Mollov I., D. Georgiev, O. Todorov (Eds.) Faunistic diversity of the city of Plovdiv (Bulgaria), Volume 1 – Invertebrates Bulletin of the Natural History Museum – Plovdiv Bull. Nat. Hist. Mus. Plovdiv, 2018, Supplement 1: 37-46
Species Composition, Distribution and Seasonal Dynamics of Ixodidae Ticks Invaded Pasture Animals in the Region of Plovdiv City
Atanas Arnaudov1*, Dimo Arnaudov2
1 - University of Plovdiv „Paisii Hilendarski“, Faculty of Biology, Department of Human Anatomy and Physiology, 24 Tzar Assen Str., BG-4000 Plovdiv, BULGARIA 2 - Regional Research Veterinary Institute, BG-4006 Plovdiv, BULGARIA * Corresponding author: [email protected]
Abstract. Based on literary data and our own research, it was found out that there are 11 species of ixodid ticks that parasitise in pasture animals in the region of Plovdiv City. Their distribution, biological features and ecological and epidemiological significance are described in the current synopsis.
Key words: biotopes, Ixodid ticks, Plovdiv Region, tick sampling.
Introduction bixenic and trixenic) ticks consecutively parasitise Ixodid ticks are temporary obligate blood- on two or three different host species (VASILEV & sucking ectoparasites in vertebrates. Most of them VISHNYAKOV, 1977). parasitise on mammals, including on marsupials Ixodid ticks have great epidemiological and monotremes. Less frequently, the hosts could importance. They can transmit the causative be reptiles and birds, and there are few cases found agents of infectious or protozoal diseases on amphibians (Bufo marinus Gran.) and even on transovarially and through three-phase invertebrates - coleoptera (Platymeris horrida) and transmission, and also keep the pathogens molluscs (Limicolaria adansoni Pfr.) throughout their biological existence, which (POMERANTZEV, 1950). Ixodid ticks are makes them an important reservoir. commonly found worldwide and the largest species The populations of these arthropods contain diversity is characteristic for the subtropical and the genes that determine their effectiveness as tropical areas (BALASHOV, 1967). vectors of infectious diseases in their The duration of the development cycle of the heterozygous recessive alleles. Among species and different tick species varies depending on their populations, there are significant variations in the biological characteristics and the environmental vector's ability to carry pathogenic conditions they live in, ranging from 1 to 3-4 years. microorganisms. Their effectiveness as vectors of Based on their development and feeding transmissible infections is also influenced by age, patterns, the ixodid ticks can have one, two or nutrition and physiological state (MONOV, 2010). three hosts. One-host (or monoxenic) ticks spend In this publication, we present data from our all stages of their biological development on the own research, as well as from other authors on skin of the same host. Two- and three-host (or the distribution of ticks in the region of Plovdiv
© Bull. Nat. Hist. Mus. Plovdiv Regional Natural History Museum – Plovdiv http://rnhm.org/en/ University of Plovdiv Publishing House Species Composition, Distribution and Seasonal Dynamics of Ixodidae Ticks Invaded...
City, their biological characteristics and their (2004), MANGOLD et al. (1994), OMERAGIC ecological and epidemiological significance. (2011), PAPADOPOULOS et al. (1996), PAVLOVIĆ et al. (2013; 2014; 2016), RUBEL et al. (2016) and Material and Methods others. The ixodid tick hosts, which were investigated In Bulgaria, there are representatives of all six in our research, lived in farms that had different ixodid tick genera that are characteristic for the number of animals and were located in the continental temperate climate zone – municipalities of Asenovgrad, Parvomay, Sadovo, Rhipicephalus (Koch, 1844), Ixodes (Latreille, Saedinenie, Stamboliyski and Rodopi. Samples 1795), Dermacentor (Koch, 1844), Hyalomma were collected from sheep, goats, cattle and dogs (C. Z. Koch, 1844), Boophilus (Curtice, 1891), and and the investigations were conducted during the Haemaphysalis (Koch, 1844) (MINCHEVA et al., period 1999-2016, with some interruptions. 