Hazard associated with tick species
Epidemiology and transmission of pathogens
Public health (surveillance and control)
Current areas of uncertainty
HAZARD ASSOCIATED WITH TICK SPECIES
Upsurge in Turkey and parts of Russia
Prior to 2005 the proportion of Hyalomma marginatum ticks collected from previous studies in Turkey did not exceed 5%. However in 2005, 74% of cattle were found infested with ticks, and 85% of ticks collected were Hyalomma marginatum .
Importation via migratory birds
Hyalomma marginatum is a common ectoparasite of passerine birds. Immatures remain attached for up to 26 days which enables their passive transport across continents [2-4] . Although it is likely that ticks on long-distance migrants are unable to establish, infested birds migrating short distances have a better chance of establishing new local populations (Vatansever, personal communication).
Importation via livestock
Livestock are at particularly high risk of importing Hyalomma marginatum as they can support large infestations. It is not uncommon for up to 100 Hyalomma ticks to be found on one animal . Tick control on imported livestock is rarely, if ever, performed.
Hyalomma marginatum ticks have a great capacity to support a wide range of temperature and humidity conditions . The tick’s ability to adapt to a wide range of conditions and a variety of habitats including arid open, marsh and scrub make it extremely difficult to eradicate on a large scale .
Hyalomma marginatum is the main vector of Crimean-Congo haemorrhagic fever virus in Europe .
Africa and Asia
Hyalomma marginatum is widely distributed across North Africa and Asia where it is reported from Algeria, Armenia, Azerbaijan, Egypt, Ethiopia, Georgia, Iran, Iraq, Israel, Morocco, Sudan, Syria, Tunisia and Turkey [3,7,9] .
Europe: Hyalomma marginatum is present in southern and eastern Europe, having been recorded in Albania, Bosnia and Herzegovina, Bulgaria, Croatia, Cyprus, France, Greece, Italy, Kosovo, the former Yugoslav Republic of Macedonia, Moldova, Montenegro, Portugal, Romania, Russia, Serbia, Spain and Ukraine [3,7,9-11] .
Several sporadic records have also been reported for imported animals, humans, and migratory birds in Germany , Hungary , Russia , Finland , Netherlands  and the UK [4,16] but these do not represent established populations.
Potential for future spread
Ectoparasites such as ticks have relatively little mobility by themselves, even Hyalomma marginatum. However, they can be transported over vast distances by their vertebrate hosts, in particular migratory birds and ungulates. Once attached to the skin of a host they may feed for a period of up to thirty days. It is the duration of attachment which enhances their ability for dispersal. Livestock in particular are at particularly high risk of importing ticks as they can support large infestations and it is not uncommon for up to 100 Hyalomma marginatum ticks to be found on one animal . A study of ticks infesting migratory birds entering the UK found that 21% of ticks collected were Hyalomma marginatum . The bird species most commonly infested with Hyalomma marginatum were Northern wheatear (Oenanthe oenanthe) and Whitethroat (Sylvia communis), with each positive bird harbouring 2‒5 nymphs. Hyalomma marginatum nymphs were also found singly on Sedge warbler (Acrocephalus schoenobaenus) and Common redstart (Phoenicurus phoenicurus).
Degradation of agricultural land leading to scrub encroachment has been identified as a risk factor for population explosions of Hyalomma marginatum, particularly when the land was previously cattle pasture .
Populations in the Mediterranean basin (southern Europe and North Africa) are currently considered to be regulated by rainfall and evapo-transpiration in summer. A decrease in both of these would be likely to have an impact on the available habitat for the tick and facilitate its spread towards northern latitudes. In contrast, populations in eastern Europe and the Caucasus are regulated by the minimum temperatures in late autumn. The low temperatures in late autumn force nymphs to overwinter engorged, with a subsequent high mortality rate. However, in regions where they currently survive, warmer autumns are allowing for the moulting of nymphs to adults, decreasing the mortality of the population and enabling gradual spread into suitable neighbouring territories . Models of the distribution of Hyalomma marginatum under climate warming scenarios predict that these ticks would be supported in some sites where they are currently absent, although some areas where the tick is now present would become unsuitable habitat under the same scenarios . The regions that showed the greatest probability of colonisation were Italy, south of the Alps, the Balkans, Romania, Ukraine, Moldova, wide areas of southern Russia and some areas of Germany and the Netherlands .
Livestock from the Balkans have previously been highlighted as a risk factor for importing Hyalomma marginatum into western Europe .
SPECIES NAME/CLASSIFICATION: Hyalomma marginatum Koch, 1844
Under the genus Hyalomma Koch, 1844, Hyalomma (Euhyalomma) marginatum Koch 1844 was previously considered to be a complex grouping four subspecies: Hyalomma (E.) marginatum marginatum Koch, 1844; Hyalomma (E.) marginatum rufipes Koch 1844; Hyalomma (E.) marginatum turanicum Pomerantzev, 1946 and Hyalomma (E.) marginatum isaaci Sharif, 1928 .
