J Arthropod-Borne Dis, June 2021, 15(2): 187–195 K Arzamani et al.: Biodiversity Indices and … 187 http://jad.tums.ac.ir Published Online: June 30, 2021 Original Article Biodiversity Indices and Medically Importance of Ticks in North Khorasan Province, Northeast of Iran Kourosh Arzamani1; *Abedin Saghafipour2; Seyed Ahmad Hashemi1; Hassan Vatandoost3; Mohammad Alavinia1,4; Saber Raeghi5; Zakkyeh Telmadarraiy3 1Vector-borne Diseases Research Center, North Khorasan University of Medical Sciences, Bojnurd, Iran 2Department of Public Health, Faculty of Health, Qom University of Medical Sciences, Qom, Iran 3Department of Medical Entomology and Vector Control School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 4Toronto Rehabilitation Centre, University Health Network, Toronto, Canada 5Department of Laboratory Sciences, Maragheh University of Medical Sciences, Maragheh, Iran *Corresponding author: Dr Abedin Saghafipour, E-mail: abed.saghafi@yahoo.com (Received 31 Dec 2019; accepted 26 Apr 2021) Abstract Background: Ticks are considered as the main vectors for the transmission of various pathogens such as relapsing fever and CCHF to humans. This study was investigated the biodiversity indices and medically importance of ticks in North Khorasan Province, Northeast of Iran during 2015–2019. Methods: Specimens were captured from infested ruminants including cows, sheep, and goats. Additionally, tick col- lections also were performed on non-domesticated creatures such as turtles, rodents, and hedgehogs. Specimens were identified using valid identification keys. Species diversity, species richness and evenness indices have been calculated to estimate species biodiversity of ticks. Results: A total of 1478 adult ticks were collected. The specimens were from two families: Ixodidae (90.05%) and Ar- gasidae (9.95%), 6 genera and 17 species including: Rhipicephalus sanguineus (55.9%), Rhipicephalus bursa (13.4%), Hyalomma marginatum (9.5%), Hyalomma anatolicum (9.5%), Hyalomma asiaticum (0.2%), Hyalomma aegyptium (0.5%), Hyalomma scupense (1.3%), Hyalomma sp (1.2%), Haemaphysalis sulcata (0.7%), Haemaphysalis erinacea (0.1%), Haemaphysalis inermis (0.1%), Haemaphysalis punctata (0.2%), Haemaphysalis concinna (0.1% Boophilus annulatus (1.2), and Dermacentor marginatus (6.1%) among hard ticks as well as Argas persicus (91.8%) and Argas reflexus (8.2%) amongst soft ticks. Rhipicephalus sanguineus, Rh. Bursa, Hy. marginatum and Hy. anatolicum were known as the most frequent species of hard ticks. Tick’s species richness, Shannon diversity index and Simpson index in this area were S= 17, H’= 1.69, D= 0.294 respectively. Conclusion: Based on tick distribution veterinary authority, public health organizations and other officials should act for implementation of disease prevention. Keywords: Tick infestations; Ruminant; Geographic information system; Ixodidae; Argasidae Introduction There are two major tick (Arthropoda: Arach- nida) families: Argasidae and Ixodidae. In these families, some genera and species are able to transmit some important pathogens to humans and livestock. The adult ticks live for some years. In the absence of host, they can survive and may endure hunger for several years. Both male and female ticks are blood sucking and paly as vector of diseases. Some of tick species are able to transmit these agents to the next generation (1). Ticks are blood-sucking ecto- parasites of vertebrates, especially wild animals. After a tick bite, people may develop any of flu-like symptoms including fever, weakness, pain and swelling (2). The ticks transmit sev- eral bacterial, protozoal, rickaettsial, spirochae- tal, and viral diseases of humans such as Q fe- ver (Coxiella burnetii), tick-borne relapsing fever Copyright © 2021 The Authors. Published by Tehran University of Medical Sciences. This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International license (https://creativecommons.org/licenses/by- nc/4.0/). Non-commercial uses of the work are permitted, provided the original work is properly cited. http://jad.tums.ac.ir/ mailto:abed.saghafi@yahoo.com https://www.cdc.gov/relapsing-fever/index.html https://creativecommons.org/licenses/by-nc/4.0/ https://creativecommons.org/licenses/by-nc/4.0/ J Arthropod-Borne Dis, June 2021, 15(2): 187–195 K Arzamani et al.: Biodiversity Indices and … 188 http://jad.tums.ac.ir Published Online: June 30, 2021 (Borrelia), rocky mountain spotted fever (rick- ettsia), Tularemia (pasteurella), Crimean-Con- go Hemorrhagic Fever (CCHF) and so on (3). In addition, ticks are able to transmit veteri- nary pathogens related to babesiosis, theilerio- sis, Ehrlichiosis and Anaplasmosis in rumi- nants (4). Although, ticks were not known and familiar to humans for a very long times but their importance in terms of problems in live- stock were began from the mid-nineteenth cen- tury (5). Currently, there are 896 species of ticks all over the World (6). According to many studies have been performed on fauna of med- ical important ticks, they are distributed vastly in all