J Arthropod-Borne Dis, June 2014, 8(1): 108–116 A Sofizadeh et al.: Hard Tick Species of … 108 Short Communication Hard Tick Species of Livestock and their Bioecology in Golestan Province, North of Iran Aioub Sofizadeh 1, *Zakkyeh Telmadarraiy 2, Abbas Rahnama 1, Ahmad Gorganli-Davaji 1, Asadollah Hosseini-Chegeni 3 1Infectious Diseases Research Center, Golestan University of Medical Sciences, Gorgan, Iran 2Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 3Department of Plant Protection, Faculty of Agriculture, Guilan University, Rasht, Iran (Received 13 Nov 2011; accepted 3 Sep 2013) Abstract Background: A survey on tick species composition was carried out in Golestan Province Iran during year 2010– 2011.The aim was to determine tick species parasitizing domestic ruminants and their seasonal population dynamics. Methods: A total of 124 sheep, 92 goats, 84 cattle, 74 camels and 12 horses in several villages were inspected for tick infestation. The collected ticks preserved in 70% alcohol and then were identified. Results: The overall 1059 ticks (453 female, 606 male) were collected. The ticks occur on sheep, goats, cattle, cam- els and horses as 72.1%, 77.3%, 75.8%, 69.3%, and 50% respectively. The frequency of ticks in spring was more than other seasons and the least was observed in winter. In the spring and summer, infestation rate in domestic rumi- nants were calculated as 100%. Six genus and fourteen hard and soft tick species were identified including Rhipicephalus sanguineus, R. bursa, Ixodes ricinus, Haemaphysalis punctata, H. sulcata, H. erinacei, H. inermis, Hyalomma marginatum, Hy. asiaticum, Hy. dromedarii, Hy. excavatum, Hy. anatolicum, Hy. detritum, Boophilus annulatus and Argas persicus. Rhipicephalus sanguineus was the most abundant species in the study area. The larg- est number of ticks was collected from animal ears and tails. Haemaphysalis, Hyalomma, Rhipicephalus and Boophilus occurred in mountainous, forest and plateau areas of Golestan Province but Ixodes occurred only in mountainous and forest areas, whereas Rhipicephalus and Hyalomma were present in coastal areas of Golestan Province. Conclusion: The result of this study is a survey on tick species from domestic animals in Iran and implication of possible prevention measures for diseases transmitted by ticks. Keywords: Ticks, Domestic ruminants, Bioecology, Iran Introduction Medical and veterinary implications of ticks (Acari: Ixodidae) on human and animals life is very obvious question and proved from many years ago (Hoogstraal 1982). Annoy- ance and paralysis of livestock also trans- mission large number of pathogen agents is only some cosmopolitan associated tick prob- lems (Sonenshine 1991, Service 2001). Ap- proximately only 10% of the currently known 867 tick species are also responsible for dam- age directly due to their feeding behavior (Oliver 1989) and unavoidability act as vec- tors of a broad range of pathogens of those hosts. Ruminants are also affected by direct tick damage including tick bite abscesses, anemia, tick induced dermatophilosis. The pioneer work on tick fauna was Delpy L in Iran (Delpy 1936). Later continue by GS Pervomaisky, H Nemenz (Pervomaisky 1948, Nemenz 1953). Subsequently R Abbasian- Lintzen, Z Mazlum, G Maghami and A Rafyi et al. conducted some studies generally on do- *Corresponding author: Dr Zakkyeh Telmadarraiy, E-mail: ztelma@yahoo.co.in http://jad.tums.ac.ir Published Online: December 18, 2013 J Arthropod-Borne Dis, June 2014, 8(1): 108–116 A Sofizadeh