1965). According to DRENSKI (1955), The animals were examined monthly, during approximately 32 species can be found in the grazing period from their leave to the pasture Bulgaria. They are described in detail by BERON to their return to the barn (March - October). The (1973-1974). Most of the studies on the tick fauna examination of the animals for invasion was in Bulgaria, however, took place more than 4 performed in the following order: head (between decades ago. the horns and ears), neck, back, under the tail, groin, udder. After the collection, the tick samples MINCHEVA et al. (1965) collected and were stored in a 70% ethyl alcohol solution. identified more than 350,000 ticks from all over Determining the species of the collected ticks the country, describing their biotopes in every was carried out in the Laboratory of Parasitology region of the country, their epizootic significance at the Regional Research Institute of Veterinary and the seasonal variations of the parasites, as well Medicine, Plovdiv and in the laboratory at the as cases of piroplasmosis caused by them in Department of Anatomy and Physiology at the regions with diverse climate. According to the University of Plovdiv “Paisii Hilendarski”. The authors, in the Plovdiv region can be found 10 collected ixodid tick specimens were observed ixodid tick species within the six genera using a CARL ZEISS JENA binocular magnifier. mentioned above. The species determination was performed The studies on the species composition and the distribution of the ticks in the Plovdiv Region according to the descriptions of POMERANTSEV were triggered by the outbreak of the first (1950) and ESTRADA-PENA et al. (2004). epidemic of tick-borne encephalitis in Bulgaria in the village of Iskra in the region of Parvomay Results and Discussion Town in 1953. Studies on the distribution, species Similar studies were reported by SARBOVA composition and seasonal dynamics of ticks (1956) and PAVLOV et al. (1962) for the region of the village of Iskra in the municipality of conducted in Bulgaria and in other countries The dynamics of the global climate change Parvomay; GEORGIEV et al. (1971) and PAVLOV create a risk of drastic changes in the species et al. (1972) within a mass study of a viral composition of the ticks in a given geographic encephalitis epidemic on sheep and goats in the area (ESTRADA-PEÑA & VENZAL, 2007). This village of Dobrostan, Asenovgrad Municipality; necessitates further studies on the species ARNAUDOV et al. (2014) for the region of composition and the distribution of ixodid ticks. Parvomay; ARNAUDOV & ARNAUDOV (2017) for The high epidemiological significance of ticks the regions of Saedinenie, Stamboliiski, Sadovo from the Ixodidae family determines the number and the village of Gradina and Parvomay Town of existing studies on their spread, species and ARNAUDOV (2005) for the villages of Izbegli composition, seasonal dynamics and and Parvenets. epidemiological features in different geographic As a result of these studies, the following 11 regions – DANTAS-TORRES et al. (2011), tick species were found: Rhipicephalus bursa DUMITRACHE et al. (2012), ESTRADA-PENA & (Canestrini et Fanzago, 1877), Rhipicephalus SANTOS-SILVA (2005), ESTRADA-PENA & sanguineus (Latreille, 1806), Rhipicephalus VENZAL (2007), GILLOT (1985), HOOGSTRAAL turanicus (Pomerancev, 1940), Ixodes ricinus & VALDEZ (1980), JONGEJAN & UILENBERG (Linneaus, 1758), Dermacentor marginatus
38 Atanas Arnaudov, Dimo Arnaudov (Sulzer, 1776) Hyalomma plumbeum (Panzer, density of invasion is the highest (ARNAUDOV & 1795), Hyalomma scupense (Schulze, 1918), ARNAUDOV, 2017). Boophilus calcaratus (Birula, 1895), Rh. bursa has been established throughout the Haemophysalis sulcata (Canestrini & Fanzago, whole period during which the animals are on the 1878), Haemophysalis punctata (Canestrini & pasture, with the maximum of infestation being in Fanzago,1878) and Haemophysalis intermis June (ARNAUDOV & ARNAUDOV, 2017). Because (Birula, 1895). it is a thermophilic tick species, a connection can be found between the wide spread of this species and the climate conditions in the region of Distribution and biological characteristics of Plovdiv - wet and hot (HOOGSTRAAL & VALDES, ticks found in the Plovdiv Region 1980). For this reason it is also widespread in the Mediterranean region (PAPADOPULUS et al., 1996; The Genus Rhipicephalus ESTRADA-PENA & SANTOS-SILVA, 2005). In the region of Plovdiv City three species Rh. turanicus is also commonly found in the from this genus were identified - Rh. bursa, Rh. region of Plovdiv. It is usually observed together turanicus and Rh. sanguineus. with Rh. bursa, but it can be found earlier – in Rh. bursa (Fig. 1) is the most widespread March, and the majority of he infestation is in species in the area. On the territory of Plovdiv May (MINCHEVA et al., 1965). A typical species Region it was discovered in the village of Iskra by for dry subtropical areas (VASILEV & SARBOVA (1956) and by PAVLOV