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Ectoparasites of Feral Horses [Equus Ferus Caballus (Linnaeus., 1758)] on Karadag˘ Mountain, Karaman, Turkey

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Ectoparasites of Feral Horses [Equus Ferus Caballus (Linnaeus., 1758)] on Karadag˘ Mountain, Karaman, Turkey J Parasit Dis https://doi.org/10.1007/s12639-020-01234-4 ORIGINAL ARTICLE Ectoparasites of feral horses [Equus 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 Hippobosca equina Á Haemaphysalis parva near Karaman City were caught by Kazakh horse 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), Hippobosca equina 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 cattle 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 arthropods 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, genus 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. 123 J Parasit Dis 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).
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