et al.: Hard Tick Species of … 109 mestic animals ticks in Iran (Abbasian-Lintzen 1960, Maghami 1968, Mazlum 1971). How- ever certain studies also has been carried out on the ticks of wild animals by NA Filippova et al former presented data for 642 ixodid ticks taken from small-sized mammals main- ly rodents in different zoogeographical zones of Iran and the latter studied ixodid ticks parasitizing wild sheep and goats in Iran fo- cusing on maintaining natural foci of many hazardous diseases for human (Filippova et al. 1976). Recently Nabian et al and Rahbari et al published a list of adult ticks collected from domestic animals in North and whole Iran (Nabian et al. 2007, Rahbari et al. 2007a). Telmadarraiy et al. published a list of tick spe- cies and their prevalence in the Northwest and the Western part of Iran (Telmadarraiy et al. 2004, Telmadarraiy et al. 2008a, Telmadarraiy et al. 2010). Furthermore there are several reports on epidemiology, distri- bution, medically importance and acaricide susceptibility of different tick species through in this country (Telmadarraiy et al. 2007b, Vatandoost et al. 2010a). Since thus far only few studies were accomplished on tick fauna in different areas of Iran, it seems to be a gap in our knowledge about distribution of tick species in the Iran. In addition there is lack of finding about the frequency of ixodid tick species from domestic ruminants in Golestan Province. Therefore, this study is aimed to figure out the frequency of ticks on domestic ruminants likewise their seasonal and topo- logical abundance and their host in the afore- mentioned part of Iran. Materials and Methods Study area The present study carried out in different zone of Golestan Province which is located in Northeastern of Iran and geographically located at 36°25´N and 53°51´E on the South- eastern coast of Caspian Sea, a region suita- ble for agriculture and animal husbandry. This province geographically divided into three parts: covered forest mountainous parts and plateau areas as well as the coastal plains. Ticks Tick sampling was carried out on all three part of the study area at different time inter- vals. A total of 124 sheep, 92 goats, 84 cat- tle, 74 camels and 12 horses in several vil- lages in Golestan Province were examined for tick infestation on the whole body of each animal. The sites of tick attachment were recorded during collection, collected ticks were preserved in 70% alcohol, count- ed and tick identification done by using the suitable and comprehensive keys including Pomerantzev (1950) and Hoogstraal (1956) (Pomerantzev 1950, Hoogstraal 1956). Results During the study period among several villages the total number of 1009 ticks were collected and identified, the occurrence of ticks on sheep, goats, cattle, camels and horses were 72.1%, 77.3%, 75.8%, 69.3%, 50% respectively. Table 1 show the number of hard tick species in whole study area. The frequency of ticks in spring was more than other sea- sons and the least was observed in winter. In the spring and summer infestation rate of do- mestic ruminants was higher than 90% and in autumn and winter was lower than 25%. The mean number of ticks on each animal was high in spring and summer (40–50 ticks per animal) and was low in autumn and winter (3–5 ticks per animal), so the largest number of ticks were collected from animal ears and tails. Fifteen species of ticks were identified based on the morphological characteristics which comprise Rhipicephalus sanguineus, R. bursa, Ixodes