et al., (1962); in VISHNYAKOV, 1977), it prefers flat terrains and the municipalities of Parvomai, Saedinenie, pastures located not more than 500 m above sea Stamboliyski and Sadovo by ARNAUDOV et al. level. It is a three-host tick where the larvae and (2014), ARNAUDOV & ARNAUDOV (2017) and in pupae parasitise mainly on domestic and wild the villages of Izbegli and Parvenets by rodents and insectivores, and the imago forms ARNAUDOV (2005). According to MINCHEVA et invade even-toed ungulates and also domestic and al. (1965), it can be found across the entire wild carnivores. The larvae and pupae parasitise territory of the area except for the high-mountain their hosts between May and September and the areas. We think that explains why this tick was not imagos - between February and late September. detected in the village of Dobrostan in the Typically, only the mature individuals hibernate research conducted by GEORGIEV et al. (1971) (VASILEV & VISHNYAKOV, 1977). and PAVLOV et al. (1972), although it was Rh. turanicus is a carrier of diseases mainly in previously found at the foot of Mount Botev in domestic animals - piroplasmosis and the area of the resort near Kalofer Town anaplasmosis on ruminants, pigs and horses (MINCHEVA et al., 1965). Its biotopes include (MINCHEVA et al., 1965, VASILEV & pastures with lush vegetation, covered in bushes VISHNYAKOV, 1977). and weeds, natural meadows, pastures in short- Rh. sanguineus (fig. 2) was found on sheep stem forests and others, mostly located up to 500 and goats in the municipality of Parvomay m above sea level. In the plain areas, it is prevalent (ARNAUDOV et al., 2014), around the towns of in regions which have well-developed agriculture Saedinenie and Sadovo and the village of Tsarimir (MINCHEVA et al., 1965). and in sheep near the town of Stamboliyski Rh. bursa is a two-host type of tick. The larvae (ARNAUDOV & ARNAUDOV, 2017). We have also and the pupae predominantly parasitise on large observed a tick invasion on dogs in the towns of and small ruminants and the imago - on all Saedinenie and Sadovo (unpublished data). Nearly domestic animals, as well as on humans (VASILEV 42% of the dogs were infected, which is the & VISHNYAKOV, 1977; HOOGSTRAAL, 1979). As highest level of invasion. According to a two-host parasite, Rh. bursa plays an important MINCHEVA et al. (1965), Rh. sanguineus is spread role in the epidemiology of the Crimean Congo among dogs in a number of towns and villages in hemorrhagic fever (CCHF) in the countries on the area. Globally, it is the most common tick the Balkan Peninsula (PAPA et al., 2014; 2017; species (DANTAS-TORESS, 2010). SHERIFI et al., 2014). The maximum levels of infestation with this This tick is the predominant species acarid are reached in May and June. This can be parasitizing on sheep and goats, in which the related to its biological features – intense feeding
39 Species Composition, Distribution and Seasonal Dynamics of Ixodidae Ticks Invaded... and molting of the larvae and pupae in the imago forms parasitise on a variety of domestic summer (DANTAS-TORESS et al., 2011). and wild animals – cattle, buffaloes, horses, sheep, Rh. sanguineus is a three-host parasite, and its goats, dogs, deer, foxes, rabbits, badgers and main hosts are domestic and wild carnivores, it hedgehogs. It often invades (VASILEV & even parasitises on humans, although it is VISHNYAKOV, 1977). High humidity conditions relatively less anthropophilic (VASILEV & benefit the distribution of I. ricinus (ESTRADA- VISHNYAKOV, 1977, DANTAS-TORRES, 2008). PENA & SANTOS-SILVA, 2005), which explains That is why its epidemiological significance should the fact that two waves of infestation have been not be underestimated. observed - one in spring and one in autumn, during the wet months (March-April and The Genus Ixodes September) and its absence through the dry Within this genus, there are three species that months. Ix. ricinus is a widespread species in are found in Bulgaria - I. ricinus, I. redikorz and different parts of Europe (DANIEL et al., 2003; I. trianguliceps. In the area of Plovdiv City, only LINDGREN et al., 2000; GRAY, 1991). the first species has been found. In some areas of the former Yugoslavia and in I. ricinus (Fig. 3) was established in the village northern Greece, it is the predominant invasive species on small and large domestic ruminants of Iskra by SARBOVA (1956) and by PAVLOV et (OMERAGIC, 2011; PAVLIDOU et al., 2008; al. (1962) where it is the predominant parasitic PAVLOVIC et al., 2013; 2014; 2016). In Bulgaria, it species in cattle and