In 2008, Apanaskevich & Horak re-evaluated this taxonomic classification leading to the re-establishment of Hyalomma rufipes, H. turanicum and H. isaaci as full species and H. marginatum no longer being referred to as H. m. marginatum.
COMMON NAMESYNONYMS: Mediterranean Hyalomma;
OTHER NAMES IN USE: Hyalomma plumbeum Panzer, 1795 (mainly used in former Soviet countries) [3,18].
SUGGESTED IDENTIFICATION KEYS: A recent comprehensive taxonomic re-evaluation of the ‘marginatum’ group of Hyalomma ticks was published by Apanaskevich and Horak [3,18]. Useful information can also be found in [10,19-21]
Morphological characteristics/similar species
Hyalomma rufipes (distinguishable by dense punctuations, dense circumspiracular setae, and shape of the spiracular plate); Hyalomma turanicum (distinguishable by moderately dense punctuations, circumspiracular setae, and shape of the spiracular plate).
Hyalomma marginatum is a ditropic tick, meaning that engorged larvae remain on the same host to moult and feed again as nymphs. Adults seek and feed on a second host individual following a period of diapause . All stages are generally most active in the summer months [3,22] .
Active between June and October with peak numbers in July and August [23,24]. After feeding, the immatures either i) detach in early summer, moult to adults during the same season and overwinter as an adult or ii) those that feed in late summer detach in September/October and overwinter as nymphs, moulting to adults the following spring. However, the former is more common.
Adult ticks become active in spring when average monthly temperatures reach 10.5°C. They actively seek/wait for a host when average daily temperatures are 22‒27°C and humidity is 75‒100%. When air temperature increases above 30°C and soil temperature above 45°C, ticks prefer to hide or even bury themselves in the soil [23,25]. Males and females mate on the host, with one male mating with many females over several weeks. Engorged females drop off the host, lay up to 7 000 eggs in soil and die. Larvae hatch after 20‒40 days [22,26] .
Usually there is a maximum of one generation per year [3,19,22] .
In contrast to Ixodes spp. that passively wait for a passing host at an elevated location in vegetation, Hyalomma sp. actively seek their hosts [3,23,27] .
Adults of Hyalomma ticks prefer to feed on large animals (Artyodactyla and Perissodactyla). Adult Hyalomma ticks hide on the ground and actively run toward an animal host when they sense certain signals including vibration, visual objects, carbon dioxide, ammonia or body temperature heat. They can visually recognise the host from 3‒4 metres up to 9 metres [7,27]. Adults of Hyalomma asiaticum can follow the host for ten minutes or more and during that time they walk/run a distance of up to 100 metres [27,28] . Similar observations have also been recorded for Hyalomma marginatum (Vatansever, personal communication).
Immature stages preferably feed on small mammals such as Lagomorpha (Leporidae) and Insectivora (Erinaceidae) and ground-foraging birds, especially in the orders Passeriformes (Alaudidae and Corvidae) and Galliformes (Phasianidae) [23,24,29] They do not like to feed on rodents [22,26] . The immatures feed for two to three weeks with a resting period of three weeks to several months if they overwinter [3,19].
On birds and small-medium-sized wild mammals Hyalomma marginatum ticks congregate around the head, in particular in and around the ears . On hares, larvae first attach to the margins of the ears and after moulting to nymphs they migrate towards the face, neck and around the eyes (Z Vatansever, personal communication). As well as attaching to humans, adults are especially common on cattle and other ungulates including horses, sheep, goats, camels, deer and wild boar feeding for one to two weeks and mating on the host. On ruminants Hyalomma marginatum ticks congregate around the hind quarters, in particular the udder, scrotum, inguinal area and perineum .
Hyalomma marginatum ticks prefer the Mediterranean climate of North Africa and southern Europe with low to moderate levels of humidity and a long dry season during the summer months. Both immature and adult stages are characteristically found in steppe, savannah and scrubland hill and valley biotypes [3,9,10,19] . They are absent from contemporary and former European deciduous and mixed forest biotypes where they are replaced chiefly by Ixodes ricinus, and Dermacentor marginatus .
Environmental thresholds/constraints/development criteria
Adults are active at temperatures of >12°C [31,32] and larvae between 14‒16°C. Established populations are currently only maintained when the yearly accumulation of temperatures falls between 3 000‒4 000°C and water vapour deficit is below an average of 15 hPa . Cuticle hardening: larva-nymph five days, nymph-adult eigh8 days [23,32,33] . Feeding period: larva/nymph 26 days, adults 14 days .
Engorged nymphs and unfed adults are capable of overwintering, however mortality rates are increased for engorged nymphs compared to unfed adults [22-24,26] . Populations are reported as surviving at temperatures down to -20°C in Russia. Below this, population crashes have been reported .
Hyalomma ticks have well-developed eyes which are the main receptor for finding hosts and hiding places. In contrast to ambushing ticks such as Ixodes spp., they can migrate long distances horizontally. For example, Hyalomma asiaticum can migrate up to 500 metres in a month, but usually they disperse in a 80‒100m radius .