ricinus, Haemaphysalis punctata, H. sulcata, H. erinacei, H. inermis, Hyalomma marginatum, Hy. asiaticum, Hy. excavatum, http://jad.tums.ac.ir Published Online: December 18, 2013 J Arthropod-Borne Dis, June 2014, 8(1): 108–116 A Sofizadeh et al.: Hard Tick Species of … 110 Hy. anatolicum, Hy. dromedarii, Hy. detritum, B. anulatus and Argas persicus was collect- ed in nests of hen and domestic ruminants. Out of 1059 collected ticks from animal, a significant number of 593 R. sanguineus were identified. This species stands out as being the most prevalent tick species comprising 56% of the all ticks collected from domestic ruminants in Golestan Province. The tick spe- cies prevalence is shown in Table 1. Latter spe- cies was the most abundant tick in both moun- tainous areas and the coastal plains, as well as Hy. anatolicum in the plateau areas. Whereas I. ricinus, R. bursa, B. annulatus and H. inermis occurred in mountainous areas and Hy. dromedarii, Hy. asiaticum, Hy. excavatum and Hy. detritum occurred in plateau areas only. The species diversity of hard ticks in plateau areas was more than other areas (Fig. 1). The tick species diversity on sheep is highest from the other hosts (Table 2). Table 1. Seasonal abundance of hard ticks in Golestan Province Species number (percent) Season Spring Summer Autumn Winter Total ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂ Hy. anatolicum 148(14/7) 0 35 33 24 0 56 0 0 33 115 Hy. asiaticum 2(0/2) 0 2 0 0 0 0 0 0 0 2 Hy. detritum 2(0/2) 0 0 0 2 0 0 0 0 0 2 Hy. dromedarii 64(6/3) 26 24 0 11 0 1 1 1 27 37 Hy. excavatum 4(0/4) 0 2 0 0 0 2 0 0 0 4 Hy. marginatum 64(6/3) 8 21 2 27 0 6 0 0 10 54 H. erinacei 4(0/4) 0 0 0 0 3 0 1 0 4 0 H. inermis 24(2/4) 0 0 0 0 22 2 0 0 22 2 H. punctata 66(6/5) 0 0 0 0 52 11 0 3 52 14 H. sulcata 3(0/3) 0 0 0 0 1 0 1 1 2 1 I. ricinus 13(1/3) 6 0 1 0 6 0 0 0 13 0 R. (B.) annulatus 4(0/4) 0 0 0 0 4 0 0 0 4 0 R. bursa 18(1/8) 0 0 10 8 0 0 0 0 10 8 R. sanguineus 593(58/8) 163 250 88 92 0 0 0 0 251 342 Total 1009(100) 203 334 134 164 88 78 3 5 428 581 Fig. 1. Topological preference of hard ticks collected in Golestan Province (the number of specimens presented between two parenthesis) http://jad.tums.ac.ir Published Online: December 18, 2013 J Arthropod-Borne Dis, June 2014, 8(1): 108–116 A Sofizadeh et al.: Hard Tick Species of … 111 Table 2. The host diversity of hard tick species in Golestan Province Species number (percent) Host Cattle Sheep Goat Camel Horse Hy. anatolicum 108 0 0 25 15 Hy. asiaticum 1 0 0 1 0 Hy. detritum 0 0 0 2 0 Hy. dromedarii 0 0 0 64 0 Hy. excavatum 4 0 0 0 0 Hy. marginatum 40 0 0 13 11 H. erinacei 3 1 0 0 0 H. inermis 24 0 0 0 0 H. punctata 63 3 0 0 0 H. sulcata 1 2 0 0 0 I. ricinus 7 0 6 0 0 R. (B.) annulatus 4 0 0 0 0 R. bursa 10 5 0 0 3 R. sanguineus 15 359 202 4 13 Total 280 370 208 109 42 Discussion In the present study 206 (53.3%) out of 386 livestock was infested with tick. The number of ticks was high in spring and summer (40–50 tick per animal) but low in autumn and winter (3–5 tick per animal, av- erage 21.5–25). Hosseini vasoukolaei et al. (2010) in Ghaemshahr recorded that tick in- festation rate of animal and the number of ticks per animal was 24% and 3–5 respec- tively (Hosseini vasoukolaei et al. 2010). In the study conducted by Rahbari et al. (2007) in four different zoogeographical areas in Iran where the majority of the domestic ru- minants in Iran exist the number of ticks per animal (10–20) was low (Rahbari et al. 2007a). In respect of this result to result of the