goats. GEORGIEV et al. is the predominant species in the region of Veliko (1971) and PAVLOV et al. (1972) found it in the Tarnovo (GEORGIEVA, 1991). village of Dobrostan and ARNAUDOV et al. (2014) and ARNAUDOV & ARNAUDOV (2017) The Genus Dermacentor observed it in the municipalities of Parvomay, D. marginatus is the only representative of Saedinenie, Stamboliyski and Sadovo. According this genus in Bulgaria. It is known to be spread in to MINCHEVA et al. (1965), in the region of mountain-steppe and valley-steppe terrains but Plovdiv, the tick inhabits the long-stem beech can also be found in forest areas. Its biotopes are forests on of the northern slopes of the Rhodopes mainly mountain pastures covered in vegetation, Mountains, Sredna Gora Mountains and parts of but can also be found on open pastures, dry the Stara Planina Mountains. Its biotopes include valleys and on small, bushy hills. In the region of pastures in broadleaf forests, as well as bare Plovdiv, it has been found mostly in mountain terrains with bushes. Although it is a moisture- terrains – the valleys of Chepelarska River (Chaya) loving species, it avoids very wet and shady places and Vacha River (MINCHEVA et al., 1965), in the (MINCHEVA et al., 1965). In this respect, the village of Dobrostan, where it is one of the two Plovdiv Region is not particularly different to the species carrying viral Encephalomyelitis on sheep other regions in the country as the tick is and goats, as well as in the mountain parts of the distributed almost evenly in Bulgaria (DRENSKI, municipality of Parvomay (SАRBOVA, 1956, 1955). PAVLOV et al., 1962, ARNAUDOV et al., 2014). In Unlike its wide territorial distribution, the a more recent study, we found this tick species in invasion intensity of the species is relatively low. the region of Saedinenie and Stamboliyski, where However, according to LINDGREN et al. (2000), it its biotopes are the damp grassy terrains near the will grow under the influence of environmental, Maritsa River (ARNAUDOV & ARNAUDOV, 2017). climate and anthropogenic factors. This This tick is a three-host parasite. The larvae determines its high epidemiological significance as and the pupae invade smaller animals - rodents, its populations in many European countries are insectivores and others. The imago parasitises on highly infected with Borelia burgdorferi and other large and small ruminants (domestic and wild), dangerous pathogens (DUMITRACHE et al., 2012). odd-toed ungulates, dogs, rabbits, hedgehogs and ANGELOV et al. (1995) proved its leading role in others. It reproduces just once per year. the epidemiology of Lyme borreliosis in Bulgaria. Throughout the year, D. marginatus is one of I. ricinus is a three-host parasite. Its larvae the earliest ticks to be found - it starts invading and pupae parasitise mainly on rodents, but sheep and goats as soon as they start grazing during the summer months they mainly invade (mainly in March and in mild winters, in reptiles, wild ducks and small mammals. The February). Thus, two waves of infestation are
40 Atanas Arnaudov, Dimo Arnaudov likely to be observed - a spring (March-April) and piroplasmosis in horses in Southeastern Europe, a autumn (September-October) one, the former the Middle East and the South of Russia (SCOLES having higher levels of invasion. During the hot & UETI, 2015). months of the year, this tick species has not been Within the same genus, H. scupense (syn. H. detected (MINCHEVA et al., 1965; ARNAUDOV et detrium) is also found in the region. It has been al., 2014; ARNAUDOV & ARNAUDOV, 2017). located in the villages located in the Sredna Gora Besides in Bulgaria, this tick species is found Mts., near the Stryama River Gorge (MINCHEVA in many Mediterranean countries. There it et al., 1965). Its biotopes are hilly pastures in inhabits biotopes located in forests (especially the short-stem forests. In Bulgaria, this tick is Quercus sp.) at an altitude of 800-1000 m widespread in the region of Bourgas, where it (ESTRADA-PENA & SANTOS-SILVA, 2005). mainly invades cattle during the autumn-winter period and in early spring (MINCHEVA et al., The Genus Hyalomma 1965). Worldwide, H. scupense is one of the most H. plumbeum (Fig. 4) is widely spread in the widespread tick species out of the 30 valid region of Plovdiv. It is found in all parts of the Hyalomma species. It is present in the Palaearctic area, except for in the higher mountain areas. As zoogeographic region, in the humid to arid well as in this region of Bulgaria, it is commonly regions of 42 countries on three continents found