J Parasit Dis https://doi.org/10.1007/s12639-020-01234-4

ORIGINAL ARTICLE

Ectoparasites of feral [ ferus caballus (Linnaeus., 1758)] on Karadag˘ Mountain, Karaman, Turkey

1 1 1 2 Bilal Dik • Onur Ceylan • Ceylan Ceylan • Mustafa Agah Tekindal • 3 2 1 Asma Semassel • Gonca So¨nmez • O¨ zlem Derinbay Ekici

Received: 20 February 2020 / Accepted: 3 June 2020 Ó Indian Society for Parasitology 2020

Abstract Approximately 250 feral horses [Equus ferus Keywords Tick Á Louse Á Bovicola equi Á caballus (Linnaeus, 1758)] living on Karadag˘ Mountain equina Á Haemaphysalis parva near Karaman City were caught by Kazakh herdsmen with permission of the Turkish Ministry of Agriculture and Forestry and brought to a farm in Karkın village in Konya Introduction Province, 70 km from Karadag˘, in November, 2017. This study was carried out to determine the presence of Linnaeus described domestic horse as Equus caballus in ectoparasites infesting a subsample of 36 feral horses. The 1758. Equus caballus, which is known as Equus ferus, horses were visually inspected, and then their bodies were contains seven subspecies some of which are extinct checked by hand for ectoparasites. Thirty-five (97.2%) (Bennett and Hoffmann 1999). The origin of domestic were infested with at least one of five species of ectopar- horses (Equus caballus caballus and Equus ferus caballus) asites: Bovicola equi (Linnaeus, 1758), stems from potential wild ancestors known as the Prze- (Linnaeus, 1758), Haemaphysalis parva (Neuman, 1897), walski horse and the Tarpan horse. Even today, the Prze- Hyalomma excavatum (Koch, 18449), Dermacentor walski horse (Equus ferus przewalskii Poliakov, 1881) lives marginatus (Sulzer, 1776). Most of the horses were coin- free in Siberia and Mongolia. The Tarpan horse (Equus fested with two ectoparasite species. Prevalence of infes- ferus ferus Boddaert, 1785) is a subspecies of the Eurasian tation with H. equina was 80.6% and with B. equi 72.2%. wild horse that is now extinct. In Anatolia, feral horses (E. In addition, prevalence of Ha. parva was 25.0%, Hy. ferus caballus) living free in nature are called the Yılkı excavatum 13.9%, and D. marginatus was 5.6%. This is the horse (Aksoy 2016). first systematic examination for external parasites of feral Ectoparasites such as ticks, mange mites, lice, fleas, and horses in Turkey. Further studies are needed to determine some flies are found on domestic horses. They can cause ectoparasites of greater numbers of feral horses in different irritation, itching, hair loss, deterioration of the skin qual- localities. ity, and decreased performance, and they can transmit several viral, bacterial, and parasitic agents (Halos et al. 2004; Laus et al. 2013). Two louse species Haematopinus asini (Linnaeus, 1758) & Bilal Dik and Bovicola (Werneckiella) equi (Denny, 1842) (Durden [email protected] and Musser 1994; Price et al. 2003; Gawler et al. 2005; Gu¨leg˘en and C¸ ırak 2005; Larsen et al. 2005; Bermu´dez 1 Department of Parasitology, Veterinary Faculty, Selc¸uk University, 42250 Selc¸uklu, Konya, Turkey et al. 2006; Lowden et al. 2007; Moreno et al. 2011; Payne et al. 2017) typically infest horses worldwide. Both species 2 Department of Zootechnics and Husbandry, Veterinary Faculty, Selc¸uk University, 42250 Selc¸uklu, Konya, Turkey are obligatory and permanent ectoparasites of horses and spend their entire lives on the hosts. It was reported that B. 3 Department of Veterinary Parasitology, Graduate School of Health Sciences, Selc¸uk University, 42250 Selc¸uklu, Konya, equi was common on Dartmoor ponies than privately Turkey owned horses (Gawler et al. 2005). It was stated that B. 123 J Parasit Dis equi is rarely seen on horses in USA and Ontario in Canada Materials and methods (Wright 1999; Gawler et al. 2005), and has narrowed dis- tribution in Panama and Cameroon (Bermu´dez et al. 2006; Approximately 250 feral horses [E. f. caballus (Linnaeus, Payne et al. 2017). 