pre- sent investigation tick infestation rate of an- imals was high in our studied area. Through viewpoint of tick infestation of livestock the percentage of tick per sheep, goat, cattle, camel and horse were equal 45.1%, 47.8%, 64.2%, 62.1%, and 50.0% respectively. Tick infestation of cattle, sheep and goat in the study of Rahbari et al. (2007) was equal 62%, 55% and 57% respectively (Rahbari et al. 2007a). In the other study carry out by Davoudi et al. (2008) in Northwestern parts of Iran 10.16% of cattle and 1.07% of buffaloes were infested by ticks. Thus tick infestation of an- imals in our studied areas than Ghaemshahr and Northwestern parts of Iran was higher but coincided with the result of Rahbari et al. (2007). These results reveal significant dif- ferences concerning tick abundance on dif- ferent hosts in different geographical areas. In a survey conducted from April 2001 to January 2003 in Tamil Nadu of India from 600 sheep and goat was selected randomly 64.6% sheep and 97.66% goat were infested by ticks (Vathsala et al. 2008) and therefore tick infestation rate of animals in Indian study is higher from tick infestation rate of animals in our country. We observed that in- festation rate may be maximized in the spring and summer seasons. This result is in agreement with study of Davoudi et al. (2008) he also sees the highest rate of infestation occur in spring (Davoudi et al. 2008). How- ever Telmadarraiy et al. (2004) and Salari Lak et al. (2008) in the Northwestern Iran most of tick collected in the summer and spring respectively (Telmadarraiy et al. 2004, Salari http://jad.tums.ac.ir Published Online: December 18, 2013 J Arthropod-Borne Dis, June 2014, 8(1): 108–116 A Sofizadeh et al.: Hard Tick Species of … 112 Lak et al. 2008). It may be as a result of that climate condition and flora of Northwestern Iran in summer is similar to climate condition of our studied area in spring. In the studies conducted in Iran and also in our study, the lowest number of ticks were collected during winter, whereas interestingly in Tamil Nadu of India seasonal tick infestation rate of sheep and goat in winter (January to March) was 61% and 97.66% respectively (Vathsala et al. 2008). This could be due to Indian cli- mate conditions in winter agree with climate condition of Northwestern Iran in same sea- son. In the present study, the ticks were obtained in more number from animal ears and tails. The possible factors effect question include temperature and humidity of skin also delicateness of it that cause tick attached and engorged on this sites. Whereas in win- ter which is colder than other seasons ticks attached the trunk between wool’s host which is warmer than ears and tail thus become their preference site in the winter season. In our study, five genera of ixodid ticks in- cluding Rhipicephalus (60.5%), Hyalomma (27.1%), Haemaphysalis (10.6%), Ixodes (1.3%), and Boophilus (0.4%) were collected and Rhipicephalus ticks were dominant in the investigated area. In a survey on ticks collected from sheep, in Bahar township of Hamadan Province in the Western part of Iran, the ixodid ticks found were Hyalomma, Rhipicephalus and Haemaphysalis and Hyalomma ticks were predominant ticks (Telmadarraiy et al. 2008a). The frequency of Hyalomma and Rhipicephalus species in a study conducted in Ardabil Province located in the Northwest of Iran, comprising 43.6% and 41.7% of all collected ticks respectively (Telmadarraiy et al. 2010). In the studies performed in West Azerbaijan Province