throughout the whole country. It prefers (GHARBI & DARGHOUTH, 2014). low mountain areas, where it is the the most It is a single-host parasite. It parasitises mainly common tick species (SARBOVA & GEORGIEVA, on large ruminants and more rarely on sheep and 1973). It is also found in plains. It is the horses. It has been observed in spring months, predominant species in the region of Bourgas February, March and April, as well as in May when (GEORGIEVA, 1991). only single specimens have been found. Its Its biotopes are natural meadows, dry epidemiological significance is limited; it takes part pastures, field boundaries, old alfalfa fields, and in the spread of piroplasmosis in domestic animals. others (MINCHEVA et al., 1965). It sometimes It can be a reservoir of the cause of brucellosis and gets transported into the barns together with the plague (VASILEV & VISHNYAKOV, 1977). forage and this allows it to invade its hosts there. This tick species is a two-host parasite. The The Genus Boophilus larvae and the pupae mainly invade domestic and Within this genus, only one species, B. wild birds, as well as the European hare (Lepus calcaratus, is found across Europe, including in europeus), which is their main host. The imago Bulgaria. In the region of Plovdiv, it is widely form prarasitizes on large and small ruminants, distributed in places with altitudes of up to 750 m. odd-toed ungulates and pigs. It often attacks Its biotopes are situated on South-facing slopes humans as well (VASILEV & VISHNYAKOV, 1977). and hills with a high concentration of ravines, It is a predominant parasitic species for cattle streams and gullies and along river valleys (in the (ARNAUDOV & ARNAUDOV, 2017). areas of Saedinenie, Sadovo, Manole, Gradina). In H. plumbeum has a one-year life cycle. Its most of these biotopes there is a lush spring activity depends on the temperature and the vegetation, which lasts during the summer in the humidity, as well as on other environmental presence of precipitation. In the plains, where characteristics of their biotope. The larvae invade intensive agriculture is developed, the tick is not the European hare and some other hosts in June spread. and the pupae parasitise from July until the end of According to MINCHEVA et al. (1965) this October (and sometimes early November). The species is commonly found countrywide, except adult forms attack their hosts almost all year for in the regions of Sofia, Blagoevgrad, Smolyan, round (from February to December), with the Vidin, Vratsa, Montana and most of the Pleven intensity of invasion being the highest between and Lovech regions. Globally, it spreads in March and August. countries with tropical and subtropical climates Its important epidemiological significance is (TAYLOR et al., 2013). The northern boundaries determined by the fact that it is the main carrier of of its range reach a latitude of 490 North the tick-borne encephalitis (SARBOVA, 1964) and (VASILEV & VISHNYAKOV, 1977). is one of the main carriers of CCHF (SHERIFI et B. calcaratus is a single-host parasite. All of its al., 2014). In animals, the tick is a carrier of forms parasite mainly on cattle and sheep, and
41 Species Composition, Distribution and Seasonal Dynamics of Ixodidae Ticks Invaded... more rarely on pigs, horses and goats. In our and summer (April and July). The imago study, we only found it in cattle (ARNAUDOV & parasitises on even-toed ungulates, mainly on ARNAUDOV, 2017). Its invasion pattern is related sheep and goats. It attacks the hosts in winter in to the periods when the animals graze - the larvae two waves of invasion – In December and March. are found mostly in April, and the imago forms - Ha. punctata has a more limited distribution in May. This tick can be found on specific areas of in the region of Plovdiv. It is found in Sredna the animals’ skin - the head, neck and around the Gora Mts., as well as in the hilly part of the tail and more rarely on the ears and legs of the Parvomay Municipality (the villages of host. Its epidemiological significance is related to Pravoslaven, Dragoynovo and Bukovo) and in its ability of transmitting infectious agents the village of Dobrostan within the Asenovgrad transovarially and the possibility of the pathogen Municipality (MINCHEVA et al., 1965, to be stored in it for three generations. This tick is ARNAUDOV et al., 2014; PAVLOV et al., 1972). It a carrier of piroplasmosis in cattle, but it is not is known as well adaptive species. Its biotopes are dangerous for humans. both low, medium-high and high-mountain pastures. It prefers areas with