1758)] living on Karadag˘ Mountain near Karaman City Hippoboscid flies feed on mammals and birds. Hippo- were caught by Kazakh horse herdsmen with permission of bosca equina (Linnaeus, 1758) lives on horses; however, it the Turkish Ministry of Agriculture and Forestry and may be found on also (Hutson 1984). Adults of both brought to a farm in Karkın village in Konya Province, sexes are blood feeders. Their predilection sites are per- 70 km from Karadag˘, in November, 2017 (Fig. 1). We first ineal region and between the hind legs. Hippobosca equina visited the farm in late November, a few days after the cause disturbance on their hosts (Wall and Shearer 2001). horses were brought to the farm, and the second at the Ticks are significant vectors of the causative agents of beginning of December. On the first visit, 21 horses, and on piroplasmosis (theileriosis and babesiosis) in horses. There the second 15 horses were examined. When the horses are several studies reporting the tick infestations on horses were caught, their ear tags were checked. The horses in the Palearctic Region, including Turkey (Ros-Garcia caught the second time were released. During the study, 36 et al. 2013; Abedi et al. 2014; Shubber et al. 2014; Vial wild horses caught by the herdsmen were uniquely exam- et al. 2016; Tirosh-Levy et al. 2018). Haemaphysalis parva ined for ectoparasites. The horses were properly restrained Neumann, 1897; Hyalomma anatolicum Koch, 1844; and visually inspected for presence of ectoparasites. Head, Hyalomma excavatum Koch, 1844; Hyalomma marginatum mane, neck, shoulders, base of the tail, inguinal region and Koch, 1844; Hyalomma turanicum Pomerantsev, 1946; back of the horses were palpated by hand. We could not Rhipicephalus (Boophilus) annulatus (Say, 1821); Rhipi- examine the horses for mites. The ectoparasites collected cephalus bursa Canestrini and Fanzago, 1878; and Rhipi- from each horse were preserved separately in individually cephalus turanicus Pomerantsev, 1936 are known to infest labelled vials containing 70% ethanol, and brought to the Palearctic horses (Khosravi et al. 2012; Shubber et al. laboratory. All collected were examined using a 2014; Tirosh-Levy et al. 2018). Some researchers (Roth- stereozoom microscope (Nikon SMZ745T) and identified schild 2013; Scoles and Ueti 2015) reported that equine to family, and/or species, if possible. Ticks were piroplasms, which are the most significant infectious agents identified by using Estrada-Pen˜a et al. (2004) and Karaer of horses, can be transmitted by a great number of ticks et al. (1997). Lice were cleared in 10% potassium including Dermacentor marginatus, D. nuttalli, D. pictus, hydroxide at room temperature for 1 day, rinsed in distilled D. reticulatus, D. silvarum, Hyalomma anatolicum, Hy. water, dehydrated in 70% and then 99% ethanol for a few excavatum, Hy. dromedarii, Hy. lusitanicum, Hy. hours to 1 day, respectively, and mounted in Canada bal- marginatum, Hy. scupense, Hy. truncatum, Ixodes ricinus, sam on microscope slides. Slides were kept in a drying Rhipicephalus bursa, Rh. annulatus, Rh. sanguineus and oven at 50 °C for 3 weeks, and the specimens then iden- Rh. turanicus in this region. tified using a compound microscope. Nomenclature of the Equine ectoparasites are poorly studied in Turkey. lice follows Price et al. (2003) and Werneck (1936). Hip- Haematopinus asini, B. equi (Merdivenci 1965;I˙nci et al. poboscid flies were identified by using Maa (1963) and 2010) and H. equina (Merdivenci 1965) have been detected Hutson (1984). on domestic horses in Turkey. However, there are no data SPSS 25 (IBM Corp. Released 2017. IBM SPSS on the prevalence of these lice in feral horses, though B. Statistics for Windows, Version 25.0. Armonk, NY: IBM equi infested two of 15 examined domestic horses in Bursa Corp.) was used for data analysis. Prevalence (% infested), Province, Turkey (Gu¨leg˘en and C¸ ırak 2005). Although multi-response percentage and frequency values were used there are some data on species of ticks infesting domestic as variables. horses in Turkey, the prevalences of these ticks have not been studied (Karaer et al. 1997). Although all these studies were carried out on domestic Results horses, we could not find any published reports on ectoparasites infesting feral horses in Turkey. This study Thirty-five (97.2%) of the 36 horses examined were was performed to assess ectoparasite species on the feral infested with ectoparasites. Five species of ectoparasites horses brought to Konya from Karadag˘, Karaman, in were found: B. equi, Hippobosca equina, Ha. parva, Hy. Central Anatolia, Turkey. excavatum, Dermacentor marginatus were detected (Table 1). Prevalence of Hippobosca equina was 80.6%, and this rate was detected 72.2% for B. equi, 25.0% for Ha.

