Accepted Manuscript Title: AN INSIGHT INTO THE ECOBIOLOGY, VECTOR SIGNIFICANCE AND CONTROL OF HYALOMMA TICKS (ACARI: IXODIDAE): A REVIEW Authors: M.S. Sajid, A. Kausar, A. Iqbal, H. Abbas, Z. Iqbal, M.K. Jones PII: S0001-706X(18)30862-3 DOI: https://doi.org/10.1016/j.actatropica.2018.08.016 Reference: ACTROP 4752 To appear in: Acta Tropica Received date: 6-7-2018 Revised date: 10-8-2018 Accepted date: 12-8-2018 Please cite this article as: Sajid MS, Kausar A, Iqbal A, Abbas H, Iqbal Z, Jones MK, AN INSIGHT INTO THE ECOBIOLOGY, VECTOR SIGNIFICANCE AND CONTROL OF HYALOMMA TICKS (ACARI: IXODIDAE): A REVIEW, Acta Tropica (2018), https://doi.org/10.1016/j.actatropica.2018.08.016 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. AN INSIGHT INTO THE ECOBIOLOGY, VECTOR SIGNIFICANCE AND CONTROL OF HYALOMMA TICKS (ACARI: IXODIDAE): A REVIEW M. S. SAJID 1 2 *, A. KAUSAR 3, A. IQBAL 4, H. ABBAS 5, Z. IQBAL 1, M. K. JONES 6 1. Department of Parasitology, Faculty of Veterinary Science, University of Agriculture, Faisalabad-38040, Pakistan. 2. One Health Laboratory, Center for Advanced Studies in Agriculture and Food Security (CAS-AFS) University of Agriculture, Faisalabad-38040, Pakistan. 3. Veterinary Research Institute (VRI), Lahore, Punjab, Pakistan. 4. Department of Parasitology, Riphah International University, Lahore, Punjab, Pakistan. 5. KBCMA, College of Veterinary and Animal Sciences (CVAS), Narowal, Sub-campus, UVAS, Lahore-51600, Pakistan. 6. School of Veterinary Science, The University of Queensland, Gatton Queensland 4343, Australia. Corresponding author: Dr. Muhammad Sohail Sajid Email: [email protected] Abstract Ticks (Acari: Ixodoidea) are important ectoparasites infesting livestock and human populations around the globe. Ticks can cause damage directly by affecting the site of infestation, or indirectly as vectors of a wide range of protozoa, bacteria and viruses which ultimately lead to lowered productivity of livestock populations. Hyalomma is a genus of hard ticks, having more than 30 species well-adapted to hot, humid and cold climates. Habitat diversity, vector ability, and emerging problem of acaricidal resistance in enzootic regions typify this genus in various countries around the world. This paper reviews the epidemiology, associated risk factors (temperature, climate, age, sex, breed etc.), vector role, vector-pathogen association, and reported control strategies of genus Hyalomma. The various proteins in saliva of Hyalomma secreted into the blood stream of host and the prolonged attachment are responsible for the successfulACCEPTED engorgement of female ticks in spite MANUSCRIPT of host immune defense system. The various immunological approaches that have been tried by researchers in order to cause tick rejection are also discussed. In addition, the novel biological control approaches involving the use of entomo- pathogenic nematodes and Bacillus thuringiensis (B. thuringiensis) serovar thuringiensis H14; an 1 endotoxin, for their acaricidal effect on different species and life cycle stages of Hyalomma are also presented. KEY WORDS Ticks, Hyalomma, prevalence, immunization, salivary glands, entomo-pathogenic nematodes 1 | SIGNIFICANCE OF TICKS Ticks (Acari: Ixodoidea) are voracious blood suckers, causing heavy blood losses. The livestock industry all around the globe is under economic threat due to ticks and tickborne diseases (Sajid et al., 2017). Tick infestation has been reported to cause reduction in live weight, affect appetite, body condition, blood composition, respiratory rate of animals, losses in milk production and damage to hides and open wounds leading to secondary infections (Springell, 1974; Rajput et al., 2006; Schroder et al., 2013). Three families of ticks are identified, including the recently identified family Nuttalliellidae, the Ixodidae, or hard ticks and Argasidae, the soft ticks (Guglielmone et al., 2010; 2014). The saliva of ticks contains several pharmacologically active chemicals which help in their blood feeding by modulating inflammation, immunity, and hemostasis of their host. Furthermore, antimicrobial factors are also the part of their saliva among the several other adaptations towards blood feeding (Brossard, 2004; Valenzuela, 2004; Steen, 2006; Hovius, 2008; Francischetti, 2009; 2010). Long hypostome ticks may induce abscesses due to secondary bacterial infections (Ambrose et al., 1999) and those with short hypostomes may cause devaluation of hides and skins (Jongejan & Uilenberg, 2004). As a result, ticks have a direct effect on the availability of good