abundant The Genus Haemaphysalis vegetation. In humid areas it is drawn to places The different species within this genus are with moderate humidity and dry biotopes – to widespread in all parts of the earth. The most wetter areas. species have been observed in Southeast Asia Ha. punctata is a three-host parasite. The (VASILEV & VISHNYAKOV, 1977). In the region larvae parasitise mainly on birds, and the pupae – of Plovdiv, the following species are found: Ha. on rodents and insectivores. The adults invade sulcata, Ha. punctata and Ha. intermis. Besides large and small wild and domestic ruminants, odd- them, H. otophila is also present in Bulgaria toed ungulates, pigs and other animals. The (MINCHEVA et al., 1965). Their epidemiological parasitism of this tick is outlined in two waves – significance is limited to spreading piroplasmosis spring and autumn. and some other bacterial and viral diseases in large Ha. intermis is found in the region of the and small ruminants. Together with D. Rhodope mountains – in the village of Dobrostan marginatus, Ha. punctata is one of the two (PAVLOV et al., 1972) and in Sredna Gora Mts., carriers of viral encephalitis in sheep and goats in mainly in the valleys of the rivers flowing down a natural outbreak in the village of Dobrostan in these mountains (Vacha River and others). Its the municipality of Asenovgrad (GEORGIEV et prevalence is mainly focal. The habitats of the tick al., 1971). are broadleaf forests at altitudes of up to 500 m. Ha. sulcata is the most widely spread in the Apart from the region of Plovdiv, in Bulgaria, it is region. It is known as the desert-steppe type. Its also found in the Burgas Region, and single biotopes are located on hilly areas that have individuals have been discovered in the northern pastures covered in bushes. It is found in the and middle slopes of the Stara Planina Mts. foothills of the Rhodopes Mts., Stara Planina and (MINCHEVA et al., 1965). Sredna Gora Mountains. In our study, it was This tick is a two-host parasite. The immature located in the hilly areas within the Parvomay forms parasitise on small mammals, rodents and Municipality, in the villages of Pravoslaven, insectivores. The imago parasitises mainly on Dragoynovo and Bukovo (ARNAUDOV et al., sheep, goats and deer, and it can also invade 2014). Across Bulgaria, the species is also spread humans. It is also found in other countries on the in Southeast Bulgaria and at isolated places in the Balkan Peninsula, in the Mediterranean, in France, region of Kyustendil. It is not found in Northern Poland and others. It parasitises during the winter months, which is why it is called "winter tick" Bulgaria (MINCHEVA et al., 1965). (SALMAN, 2012). Ha. sulcata is a two-host parasite. The larvae are found in sheep (on the ears) in winter and Acknowledgements. The authors thank spring. The pupae parasitise the same spots, but Svetla Gospodinova, Nelly Mukareva, Liliya during a different period - from April to Gavrailova and Victoriya Andreeva (University December. In November–December they also of Plovdiv “Paisii Hilendarski”) for their invade horses, cattle and young turkeys. The assistance in the collection and handling of larvae and pupae also parasitise reptiles in spring samples.
42 Atanas Arnaudov, Dimo Arnaudov
Fig.1. Rh. bursa female, dorsal side. X 0.6 Fig.2. Rh. sanguineus female, dorsal side. X 0.6 (original). (original).
Fig. 3. I. ricinus female, dorsal side. X 0.6 Fig. 4. H. plumbeum female dorsal side. X 0.6 (original). (original).
References ARNAUDOV A., D. ARNAUDOV. 2017. Ixodid ANGELOV L., D. ARNAUDOV, T. RAKADJIEVA, ticks on domestic ruminants: an D. LICHEV, E. KOSTOVA. 1995. Lyme Investigation in the Valley of Maritsa borreliosis in Bulgaria (epidemiologic River in Plovdiv Region, Bulgaria. Acta and epizootologic review). In: Report of Zoologica Bulgarica, Supplement 8: WHO Workshop on Lyme Borreliosis 221-226. Diagnosis and Surveillance. Warsaw, ARNAUDOV D., A. ARNAUDOV, D. KIRIN, S. Poland: 41-52. GOSPODINOVA. 2014. Ixodidae ticks of ARNAUDOV A. 2005. Biochemical and small ruminants in the region of hemocoagulant investigations on the Parvomai, southern Bulgaria. Bulgarian salivary glands of Ixodes ricinus and Journal of Agricultural Science, 20(3): Rhipicephalus bursa (Ixodidae) from the 590-594. Plovdiv region, Scientific studies of the BALASHOV Y. 1967. Blood-sucking ticks University of Plovdiv “P. Hilendarski” (Ixodidea) - vector of diseases of man - Biology, Animalia, 41: 13-22. (In and animals, Nauka, Leningrad, 320 p. Bulgarian, English summaries). (In Russian).