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Fig. 1 Locality where feral horses were captured, and study area where ectoparasites were collected

Table 1 Summary of the ectoparasites found on 36 examined feral horses in Turkey Ectoparasite species Number of infested hosts Female Male Nymph Total number of parasites

Hippobosca equina 29 41 52 – 93 Bovicola equi 26 52 0 103 155 Haemaphysalis parva 93110041 Hyalomma. excavatum 53407 Dermacentor marginatus 21102 Total – 128 67 103 298

parva, 13.9% for Hy. excavatum, and 5.6% for D. Discussion marginatus. Infestation status of horses with species of ectoparasites We found only one publication related to parasites of the is shown in Table 2. Mean intensity of all ectoparasites per feral horses in Turkey. In that study, faecal samples from infested horse was 8.5 (range 1–27). Mean intensity was feral horses were collected near the water reservoir on 6.0 (range 1–20) for B. equi, 4.6 (range 1–11) for Ha. Karadag˘ Mountain and examined for helminth eggs parva, 3.2 (range 1–10) for H. equina, 1.4 for (range 1–2), (Karaman Il C¸ evre ve Orman Mu¨du¨rlu¨gu¨ 2010). We found Hy. excavatum, and 1.0 for D. marginatus. no published papers on the presence or prevalence of ectoparasites infesting feral horses in Turkey. It is very difficult to do such a study, because it is necessary to get permission from the Ministry of Agriculture and Forestry

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Table 2 Infestation status of the horses with ectoparasites Infestation (n) species Infested horses (n) %

None (1) – 1 2.8 One species (8) H. equina 5 13.9 B. equi 3 8.3 Two species (20) B. equi ? H. equina 15 41.7 H. equina ? Hy. excavatum 2 5.5 B. equi ? Ha. parva 2 5.5 H. equina ? Ha. parva 1 2.8 Three species (5) H. equina ? Ha. parva ? Hy. excavatum 1 2.8 B. equi ? H. equina ? Ha. parva 2 5.5 B. equi ? H. equina ? Hy. excavatum 1 2.8 B. equi ? Ha. parva ? D. marginatus 1 2.8 Four species (2) B. equi ? H. equina ? Ha. parva ? D.marginatus 1 2.8 B. equi ? H. equina ? Ha. parva ? Hy. excavatum 1 2.8 Total 36 100.0