Hyalomma ticks were dominant as 63.2% and 61.3% respectively (Davoudi et al. 2008, Salari Lak et al. 2008). In the other study in West Azerbijan Rhipicephalus (42%), Hyalomma (41%), Boophilus (7%), Dermacentor (7%), and Haemaphysalis (3%) were found where Rhipicephalus as well as Hyalomma were the most prevalent tick species (Telmadarraiy et al. 2004). Thus could not be understand that in the most aforesaid studies Hyalomma ticks were the most abundant ticks, but the largest number of ticks that in Northwest of Iran were found belonging Rhipicephalus genus and the most abundant species in the study area was Rhipicephalus sanguineus which is in agree- ment with study of Hosseini vasoukolaei et al. (2010). Along with our findings, Nabian et al. (2007) found that R. sanguineus is the major species in Mazandaran Province and did not find R. bursa (Nabian et al. 2007), but result of our study show eight male and ten female R. bursa in contrast with only one female R. bursa (Hosseini vasoukolaei et al. 2010). In the study conducted by Rahbari et al. (2007) R. sanguineus was the main spe- cies in the North of Iran (Rahbari et al. 2007a). From the studies accomplished by Telmadarriy et al. (2004, 2008) and Davoudi et al. (2008) two species R sanguineus and R bursa were collected from different animals including sheep, goats, cattle, buffaloes and camels (Telmadarraiy et al. 2004, Telmadarraiy et al. 2008a), showing Rhipicephalus are con- cerned to blood of different hosts. According to these studies, it can be concluded that R. sanguineus is the tick species with great sig- nificance for domestic ruminants in the North of Iran. Razmi et al. (2007) found that Boophilus comprising the majority (51.3%) of ticks collected in a study conducted in Mazan- daran Province following Hyalomma (18.5 %), Rhipicephalus (16.8%), Haemaphysalis (6.3%), Ixodes (6.3%) and Dermacentor (0.1%) were also present in the study area (Razmi et al. 2007), but in our study Boophilus collected with low frequency and never we collected Dermacentor species. The ticks of the genus Ixodes are the important vectors of Lyme borreliosis in Europe and America commonly collected in Iran with species I. http://jad.tums.ac.ir Published Online: December 18, 2013 J Arthropod-Borne Dis, June 2014, 8(1): 108–116 A Sofizadeh et al.: Hard Tick Species of … 113 ricinus only in the Caspian Sea littoral area (Nabian et al. 2007 Rahbari et al. 2007a, Razmi et al. 2007). In our study Ixodes tick were found with low frequency (1.3%). The most common ixodid tick vector of Human Granulocytic Ehrlichiosis (HGE) in Europe is I. ricinus (Rymaszewska and Grenda 2008). In a study by Bashiribod et al. (2004) in Ghaemshahr, 5.1% of all I ricinus ticks ex- amined by molecular methods was shown to be infected with Anaplasma phagocotophilum (Bashiribod et al. 2004). In a study by Hosseini Vasoukolaei et al. (2010) 49 out of 323 collected ticks were identified as I ricinus, which is an important vector of tick- borne disease aforesaid and may be consid- ered in the study area, need for further in- vestigation (Hosseini vasoukolaei et al. 2010). In the study undertaken by Nabian et al. (2007) genus Ixodes was found with fre- quency 2.32% (Nabian et al. 2007). Several Haemaphysalis species were found in Iran. In the present study, H. erinacei, H. sulcata, H. punctata and H. inermis were collected from farm animals, in spite of only H. erinacei was reported in study of Hosseini Vasoukolaei et al. (2010) from North of Iran (Hosseini vasoukolaei et