43 Species Composition, Distribution and Seasonal Dynamics of Ixodidae Ticks Invaded...
BERON P. 1973-1974. Catalogue des Acariens ticks of the natural focus of tick-borne parasites et commensaux des encephalitis of sheep and man in the Mammifères en Bulgarie. Bulletin d’ Rhodope Mountains (Bulgaria). Folia Institute de Zoology et Museum, Sofia, Parasitologica, 18(3): 267-273. Partie I, 37: 167-199; Partie II, 38: 105- GEORGIEVA G. 1991. Species composition and 136; Partie III, 39: 163-194. seasonal number of ixodidae ticks, DANIEL M., V. DANIELOVÁ, B. KŘÍŽ, A. JIRSA, isolated from two different geographic J. NOŽIČKA. 2003. Shift of the tick regions and their relation to Crimean Ixodes ricinus and tickborne haemorrhagic fever diseases. encephalitis to higher altitudesin central Epidemiological, Microbiological. and Europe. European Journal of Clinical Infectious Diseases, 27(4): 65-69. (In Microbiology and Infectious Diseases, Bulgarian). 22(5): 327-328. GHARBI M., M. DARGHOUTH. 2014. A review DANTAS-TORRES F. 2010. Biology and ecology of Hyalomma scupense (Acari, of the brown dog tick, Rhipicephalus Ixodidae) in the Maghreb region: from sanguineus. Parasites & Vectors, 3: 26, biology to control. Parasite, 21(2): 1-12. doi: 10.1186/1756-3305-3-26. GILLOT B. 1985. Bases biologiques, e’cologiques DANTAS-TORRES F., L. FIGUEREDO, D. et cartographiques pour l’etude des OTRANTO. 2011. Seasonal variation in maladies transmises par tiques (Ixodidae the effect of climate on the biology of et Argasidae) dans les Alpes Francaises et Rhipicephalus sanguineus in southern leur avant pays. PhD Thesis, Universite Europe. Parasitology, 38 (4): 527-536. de Grenoble, 535 p. DRENSKI P. 1955. Composition and GRAY J. 1991. The development and seasonal distribution of ticks (Ixodidae) in activity of the tick Ixodes ricinus: a Bulgaria. Bulletin of the Zoological vector of Lyme borreliosis. Revew of Institute, 4-5: 109-168 (In Bulgarian). Medical and Veterinary Entomology, 6: DUMITRACHE M., C. GHERMAN, V. COZMA, V. 323-333. MIRCEAN, A. GYORKE, A. SANDOR, A. HOOGSTRAAL H. 1979. The Epidemiology of MIHALCA. 2012. Hard ticks (Ixodidae) Tick-Borne Crimean-Congo Hemorrhagic in Romania: surveillance, host Fever in Asia, Europe and Africa. Journal associations, and possible risks for tick - of Medicinal Entomology, 15(4): 307-417. borne diseases. Parasitological HOOGSTRAAL H., R. VALDEZ. 1980. Ticks Resources, 110: 2067-2070. (Ixodoidea) from wild sheep and goats in ESTRADA-PENA A., A. BOUATTOUR, J. CAMICA, Iran and medical and veterinary implications. A. WALZER. 2004. Ticks of domestic Fieldiana Zoology, 6: 203-221. animals in the Mediterranean region: a JONGEJAN F., G. UILENBERG. 2004. The global guide to identification of species. importance of ticks. Parasitology, University of Zaragoza, Spain, pp. 1-131. 129(S1): S3-S14. ESTRADA-PENA A., J. VENZAL. 2007. Climate LINDGREN E., L. TÄLLEKLINT, T. POLFELDT. niches of tick species in the 2000. Impact of climatic change on the Mediterranean region: modelling of northern latitude limit and population occurrence data, distributional density of the disease-transmitting European constraints, and impact of climate tick Ixodes ricinus. Environmental Health change. Journal of Medicinal Perspectives, 108(2): 119-123. Entomology, 446: 1130-1138. MANGOLD A., D. AGUIRRE, A. GAIDO, A. ESTRADA-PENA A., M. SANTOS-SILVA. 2005. GUGLIELMONE. 1994. Seasonal The distribution of ticks (Acari: variation of ticks (Ixodidae) in Bos Ixodidae) of domestic livestock in taurus×Bos indicus cattle under Portugal. Experimental and Applied rotational grazing in forested and Acarology, 36(3): 233-246. deforested habitats in northwestern GEORGIEV B., B. ROSICKÝ, P. PAVLOV, M. Argentina. Veterinary Parasitology, DANIEL, D. ARNAUDOV. 1971. The 54(4): 389-395.