to conduct research. In addition to this, it is difficult to find in either the Mediterranean countires (Estrada-Pen˜a et al. and catch feral horses. This study was carried out oppor- 2004) or Africa (Walker et al. 2014). Haemaphysalis parva tunistically on feral horses captured for other purposes was reported on ruminants, horses, hares and humans in shortly after their transfer from Karadag˘ to Karkın village Turkey (Karaer et al. 1997;C¸ icek 2004; Bursali et al. 2012; in Konya. The horses were wild and free, difficult to catch, Keskin 2014; Dik and Uslu 2018; Orkun 2018). In Turkey, and to distinguish from each other. Even horses examined this species has been reported as the most common species were difficult to lasso by skilled Kazakh horse herdsmen of Haemaphysalis spp. collected from cattle and sheep in and a challenge to examine for ectoparasites by reseachers. Ankara Province (C¸ icek 2004). Haemaphysalis parva has Hyalomma anatolicum and Rh. annulatus previously been identified as the most common Haemaphysalis spe- were found on domestic horses in Central and Southern cies collected on humans in Tokat Province (Keskin 2014). Iraq (Shubber et al. 2014). In Iran, 63 (52%) of 120 horses C¸ icek (2004) stated that numbers of adult Ha. parva in Ahwaz Region were infested with ticks. Hyalomma peaked on sheep, goats, and cattle in March and October in species were common, while Rhipicephalus and Boophilus Ankara Province. Numbers of this species peaked in species were less prevalent. The mean intensity of all ticks autumn in Israel (Tirosh-Levy et al. 2018). Hyalomma was 13 per horse (Khosravi et al. 2012). In Israel, 396 excavatum occurs on mammals including horses (Bursali horses in 24 farms were examined for ticks, 25% of horses et al. 2012; Walker et al. 2014), and it has been previously were infested with ticks, 70% of 3267 ticks collected were reported from sheep, cattle, horse, and humans in Turkey Hyalomma spp., and the most common species was (Bursali et al. 2012). This species was detected as the most expressed as Hy. excavatum. In addition, Ha. parva, Rh. common species on horses in Israel (Tirosh-Levy et al. turanicus, Rh. annulatus, and Hy. marginatum species have 2018). Our unpublished experiences show that Hy. exca- been found, and a few samples of Rh. bursa, Hy. rufipes vatum is common on sheep and cattle between spring– and Hy. turanicum were present (Tirosh-Levy et al. 2018). autumn in Konya Province. Unfortunately, no published Some researchers (Khosravi et al. 2012; Shubber et al. paper could be found on prevalence of this species on 2014; Tirosh-Levy et al. 2018) reported that Hyalomma horses in our country. spp. were dominant on horses. Some authors (Estrada-Pen˜a et al. 2004; Walker et al. Some tick species, including Ha. parva and D. 2014) stated that D. marginatus occurs mainly in Europe marginatus, previously were detected on domestic horses and very locally in North Africa, where it has been reported in Turkey (Karaer et al. 1997; Bursali et al. 2012). from cattle, sheep, goats, dogs, and humans. This species Haemaphysalis parva lives on many mammal and bird was rarely found on ruminants in southwest Iran (Fatemian species in the Palearctic Region (Bursali et al. 2012; et al. 2018), but it could not be detected on horses in Israel Guglielmone et al. 2014), but Guglielmone et al. (2014) did (Tirosh-Levy et al. 2018). Adults are active during the end not specifically mention equine hosts. Interestingly, Ha. of autumn through into winter in Africa (Estrada-Pen˜a parva is not treated in the tick faunas on domestic et al. 2004; Walker et al. 2014). Similarly, this species was