al. 2010). Rahbari et al. (2007) in a study completed in three geographical zone of Iran reported 6 species H. punctata (3.4%), H. parva (0.5%), H. sulcata (0.6%), H. choldokovskyi (1.7%) (now synonymized as H. sulcata), H. concinna (0.06%) and Haemaphysalis sp. (0.6%) but never reported H. erinacei and H. inermis (Rahbari et al. 2007b). Interestingly the lat- ter species recorded by Telmadarraiy (2008) in South of Sari in Mazandaran Province (Telmadarraiy et al. 2008b). In respect of much Haemaphysalis are three host ticks thus they may be serve as competent vectors of different domestic ruminant thereupon human diseases. In the present work several Hyalomma including Hy. dromedarii, Hy. marginatum, Hy. asiaticum, Hy. excavatum, Hy. anatolicum, Hy. detritum were collected at least in all studied geographical areas. Whereas in a series studies conducted by one of authors (ZT) from year 2004 to year 2010 in Yazd, Ilam, East and West Azerbaijan, Ar- dabil, Hamadan, Khorasan Jonoobi Provinces as well as South of Sari in Mazandaran Prov- ince (Telmadarraiy et al. 2004, Telmadarraiy et al. 2006, Telmadarraiy et al. 2008a, Telmadarraiy et al. 2008b, Nasiri et al. 2010, Salim abadi et al. 2010, Telmadarraiy et al. 2010) various Hyalomma species were rec- ognized like present study. Also author with cooperation other (2007, 2009, 2010) studied ectoparasite of rodents including ticks as well as lesser mouse eared bat, Myotis blyti ( Telmadarraiy et al. 2007a, Kia et al. 2009, Vatandoost et al. 2010b). It is necessary in- dicate which Hyalomma species has critical role for transmission of Crimean Congo Hem- orrhagic Fever. With respect to which is three geographic continents including moun- tainous, littoral and plateau possess Golestan Province species diversity and the number of species found in mountainous, littoral and plateau area comprising 6, 2 and 10 species respectively. Otherwise following ticks gen- era and species collected respect to three aforesaid situation constitute R. sanguineus (69%) in mountainous and (93.5%) in littoral area which is more incident from other species. Beside Hy. anatolicum (47.9%) and Hy. dromedarii (29%) in plateau area were dominant species. Whereas in a study con- ducted in plateau area of Yazd Province Hy. dromedarii was more prevalent species (55.92 %) while D. marginatus, Hy. marginatum and Hy. anatolicum ticks were collected with very slightly frequency (Salim abadi et al. 2010). In another study directed in Esfahan Province R. sanguinus in mountainous and Hy. anatolicum in plateau areas were the most abundant ticks respectively (Noaman et al. 2008). It may be concluded that genera of Rhipicephalus and Hyalomma are as princi- pal genera in mountainous and plateau area respectively. In the present study most of http://jad.tums.ac.ir Published Online: December 18, 2013 J Arthropod-Borne Dis, June 2014, 8(1): 108–116 A Sofizadeh et al.: Hard Tick Species of … 114 tick species were collected from cattle, only Hy. dromedarii and Hy. detritum were found on camel. In addition Hy. anatolicum was predominant Hyalomma species obtained from cattle and the other tick genera and species including H. sulcata, H. erinacei (Haemaphysalis), Hy. asiaticum, Hy. exca- vatum (Hyalomma) and Boophilus (Rhipi- cephalus) annulatus only with low fre- quency collected from cattle host. Likewise the most number of species collected from two hosts camel and horse including Hy. dromedarii and Hy. anatolicum respectively. Acknowledgements This study was supported by