Ixodid ticks from Kallar and Buliar areas of Nilgiri Hills (Tamilnadu). J. Commun. Dis. 15, 209–210. Seebeck, R.M., Springell, P.H., O’Kelly, J.C., 1971. Alterations in the host metabolism by the specific and anorectic effects of the cattle tick (Boophilus microplus) in food intake and body weight growth. Aust. J. Biol. Sci. 24, 373–380. Shahardar, R.A., Pandit, B.A., Bhat, A.S., 2002. Comparative efficacy of pestoban, diazinon and cypermethrin against Haemaphysalis tick infestation in sheep. Appl. Biol. Res. 4, 52–54. Sharma, B.D., Sharma, T., 1976. A note on contribution to the tick fauna of Jammu Province. Indian J. Anim. Sci. 44, 709–712. Sharma, J.K., Ghosh, S., Khan, M.H., Das, G., 2001. Immunoprotective efficacy of a 39 kDa purified nymphal antigen of Hyalomma anatolicum anatolicum. Trop. Anim. Health Prod. 33, 103–116. Shastri, U.V., Deshpande, M.S., Deshpande, P.D., 1983. Prevalence of hard ticks of cattle and buffaloes in Marathwada region (Maharashtra State) with notes on their habits. Cheiron 12, 318–322. Shaw, R.D., 1969. Tick control on domestic animals. (i) A brief history of the economic significance of tick infestations. Trop. Sci. 11, 113–119. Shrivastava, P.S., Sinha, S.R.P., 1990. Ectoparasiticidal and acaricidal efficacy of the herbal insecticide pestoban on cattle, buffaloes and dogs. Pashudhan 5, 4. Singh, J., Borkakoty, M.R., Miranpuri, G.S., Lahkar, B.C., 1978. Ixodid ticks infesting domestic and wild animals of Assam, India. Indian J. Parasitol. 2, 49–50. Singh, N.K., Ghosh, S., 2003. Experimental immunization of crossbred cattle with glycoprotein isolated from the larvae of Hyalomma anatolicum anatolicum and Boophilus microplus. Exp. Appl. Acarol. 3, 297–314. Singh, S., Chhabra, M.B., 1999. A note on ticks of camels in Haryana (India). J. Camel Pract. Res. 6, 77–78. Sivasankar, V., Rao, P.R., 1984. Tick fauna of Andhra Pradesh. Livestock Adv. Bangalore 9, 29–33. Soulsby, E.J.L., 1982. Helminths, Arthropods and Protozoa of Domesticated Animals, 7th ed. Bailliere Tindall, London, pp. 35–778. Sreekumar, C., Anandan, R., Balasundaram, S., John, L., 2000. Detection of an Ehrlichia bovis-like organism in cultured buffalo monocytes. Trop. Anim. Health Prod. 32, 62–67. Srivastava, R., Ghosh, S., Mondal, D.B., Azhahianambi, P., Singhal, P.S.D., Pandey, N.N., Swarup, D., 2008. Efficacy of Azadirachta indica extracts against Boophilus microplus. Parasitol. Res. 104, 149–153.

Stafford, K.C., Denicola, A.J., Kilpatrick, H.J., 2003. Reduced abundance of Ixodes scapularis (Acari: Ixodidae) and the tick parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae) with reduction of white-tailed deer. J. Med. Entomol. 40, 642–652. Sugino, M., Imamura, S., Mulenga, A., Nakajima, M., Tsuda, A., Ohashi, K., Onuma, M., 2003. A serine proteinase inhibitor (serpin) from ixodid tick Haemaphysalis longicornis: cloning and preliminary assessment of its suitability as a candidate for a tick vaccine. Vaccine 21, 2844–2851. Suliman, E.A., Mahammed, Y.O. The activity of Aspergillus terreus as entomopathogenic fungi on different stages of Hyalomma anotolicum anotolicum under experimental conditions. J. Entomol., in press Sundaram, S.G., Sasikala, J., Joseph, S.S., 1986. Studies on ixodid ticks of Tirunelveli in domestic animals. Indian J. Public Health 30, 101–105. Talukdar, S.K., Borkakoty, M.R., Sarmah, P.C., Saleque, A., 1998. Trial of deltamethrin and diazinon against Haemaphysalis bispinosa infestation in goats. J. Vet. Parasitol. 12, 137–138. Tellam, R.L., Kemp, D., Riding, G., Briscoe, S., Smith, D., Sharp, P., Irving, D., Willadsen, P., 2002. Reduced oviposition of Boophilus microplus feeding on sheep vaccinated with vitellin. Vet. Parasitol. 103, 141–156. Thakur, M., Singh, D.K., Varshney, B.C., Ragfhav, P.R.S., 1992. Experimental immunization of rabbits against Hyalomma anatolicum anatolicum. J. Vet. Parasitol. 6, 15–20. Trimnell, A.R., Hails, R.S., Nuttall, P.A., 2002. Dual action ectoparasite vaccine targeting exposed and concealed antigens. Vaccine 20, 3560–3568. Vatsya, S., Singh, N.P., 1997. Effects of chemical and herbal acaricides on calf skin. Indian J. Vet. Pathol. 21, 30–31. WHO, 1992. Vector resistance to pesticide. Fifteenth Report of the WHO Expert Committee on Vector Biology and Control, Geneva. Technical Report Service, no. 818, pp. 58. Willadsen, P., 2004. Anti-tick vaccine. Parasitology 129, S367–S387. Willadsen, P., Bird, P., Cobon, G.S., Hungerford, J., 1995. Commercialisation of a recombinant vaccine against Boophilus microplus. Parasitology 110, 43–50. Young, A.S., Groocock, C.M., Kariuki, D.P., 1988. Integrated control of ticks and tickborne diseases of cattle in Africa. Parasitology 96, 403–432. Zhioua, E., Heyer, K., Browning, M., Ginsberg, H.S., LeBrun, R.A., 1999. Pathogenicity of Bacillus thuringiensis variety Kurstaki to Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 36, 900–902.

Please cite this article in press as: Mondal, D.B., et al., Upcoming of the integrated tick control program of ruminants with special emphasis on livestock farming system in India. Ticks Tick-borne Dis. (2012), http://dx.doi.org/10.1016/j.ttbdis.2012.05.006