123 J Parasit Dis reported from sheep, goats, cattle, and humans (Karaer Dartmoor ponies. According to the some authors (Wright et al. 1997; Bursali et al. 2012; Keskin 2014), and peaked 1999; Gawler et al. 2005), some researchers stated that B. in autumn in Turkey (Bursali et al. 2012). No published equi is rarely seen on horses in USA and Ontario in paper could be found relevant to this species found on Canada. Similarly, B. equi had a limited distribution in horses in Turkey. In the current study, ixodid ticks infested Panama and Cameroon (Bermu´dez et al. 2006; Payne et al. one-third (12 of 36) of the examined feral horses, with Ha. 2017). On the other hand, in Iceland, Larsen et al. (2005) parva the most prevalent (25.0%), followed by Hy. exca- reported that 38 (40.9%) of 93 horses were infested with B. vatum (13.9%), and D. marginatus (5.6%). Most impor- equi, and that 68 horses (73.1%) had signs of dermato- tantly, these findings may vary depending on the season, logical pathology, but lice were detected on only 32 of the vegetation, and climate during the study. 68. Bovicola equi was found on two horses on a farm in According to our findings in Central Anatolia, Rhipi- Bursa province of Turkey (Gu¨leg˘en and C¸ ırak 2005). This cephalus and Hyalomma species typically/usually are species is mostly found on the neck, shoulders, mane, found on sheep, goats, and dogs, especially from spring to trunk, and base of the tail of the horses (Gawler et al. 2005; autumn, whereas Dermacentor and Haemaphysalis species Larsen et al. 2005; Lowden et al. 2007; Moreno et al. are mostly found in early spring, autumn, and winter. Our 2011). This species is more common on horses in sta- unpublished experiences showed that Rhipicephalus bles during winter months, and the females are usually far turanicus is the most common species in the provinces of more abundant than males (Moreby 1978; Gawler et al. Karaman and Konya, while Rh. sanguineus and Rh. bursa 2005; Lowden et al. 2007; Moreno et al. 2011). In our are less common. We know that Rhipicephalus species are current study, B. equi infested 26 (72.2%) of the 36 feral not active in the season that the study was carried out in horses examined. A small number of B. equi were found on Central Anatolia (Bursali et al. 2012; Keskin 2014). They the horses, and intensity of lice varied from 1 to 20 (mean could be seen earlier or later, depending on the weather intensity 6). Undoubtedly, this number is an underestimate conditions of that year. However, we have no data that of the actual number. These horses were wild and could not these species infest horses in this region. In the same be examined thoroughly because they could not be province, Hy. marginatum is rarely seen, and Hy. rufipes restrained long enough. Of the 155 B. equi collected, 52 and Hy. turanicum have not yet been reported. Derma- were females and 103 were nymphs; no males were found. centor marginatus and Ha. parva were mostly observed on These findings support previous reports that females of B. domestic animals grazing on pasture (Karaer et al. 1997) equi are parthenogenetic (Moreby 1978; Lowden et al. and on hares in nature (Dik and Uslu 2018) in autumn and 2007; Moreno et al. 2011). Although this research was winter in Turkey. Our study was carried out in late conducted at the end of autumn, B. equi was quite common November and early December, and Ha. parva was the on the horses on pasture. As reported by some researchers dominant tick species on feral horses. Mean intensity of (Gawler et al. 2005; Larsen et al. 2005; Lowden et al. 2007; Ha. parva. was 4.6 (range 1–11), while 1.4 for (range 1–2) Moreno et al. 2011), B. equi was detected on the neck, Hy. excavatum and 1.0 for D. marginatus. These findings mane, and abdomen of the horses in the current study. The are consistent with the above data. Conversely, Rh. bursa, dermatological signs, hair loss, and focal alopecia were Rh. annulatus, Rh. turanicus, Hy. marginatum, Hy. rufipes observed on most of the horses in the current study, and and Hy. turanicum reported from horses in Iraq and