the infec- tious diseases research center of Golestan University of Medical Sciences. References Abbasian-Lintzen R (1960) A preliminary list of ticks (Acarina: Ixodidae) occur- ring in Iran and their distributional data. Acarologia 2: 43–61. Bashiribod H, Kazemi B, Eslami G, Bigdeli S, Bandehpour M, Rahbarian N, Rame- zani Z (2004) First molecular detection of Anaplasma phagocytophilum in Ixodes ricinus ticks in Iran. J Med Sci. 4: 282–286. Davoudi J, Hoghooghi Rad N, Golzar Adabi S (2008) Ixodid tick species infesting cows and buffaloes and their seasonal- ity in West Azerbaijan. Res J Parasitol. 3: 98–103. Delpy LP (1936) Notes sur les Ixodidés du genre Hyalomma (Koch). Ann Para- sitol Hum Comp. 14: 206–245. Filippova NA, Neronov VM, Farhang-Azad A (1976) Data on ixodid tick fauna (Acarina, Ixodidae) of small mammals in Iran. Ent Obozr. 55: 467–479. Hoogstraal H (1956) African Ixodoidea. I. Ticks of the Sudan (with special refer- ence to Equatoria Province and with pre- liminary reviews of the genera Boo- philus, Margaropus and Hyalomma. United State Navy, Washington DC. Hoogstraal H (1982) Bibliography of Ticks and Tick Borne Diseases from Homer (about 800 BC) to 31 December 1981. Special publication NAMRU-3 Medi- cal Zoology Department, Cairo. Hosseini vasoukolaei N, Telmadarraiy Z, Vatandoost H, Yaghoobi Ershadi MR, Hosseini Vasoukolaei M, Oshaghi MA (2010) Survey of tick species para- siting domestic ruminants in Ghaem- shahr country, Mazandaran Province, Iran. Asian pac J Trop Med. 3: 804–806. Kia EB, Moghddas-Sani H, Hassanpoor H, Vatandoost H, Zahabiun F, Akhavan AA, Hanafi-Bojd AA, Telmadarraiy Z (2009) Ectoparasites of rodents cap- tured in Bandar Abbas, Southern Iran. Iran J Arthropod-Borne Dis. 3: 44–49. Maghami G (1968) External parasites of livestocks in Iran. Arch Inst Razi Hes. 20: 81–83. Mazlum Z (1971) Ticks of domestic animals in Iran: geographic distribution, host relation, and seasonal activity. J Vet Fac Univ The. 27: 1–32 [In persian]. Nabian S, Rahbari S, Shayan P, Haddad- zadeh HR (2007) Current status of tick fauna in North of Iran. Iran J Parasitol. 2: 12–17. Nasiri A, Telmadarraiy Z, Vatandoost H, Chinicar S, Moradi M, Oshaghi MA, Salimabadi Y, Sheikh Z (2010) Tick infestation rate of sheep and their dis- tribution in Abdanan county, Ilam Prov- ince, Iran, 2007–2008. Iran J Arthro- pod-Borne Dis. 4: 56–60. Nemenz H (1953) Ergebnisse der österrei- chischen Iran-expedition 1949/1950 Ixodidae. S B Ost Acad Wiss Abt. 162: 61–63. http://jad.tums.ac.ir Published Online: December 18, 2013 J Arthropod-Borne Dis, June 2014, 8(1): 108–116 A Sofizadeh et al.: Hard Tick Species of … 115 Noaman V, Abdigoudarzi M, Nabinejad AR, Heidari MR, Khalilifard M (2008) Identification of hard ticks of domestic ruminants in two ecological zones of Isfahan Province, Iran. Pajou and Sazan. 77: 88–95 [In Persian]. Oliver JJ (1989) Biology and systematics of ticks (Acari: Ixodidae). Ann Rev Ecol Sys. 20: 397–430. Pervomaisky GS (1948) On the Ixodidae of Iran fauna. Trud Voenno Med Akad Krasnoi Armii. 44: 35–40. Pomerantzev BI (1950) Fauna of USSR Arachnida: Ixodid Ticks (Ixodidae). Academy of Sciences USSR, Moscow. Rahbari S, Nabian S, Shayan P (2007a) Pri- mary report on distribution of tick fauna in Iran. Parasitol Res. 2(101 Suppl): S175–177. Rahbari S, Nabian S, Shayan P, Haddadzadeh HR (2007b) Status of Haemaphysalis tick infestation in domestic ruminants in Iran. Korean J Parasitol. 45: 129–32. Razmi GR, Glinsharifodini M, Sarvi S (2007) Prevalence of ixodid ticks on cattle in Mazandaran Province, Iran. Korean J Parasitol. 