quality hides and skins to the leather industry. Ticks have been reported to cause severe irritation, allergy, toxicosis and paralysis therefore they are global public health problem (Aktaş, 2008; Bursali et al., 2012). Ticks infesting in ears can cause laceration, ear canal abrasion or bleeding leading to otitis externa (Al- Juboori, 2013) and in some cases, canal edema and external ear hyperemia have been reported (Gökdoğan et al., 2016). Ticks are known to cause lowered productivity (Sajid et al., 2007), mortality (Niyonzema & Kiltz, 1986) and can transmit Theileria (T.) spp., Babesia (B.) spp., Coxiella (C.) burnetii, Anaplasma (A.) spp., Rickettsia (R.) spp., and several viruses that causes deadlyACCEPTED diseases (Taylor et al., 2007; Bakheit etMANUSCRIPT al., 2012; Estrada-Peña & de la Fuente, 2014; Gortazar et al., 2014; CDC, 2016). An adult female tick can cause blood loss that can result in reduction in live weight gain of cattle (Pegram & Oosterwijk, 1990), dry matter intake and milk 2 yield (Jonsson et al., 1998). Finally, ticks may cause immunosuppression of host (Inokuma et al., 1993; Ferreira & Silva, 1998) that may facilitate the attack of other microorganisms resulting in disease. According to one estimate, more than one billion cattle of the tropics and subtropics are at risk of tick infestation (Pegram et al., 1993). Hyalomma spp. are the major vectors in the livestock population of Punjab, Pakistan (Durrani et al., 2008). A multi-host tick, Hyalomma (H.) anatolicum, infects the large ruminants and small ruminants acting as a vector for Theileria spp. specifically T. lestocardi (T. hirci), T. annulata and T. buffeli in India (Ghosh et al., 2008). It has been reported from Eurasia and Africa that several human and animal pathogens can be transmitted by Hyalomma ticks (Vial et al., 2016). Facial paralysis after a bite of H. marginatum species has been reported (Campbell, 1977; Gurbuz et al., 2010; Doğan et al., 2012). Tick paralysis in humans is also caused by Hyalomma spp. (Do˘gan et al., 2012). Theileria annulata, vectored by Hyalomma spp. worldwide, causes a disease called bovine tropical theileriosis, from which about 250 million cattle are at risk (Gharbi et al., 2006). 2 | GENERAL BIOLOGY AND LIFE CYCLE OF HYALOMMINE TICKS Hyalomma spp., Amblyomma spp., and Rhipicephalus (Boophilus) spp. are the economically important tick genera belonging to family Ixodidae (Guerrero et al., 2012). Hyalomma spp. can be morphologically identified on the basis specific features which include elongate mouthparts, presence of eyes, irregular festoons, an inornate dorsal shield, a characteristic banding pattern seen on the legs and lastly the spurs on the forecoxae subequal in length (Mathison & Pritt, 2014). The unfed Hyalomma ticks are 5 to 6mm in length including the mouthparts. Striations are present on integument and lateral suture is missing. Mouthparts are anterior. Palp articles 1 and 3 are short while articles 2 are comparatively longer. Angular lateral margins (medium) can be seen on basis capituli. Legs of Hyalomma ticks have these characteristics: slender, presence of pale rings and pulvilli. Brown coloured conscutum is present in the male (a scutum is present in the ACCEPTEDfeamle). Scutum and conscutum do not have MANUSCRIPT any enamel or ornamentation except in case of H. lusitanicum (Figure 1). Convex eyes are not unusual. In males and females, festoons are prominent but fade when females are engorged. Posterior to 4th pair of legs are the larger 3 spiracular plates which have scattered spiracle goblets. Only males have the ventral plates which are three distinct pairs, usually (Figure 2). Posterior to anus, these is an anal groove. The 4th coxae are of normal size and coxae 1 have equal and large paired spurs (Bowman and Nuttall, 2008; Sonenshine and Roe, 2014; Walker et al., 2014). Hyalommines are moderately-large to large ticks with long mouthparts, and are enzootic in Africa, south-eastern Europe and Asia (Kahn, 2008). Among the Hyalomma spp., most ticks are three host in nature and their larval, nymphal, and adult phases can be existed in free form in surrounding environment standing by for a suitable host. Larval and nymphal forms quest for small mammals including moles, rabbits, rodents and also birds and reptiles. Adult Hyalomma ticks find large vertebrate host including cattle, buffaloes, sheep, goat, dogs and humans. Hyalomma ticks can complete their life cycle in one, two or three variable hosts depending on that one they find. It takes three to four months or more than a year for