Israel, there were bite wounds on some of the horses. However, it were not collected on the horses in this study. was not clear whether these wounds were caused by horses Some ixodid ticks are the main vectors of the agents of biting each other, engendered by lice, mites, or other theileriosis and babesiosis in horses, as in other mammals. ectoparasites, or the result of other reasons. Haematopinus Theileria equi and Babesia caballi are transmitted by some asini infests horses in Turkey (Merdivenci 1965; Inci et al. ixodid tick species belonging to the genera Dermacentor, 2010), but there are no published data about its prevalence. Hyalomma, and Rhipicephalus (De Waal 1992; Uilenberg Haematopinus was not found on any feral horses in this 2006). The presence of Hy. excavatum, and D. marginatus study. on the horses in this study shows that these horses are at Hippobosca equina lives on horses, however, it may be risk of theileriosis and babesiosis. As a matter of fact, T. seen on cattle (Hutson 1984). They are blood feeders, and equi and B. caballi were detected in PCR and some of the prefer to feed from perineal region and between the hind blood smears prepared from the feral horses in the study legs. Hippobosca equina cause disturbance on their hosts (unpublished data). (Wall and Shearer 2001). Bartonella chomelii and/or B. Bovicola equi is an ischnoceran louse species, that schoenbuchensis were detected by PCR in all 12 H. equina infests horses worldwide. Gawler et al. (2005) stated that B. collected from cattle in different parts of France, but none equi (Werneckiella equi equi in the article) on privately of the six H. equina collected from horses were positive for owned horses was found rarely, while it was common on Bartonella (Halos et al. 2004). We found that H. equina 123 J Parasit Dis was the most common ectoparasite species on the feral Bermu´dez SE, Miranda R, Medianero E (2006) Ectopara´sitos de horses. We could not find any publication on the pre- mamı´feros dome´sticos en Panama´ oriental, con notas sobre su importancia me´dica y veterinaria. Sci (Panama´) 21(1):19–32 valance of H. equina on horses or other hosts in Turkey. Bursali A, Keskin A, Tekin S (2012) A review of the ticks (Acari: However, our unpublished experiences show that this Ixodida) of Turkey: species diversity, hosts and geographical species is present on domestic horses in our province. It distribution. Exp Appl Acarol 57:91–104 was reported that Hippobosca was a summer species in the C¸ icek H (2004) Epizootiological studies on Haemaphysalis ticks in Ankara Province, Turkey. Turk J Vet Anim Sci 28:107–113 UK, occurring from end of spring to middle of autumn, but De Waal DT (1992) Equine piroplasmosis: a review. Br Vet J peaking in August and early September (Hutson 1984). In 148:6–14 our study, we found this species in late November and early Dik B, Uslu U (2018) Ectoparasites of hares (Lepus europaeus, December as the most common ectoparasite species, but Pallas) in Konya Province, Turkey. Turk J Vet Anim Sci 42:65–72 usually in low numbers. The mean intensity of H. equina Durden LA, Musser GG (1994) The sucking lice (Insecta, Anoplura) per infested horse was 3.2 (range 1–10). of the world: a checklist with records of mammalian hosts and Nineteen of the horses (52.8%) were coinfested with two geographical distributions. Bull Am Mus Nat Hist 218:1–90 ectoparasite species, and in most of these cases (13 cases), Estrada-Pen˜a A, Bouattour A, Camicas JL, Walker AR (2004) Ticks of domestic animals in the Mediterranean region: a guide to B. equi and H. equina were found together in the present identification of species. University of Zaragoza, Zaragoza study. The other combinations formed by multiple species Fatemian Z, Salehzadeh A, Sedaghat MM, Telmadarraiy Z, Hanafi- were detected rarely: one and three species in seven cases Bojd AA, Zahirna AH (2018) Hard tick (Acari: Ixodidae) species each (19.44%), and four species in two cases (5.56%), and of livestock and their seasonal activity in Boyer-Ahmad and Dena cities of Kohgiluyeh and Boyer-Ahmad Province, South- five