EPIDEMIOLOGY AND TRANSMISSION OF PATHOGENS
Hyalomma marginatum is considered to be the most important vector of Crimean-Congo haemorrhagic fever virus in Eurasia [3,8]. Rickettsia aeschlimannii has been isolated from Hyalomma marginatum ticks imported into Germany, Hungary and Russia on migratory birds [13,14,36] . This bacterium has also been detected in Hyalomma marginatum collected in Cyprus , and on the Italian island of Pianosa, an important stopping site for migratory birds . Dhori virus , Bahig virus  and Matruh virus  have also been isolated from this tick species; however, its vectorial capacity is yet to be determined.
Crimean-Congo haemorrhagic fever virus
Main vector and reservoir. Crimean-Congo haemorrhagic fever virus is maintained in the tick population by trans-stadial and trans-ovarial transmission with co-feeding and venereal transmission demonstrated for other Hyalomma spp. .
Infection in animals, other than suckling mice, is asymptomatic whereas in humans CCHFV is able to induce a severe multisystem syndrome associated with fever, shock and haemorrhage . Typically, the clinical course follows four distinct phases: incubation, pre-haemorrhagic, haemorrhagic and convalescence.
Confirmed disease risk
Crimean-Congo haemorrhagic fever virus is considered to be an emerging pathogen in Europe and the distribution of known tick vector species currently far exceeds that of the virus. The seasonality of human cases corresponds with the main tick activity period (spring to summer). The risk of migratory birds importing CCHFV via ticks is predicted to be very low . In the last decade Crimean-Congo haemorrhagic fever virus has been recognised as a growing problem in Eurasia, affecting several eastern European countries (Albania, Bulgaria, Kosovo and Russia), including the emergence of human clinical cases in Turkey (2002), Greece (2008), Georgia (2009) and most recently in 2010, India. Seroprevalence studies have also found evidence for virus circulation in Hungary , Portugal  and most recently Romania . Crimean-Congo haemorrhagic fever virus has been directly detected in Hyalomma marginatum collected in Turkey [48-50] , Bulgaria  and Spain .
PUBLIC HEALTH (SURVEILLANCE AND CONTROL)
Traditional flagging or dragging techniques suitable for many other ixodid ticks are less effective for hunter ticks such as Hyalomma marginatum. Instead, ticks can be collected directly from hosts while feeding or while seeking a host (collected from the ground).
To reduce contact with human populations clearing areas where ticks may survive and rest (i.e. haystacks, brush piles, leaf litter, etc.) has some benefits . However, Hyalomma marginatum ticks are particularly widespread in open lands, crop fields and scrub, which makes the use of area-wide acaricides unfeasible. It seems that the most effective way to control Hyalomma marginatum populations is periodical use of acaricides on ruminants.
The main groups of acaricides used for tick control (mainly targeted at livestock or livestock housing) are: pyrethroids, benzol-phenyl ureas, macrocyclic lactones, spinosad and fipronil . Options for use include dipping tanks, spray races or hand-held sprays, pour-ons, spot-ons and grease formulas for targeted application .
Humans can take measures for general tick avoidance, including wearing protective clothing and using chemical tick repellent such as permethrin or deltamethrin. It should be kept in mind that preparations that are effective against other ticks (Ixodes) are less effective against Hyalomma ticks. Sometimes they can stimulate attachment response in Hyalomma ticks  Z. Vatansever, personal communication) .
CURRENT AREAS OF UNCERTAINTY
There is little research on the level of resistance of Hyalomma marginatum populations to regularly used acaricides.
There is some evidence to suggest that subpopulations of this tick species have adapted to individual climate niches  - further research is required to explore whether such variations will affect future spread.
- The reason or combination of reasons which led to such a large population increase in Turkey in the late 1990s/early 2000s are still being debated. We know that in places where Crimean-Congo haemorrhagic fever occurs there is an increase in Hyalomma marginatum population and therefore human-tick contact. However, the reasons for this increase are still unknown and at the present time we can only speculate. These scenarios include:
1. Increase in wild animal population: personal observations support the fact that hare and wild boar populations have increased in Crimean-Congo haemorrhagic fever areas. Local predator-prey cycle imbalance has also been suggested as raising the risk of transmission .
- 2. Agricultural practice and migration: Focused in areas where agriculture is still practised with primitive tools and mostly based on human efforts (e.g. where the whole family is engaged in harvesting). Similarly, in places where there has been a migration towards the main urban centres, leaving abandoned land suitable for wildlife and scrub formation. This can also be affected by changes in land use resulting from changes in crop importation levels, thus reducing the need for locally grown crops, with the land subsequently returning to tick-suitable grassland .
- 3. Changes in animal husbandry and environmental regulations: In Turkey, the sheep population in the area has decreased by about 60-70% since 1990. Ministry of Environment regulations now strictly prohibit grazing of sheep and goat in bush and forests.
- a. Decrease in sheep population may influence the increase in hare and ground-feeding bird population [56,57] .
- b. Decrease in sheep population may have led to changes in tick composition (e.g. shift from Rhipicephalus to Hyalomma)
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