45: 307–310. Rymaszewska A, Grenda S (2008) Bacteria of the genus Anaplasma-characteristics of Anaplasma and their vectors: a review. Vet Med. 11: 573–584. Salari Lak S, Vatandoost H, Telmadarraiy Z, Entezar Mahdi R, Kia EB (2008) Sea- sonal activity of ticks and their im- portance in tick-borne infectious dis- eases in West Azerbaijan, Iran. Iran J Arthropod-Borne Dis. 2: 28–34. Salim abadi Y, Telmadarraiy Z, Vatandoost H, Chinikar S, Oshaghi MA, Moradi M, Mirabzadeh Ardakan E, Hekmat S, Nasiri A (2010) Hard ticks on domes- tic ruminants and their seasonal pop- ulation dynamics in Yazd Province, Iran. Iran J Arthropod-Borne Dis. 4: 66–71. Service MW (2001) Encyclopedia of Arthro- pod-Transmitted Infections of Man and Domesticated Animals. CABI Publish- ing, New York. Sonenshine DE (1991) Biology of Ticks. Oxford University press, Oxford. Telmadarraiy Z, Bahrami A, Vatandoost H (2004) A Survey on fauna of ticks in west Azerbaijan Province, Iran. Iran J Public Health. 4: 65–69. Telmadarraiy Z, Davari A, Vatandoost H (2006) Ruminant animal ticks an their role in CCHF transmission in Ghaen , south Khorasan Province, Iran during 2005. ICOPA XI11th International Congress of Parasito …, 6–11 August 2006 Gelascoo Telmadarraiy Z, Moradi AR, Vatandoost H, Mostafavi E, Oshaghi MA, Zahirnia AH, Haeri A, Chinikar S (2008a) Crimean- Congo hemorrhagic fever: a seroepide- miological and molecular survey in Bahar, Hamadan Province of Iran. Asian J Ani Vet Adv. 3: 321–327. Telmadarraiy Z, Ghiasi SM., Moradi M, Vatandoost H, Eshraghian MR, Faghihi F, Zarei Z, Haeri A, Chinikar S (2010) A survey of Crimean-Congo haemor- rhagic fever in livestock and ticks in Ardabil Province, Iran during 2004– 2005. Scand J Infect Dis. 42: 137–141. Telmadarraiy Z, Vatandoost H, Mohammadi S, Akhavan AA, Abai MR, Rafinejad J, Kia EB, Naini FF, Jedari M, Aboul- hasani M (2007a) Determination of rodent ectoparasite fauna in Sarpole- Zahab district, Kermanshah Province, Iran, 2004–2005. Iran Journal of Ar- thropod-borne Dis. 1: 58–62. Telmadarraiy Z, Nasirian H, Vatandoost H, Abuolhassani M, Tavakoli M, Zarei Z, Banafshi O, Rafinejad J, Salarielac S, Faghihi F (2007b) Comparative suscep- tibility of cypermethrin in Ornithodoros lahorensis Neuman and Argas persicus Oken (Acari: Argasidae) field popula- tions. Pak J Biol Sci. 10: 4315–4318. http://jad.tums.ac.ir Published Online: December 18, 2013 J Arthropod-Borne Dis, June 2014, 8(1): 108–116 A Sofizadeh et al.: Hard Tick Species of … 116 Telmadarraiy Z, Chinikar S, Shakeri MA, Vatandoost H, Faghihi F, Faghihi F, Moradi N, Ranjbar E, Motiei M, Hosseine Vasoukolaei N, Aboulhasani M (2008b) Crimean-Congo hemorrhagic fever: A seroepidemiological and mo- lecular survey in Poshete-kooh of Sari, Mazandaran Province Iran. Tropical Medicine and Malaria. International Con- vention Center Jeju, Jeju Island, Korea. 29th September -03 October 2009 Vatandoost H, Telmadarraiy Z, Sharifi M, Moradi A, Kamali M, Taran M (2010a) Ectoparasites of lessr mouse bat, Myotis blyti from Kermanshah, Iran. Asian Pac J Trop Med. 3: 371–373. Vatandoost H, Telmadarraiy Z, Sharifi M, Moradi A, Kamali M, Taran M (2010b) Ectoparasites of lessr mouse bat, Myotis blyti from Kermanshah, Iran. Asian Pac J Trop Med. 3: 371–373. Vathsala M, Mohan P, Sacikumar, Ramessh S (2008) Survey of tick species dis- tribution in sheep and goat in Tamil Nadu, India. Small Rumin Res. 74: 238–242. http://jad.tums.ac.ir Published Online: December 18, 2013