species in one case (2.78%). Hippobosca equina and B. west of Iran. Vet World 11(9):1357–1363 equi were present as single species in five cases (13.89%) Gawler R, Coles GC, Stafford KA (2005) Prevalence and distribution and in two cases (5.56%), respectively. Further studies are of the horse louse, Werneckiella equi equi, on hides collected at a needed to determine ectoparasites of greater numbers of horse abattoir in south-west England. Vet Rec 157:419–420 Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, feral horses in different localities. Estrada-Pen˜a A, Horak IG (2014) The hard ticks of the world (Acari: Ixodida: Ixodidae). Springer, New York. Acknowledgement The authors would like to thank Selcuk Univer- https://doi.org/10.1007/978-94-007-7497-1 sity Scientific Research Projects Coordination Office for financial Gu¨leg˘en E, C¸ ırak VY (2005) Bir At C¸ iftlig˘inde Bovicola (Damalinia) support for this project (BAP Project No: 18401042). We also cor- equi (Linnaeus, 1758) enfestasyonu ve tedavisi. Tu¨rkiye Paraz- dially thank to Dr. Terry Galloway from Department of Entomology, itol Derg 29(2):183–184 University of Manitoba, Winnipeg, Manitoba, Canada, for his sci- Halos L, Jamal T, Maillard R, Girard B, Guillot J, Chomel B, entific and linguistic edition of the manuscript. The authors also thank Vayssier-Taussat M, Boulouis HJ (2004) Role of reviewers due to their valuable comments and appreciated flies as potential vectors of Bartonella spp. infecting wild and contributions. domestic ruminants. Appl Environ Microbiol 70(10):302–305 Hutson AM (1984) Keds, flat-flies and bat-flies. Diptera, Hippobosci- Authors’ contribution BD designated the research. BD, OC, CC, dae and Nycteribiidae. In: Fitton MG (ed) Handbooks for the and AS carried out field and laboratory experiments. MAT performed identification of British , vol 10, Part 7. Royal Entomo- statistical analysis. The manuscript was written by BD, finally revised logical Society of London. Dramrite Printers Limited, Southwark by ODE, OC, CC and GS. All authors read and approved the final Inci A, Yıldırım A, Dik B, Duzlu O (2010) Current knowledge of form of the manuscript. Turkey’s louse fauna. Tu¨rkiye Parazitol Derg 34(4):212–220 Karaer Z, Yukarı BA, Aydın L (1997) Tu¨rkiye Keneleri ve Compliance with ethical standards vekto¨rlu¨kleri. In: Ozcel MA, Daldal N (eds) Parazitoloji’de Artropod Hastalıkları ve Vekto¨rler, Tu¨rkiye Parazitoloji Derneg˘i, Conflict of interest The authors declare that they have no competing 13th edn.˙ Izmir, Tu¨rkiye, pp 363–434 interest. Karaman˙ IlC¸ evre ve Orman Mu¨du¨rlu¨g˘u¨ (2010) Karadag˘ mevkiindeki Yılkı atlarının durum tespiti, genel sag˘lık durumları,u¨remeler- inin kontrolu¨ ve c¸evre u¨zerindeki etkilerinin deg˘erlendirilmesi projesi. Mevlana Kalkınma Ajansı Teknik Destek Projesi, References Referans No: TR52-10-TD01 Keskin A (2014) Tokat yo¨resinde insanlar u¨zerinde parazitlenen sert Abedi V, Razmi G, Seifi H, Naghibi A (2014) Molecular and kene (Acari: Ixodidae) tu¨rlerinin sistematik yo¨nden incelenmesi serological detection of Theileria equi and Babesia caballi ve bu kenlelerde riketsiya varlıg˘ının aras¸tırılması. Doktora Tezi, infection in horses and ixodid ticks in Iran. Ticks Tick-Borne Dis Gaziosmanpas¸a U¨ niversitesi Fen Bilimleri Enstitu¨su¨ 5:239–244 Khosravi M, Kavosh F, Taghavi-Moghadam A, Ghaem-Maghani S, Aksoy AR (2016) At yetis¸tiricilig˘i ders notları. Pirali-Kheirabadi K, Rahimi-Feyli P, Navid-Pour S, Amin-Pour https://docplayer.biz.tr/22854819-At-yetistiriciligi-ders-notlari- A, Arbabi F (2012) Comparison of helminth and hard tick yrd-doc-dr-ali-riza-aksoy-1993-guncelleme-mayis-2016.html. infestation between riding and work horses in Ahwaz, Iran. Accessed 26 Mar 2020 Comp Clin Pathol 21:333–336 Bennett D, Hoffmann RS (1999) Equus caballus. Mammalian Larsen KS, Eydal M, Mencke N, Sigurdsson H (2005) Infestation of Species, (Official Publication of the American Society of Werneckiella equi on Icelandic horses, characteristics of Mammalogist) 628:1–14 predilection sites and lice dermatitis. Parasitol Res 96(6):398–401