44 Atanas Arnaudov, Dimo Arnaudov MINCHEVA N., B. GEORGIEV, I. DJANKOV, Y. PAVLOVIĆ I., S. JOVČEVSKI, V. KUKOVSKA, A. DENEV, S. SHERKOV. 1965. DIMITRIĆ. 2014. Tick fauna of sheep Hemosporidioses of farm animals in and cattle at Kumanovo area Bulgaria and their carrier ticks. (Macedonia). Lucrari Stiintifice- Zemizdat, Sofia, 145 p. (In Bulgarian). Universitatea de Stiinte Agricole a MONOV V. 2010. Ecological Approach to Banatului Timisoara, Medicina Zoonoses. Bulgarian Medicinal Veterinara, 47(3): 88-95. Journal, 4(3): 7-11 (In Bulgarian). POMERANCEV B. 1950. Fauna SSSR - OMERAGIC J. 2011. Ixodid ticks in Bosnia and Paukoobraznye. Iksodovye kleshti Herzegovina. Experimental and (Ixodidae). Akademii Nauk SSSR, Applied Acarology, 53(3): 301-309. Moskow, 4, 2, 223 p. (In Russian). PAPA A., P. SIDIRA, V. LARICHEV, L. RUBEL F., K. BRUGGER, M. PFEFFER, L. GAVRILOVA, K. KUZMINA, M. CHITIMIA-DOBLER, Y. DIDYK, S. MOUSAVI-JAZI, U. STRÖHER, S. NICHOL. LEVERENZ, H. DAUTEL, O. KAHL. 2016. 2014. Crimean-Congo hemorrhagic fever Geographical distribution of virus, Greece. Emerging Infectious Dermacentor marginatus and Diseases, 20(2): 288-290. Dermacentor reticulatus in Europe. Ticks PAPA A., E. VELO, P. KADIAJ, K. TSIOKA, A. and Tick-borne Diseases, 7(1): 224-233. KONTANA, M. KOTA, S. BINO. 2017. SALMAN M. 2012. Ticks and tick-borne Crimean-Congo hemorrhagic fever virus diseases: geographical distribution and in ticks collected from livestock in control strategies in the Euro-Asia Albania. Infection, Genetics and region. CABI, 291 p. Evolution, 54: 496-500. SARBOVA S. 1956. Species composition and PAPADOPOULOS B., P. MOREL, A. AESCHLIMANN. seasonal dynamics of ticks of the family 1996. Tickcs of domestic animals in the Ixodidae, village of Iskra, the region of Macedonia region of Greece. Veterinary Parvomay. Works of the Research Parasitology, 63(1): 25-40. Institute of Epidemiology and PAVLIDOU V., S. GEROU, M. KAHRIMANIDOU, A. Microbiology, 3: 209-216 (In Bulgarian). PAPA. 2008. Ticks infesting domestic SARBOVA S. 1964. Distribution and animals in northern Greece. Experimental epidemiological significance of ticks of and Applied Acarology, 45(3-4): 195-198. the Ixodidae family in Bulgaria. – PAVLOV P., S. SURBOVA, O. MACHICHKA. Bulletin of the Zoological Institute with 1962. On the species composition of Museum, Sofia, 15: 135-150. ixodid ticks in the surroundings vill. SARBOVA S., G. GEORGIEVA. 1973. Particularities of Iskra, Plovdiv District. Bulletin of the the spread and parasitism of ticks of the Microbiological Institute, 11: 35-38 (In Ixodidae family in Bulgaria in view of their Russian). epidemiological significance. Epidemiology, PAVLOV P., H. RASHEV, B. GEORGIEV, D. Microbiology and Infectious Diseases, 3: 293- ARNAUDOV. 1972. Natural outbreak of 297 (In Bulgarian). viral encephalitis in sheep and goats in SCOLES G., M. UETI. 2015. Vector ecology of the vicinity of the village of Dobrostan. equine piroplasmosis. Annual Review Veterinarnomedicinski nauki, 9(6): 13- of Entomology, 60: 561-580. 19 (In Bulgarian). SHERIFI K., D. CADAR, S. MUJI, A. ROBAJ, S. PAVLOVIĆ I., S. IVANOVIĆ, A. DIMITRIĆ, M. AHMETI, X. JAKUPI, P. EMMERICH, A. VEGARA, A. VASIĆ, S. ŽIVKOVIĆ, B. KRÜGER. 2014. Crimean-Congo MIJATOVIĆ. 2016. Tick population in hemorrhagic fever virus clades V and VI goats and sheep in Šabac. Macedonian (Europe 1 and 2) in ticks in Kosovo. Veterinary Review, 39(1): 103-109. PLoS Neglected Tropical Diseases, 8(9): PAVLOVIC I., S. IVANOVIC, M. ZUJOVIC. 2013. e3168. Tick fauna of goat and sheep in TAYLOR A., R. COOP, R. WALL. 2013. Belgrade area. Scientific Works Series Veterinary Parasitology, 3rd edition, C, Veterinary Medicine, 59(1): 51-53. Hoboken (John Wiley& Sons), 600 p.
45 Species Composition, Distribution and Seasonal Dynamics of Ixodidae Ticks Invaded...
VASILEV I., Y. VISHNJAKOV. 1977. Veterinary Parasitology and Invasive Diseases, Zemizdat, Sofia, 413 p. (In Bulgarian).
Състав на видовете , разпространение и сезонна динамика на иксодови кърлежи (Ixodidae), паразитиращи по пасищни животни в Пловдивска област
АтанасАрнаудов , ДимоАрнаудов
Резюме: На базата на литературни данни и на собствени изследвания е установено, че по пасищните животни в Пловдивска област паразитират 11 вида иксодови кърлежи, принадлежащи към 6 рода. В настоящия обзор са описани тяхното разпространение, биологичните и екологичните им особености и епидемиологично значение..
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