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Laus F, Veronesi F, Passamonti F, Paggi E, Cerquetella M, Hyatt D, Rothschild CM (2013) Equine piroplasmosis. J Equine Vet Sci Tesei B, Fioretti DP (2013) Prevalence of tick borne pathogens 33:498–508 in horses from Italy. J Vet Med Sci 75(6):715–720 Scoles GA, Ueti MW (2015) Vector ecology of equine piroplasmosis. Lowden S, Gray S, Dawson K (2007) Treatment of natural Annu Rev Entomol 60:561–580 infestations of the biting louse (Werneckiella equi) on horses Shubber HWK, Al-Hassani NAW, Mohammad KM (2014) Ixodid using triflumuron a benzoylurea derivative growth regu- ticks diversity in the Middle and South of Iraq. Int J Recent Sci lator. Vet Parasitol 148(3–4):295–300 Res 5(9):518–1523 Maa TC (1963) Genera and species of Hippoboscidae (Diptera): Tirosh-Levy S, Gottlieb Y, Apanaskevich DA, Mumcuoglu KY, types, synonymy, habitats and natural groupings. Pasif Insects Steinman A (2018) Species distribution and seasonal dynamics Monogr 6:1–186 of equine tick infestation in two Mediterranean climate niches in Merdivenci A (1965) Tu¨rkiye’nin Entomolojik Cog˘rafyası. In: Unat Israel. Parasit Vectors 11:546 EK, Yas¸arol S¸, Merdivenci A (eds) Tu¨rkiye’nin Parazitolojik Uilenberg G (2006) Babesia-a historical overview. Vet Parasitol Cog˘rafyası. Ege U¨ niversitesi Tıp Faku¨ltesi Yayınları, 42nd edn 138:3–10 edn. Ege U¨ niversitesi Basımevi, I˙zmir, pp 114–154 Vial L, Stachurski F, Leblond A, Huber K, Vourc’h G, Rene- Moreby C (1978) The biting louse genus Werneckiella (Phthiraptera: Martellet M, Desjardins I, Balanca G, Grosbois V, Pradier S, Trichodectidae) ectoparasitic on the horse family Equidae Gely M, Appelgren A, Estrada-Pena A (2016) Strong evidence (Mammalia: Perissodactyla). J Nat Hist 12:395–412 for the presence of the tick Hyalomma marginatum Koch, 1844 Moreno L, Cabezas I, Ahumada J, Ortiz R, Morales A, Gonzalez- in southern continental France. Tick Tick-Borne Dis Acuna D (2011) Distribucion y abundancia de piojos (Werneck- 7:1162–1167 iella equi) y eficacia del tratamiento con trichlorphon en caballos Walker AR, Bouattour A, Camicas JL, Estrada-Pen˜a A, Horak IG, mestizos. Rev Fac Cs Vets 52(2):77–82 Latif AA, Pegram RG, Preston PM (2014) Ticks of domestic Orkun O¨ (2018) Molecular characterization based on 16S rDNA animals in Africa: a guide to tdentification of species. Bioscience phylogeny of some ixodid ticks in Turkey. Turkiye Parazitol reports, Edinbrough Derg 42:122–129 Wall R, Shearer D (2001) Veterinary ectoparasites: biology, pathol- Payne VK, Mbafor FL, Pone JW, Tchoumboue J (2017) Prelimanary ogy and control. Blackwell Science Ltd, Oxford study of ectoparasites of horses in the western highlands of Werneck FL (1936) Contribuic¸a˜o ao conhecimento dos Mallophagos Cameroon. Vet Med Sci 3:63–70 encontrados nos mammiferos sul-americanos. Mem Inst Price RD, Hellenthal RA, Palma RL, Johnson KP, Clayton DH (2003) Oswaldo Cruz 31(3):391–589 The chewing lice: world checklist and biological overview. Wright R (1999) Lice on horses. Can Vet J 40:590–591 Illinois Natural History Survey Special Publication, Champaign Ros-Garcia A, M’ghirbi Y, Hurtado A, Bouattour A (2013) Preva- Publisher’s Note Springer Nature remains neutral with regard to lence and genetic diversity of piroplasm species in horses and jurisdictional claims in published maps and institutional affiliations. ticks from Tunisia. Infect Genet Evol 17:33–37

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