regions of the world (7-10). A study on ectoparasites of sheep and goats in the eastern part of the Amhara region, northeast Ethiopia revealed that there are 5 species of ticks in- cluding Boophilus decoloratus, Amblyomma var- iegatum, Amblyomma gemma, Rh. pulchellus, Rh. evertsi on body of sheep and goats. Also, four genera and six species of ticks’ species and treatment of cows, sheep and goats in the Si- vas-Zara region, in Turkey were reported (11- 12). Previously, many studies on the distribu- tion of tick fauna in Iran have been done (13- 19). Asadollahi et al. (2014) have reported the presence of eight tick species in four different genera and they were identified as Hyalomma anatolicum (39%), Rhipicephalus sanguineus (25.4%), Hy. excavatum (14.3%), Hy. asiati- cum (6.8%), Haemaphysalis sulcata (3.7%), Hy. scupense (3.4%), Hyalomma spp. (3.4%), Rh. anuulatus (2%) and Hy. dromedarii (2%) in Khouzestan Province, South-west of Iran (20). Ramezani et al. (2014) carried out a study in Meshkinshahr County, Ardabil Province, and reported nine species of ticks including Der- macentor marginatus, D. niveus, Haem. erina- cei, Haem. punctata, Hy. anatolicum, Hy. asi- aticum, Hy. marginatum, Rh. bursa and Rh. sanguineus. Also, Ganjali et al. (2014) report- ed different species of Ixodidae (hard ticks) from sheep, goats, cattle and camels in Zabol County, the Eastern area of Iran that they were included Hy. dromedarii (17.3%), Hy. schul- zei (1.8%), Hy. marginatum (0.5%), Hy. exca- vatum (12.60%), Hy. anatolicum (11.2%), Hy. asiaticum (11.0%), Rh. sanguineus (21.2%), Rh. bursa (10.2%) and Rh. turacunis (13.911%) (21-22). The Iranian Center for Disease Control and Prevention (CDC) reported some cases of CCHF infestation in ticks that collected from endemic areas of disease in Iran such as the North Khorasan Province (23). Annually, most cases of CCHF in Sistan and Baluchestan, Is- fahan, Fars, Tehran, Khorasan, and Khuzestan are reported in Iran (24). The most recent data indicate a total of 870 confirmed cases of CCHF in Iran, with 126 deaths from 2000 to 2012 (25). North Khorasan Province is one of the transit sites of domestic animals from the eastern borders (Afghanistan and Pakistan) in- to the Country. Furthermore, ticks are able to transmit different infectious agents to humans and animals, therefore identification of ticks and geographical distribution of them are es- sential to evaluate epidemiology and risks of human and animal tick-borne diseases. This study was carried out to investigate the bio- diversity indices and medically importance of ticks in North Khorasan Province, Northeast of Iran during 2015–2019. Materials and Methods Study area This cross-sectional study was conducted in North Khorasan Province, northeast of Iran, between 36°37′-38°17′ N latitudes and 55°53′- 58°20′ E longitudes with an area of more than 28,434km2. The province is bordered by Turk- menistan in the North (Fig. 1). According to the 2011 census in Iran, it includes eight cities with a population of more than 867,000 in- habitants. The province has desert and moun- tainous areas and receives about 250mm of rainfall annually. Ticks collection In this cross-sectional descriptive study, the ticks were collected from infested ruminant in- http://jad.tums.ac.ir/ https://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=1&cad=rja&uact=8&ved=0ahUKEwjbpKKKqMjQAhWIJsAKHctqBiwQFggaMAA&url=http%3A%2F%2Fwww.cdc.gov%2F&usg=AFQjCNFZiCnTGz3JGwl6v2dGv1nb_9DNIw&bvm=bv.139782543,d.bGs J Arthropod-Borne Dis, June 2021, 15(2): 187–195 K Arzamani et al.: Biodiversity Indices and … 189 http://jad.tums.ac.ir Published Online: June 30, 2021 cluding cows, sheep, and goats during the pe- riod from 2015 to 2019. Additionally, some specimens collected from turtle, rodent, and hedgehog. The tick samples were collected from 53 different areas in the province. Specimens were performed by examining the whole body including, ears, abdomen, tail, perianal regions, milk gland area, and back of the animals. Col- lected ticks were placed in separate dry and labeled vials and transferred to the laboratory of Vector-borne Diseases Research Center, North Khorasan University of Medical Sciences. Determination of the Species Diversity All specimens were identified based on mor- phological characteristics and the keys given by Estrada-pena (2004) in the laboratory of med- ical entomology, Tehran University of Medi- cal Sciences (26). All statistical analyses were done by excel software Ver. 2010. and Alpha di- versity indices were calculated using an online biodiversity calculator (27). Results In this study, 515 (55.2%), out of the total 933 inspected sheep, goat and cow were in- fested with ticks. A total of 1478 ticks (770 males and 708 females) were collected (Table 1). The identified tick specimens belonged to two families: Ixodidae (90.05%) and Argasidae (9.95%), 6 genera and 17 species including con- cerning Ixodidae families, Rh. sanguineus (55.9 %), Rh. bursa (13.4%), Hy. marginatum (9.5%), Hy. anatolicum (9.5%), Hy. asiaticum (0.2%), Hy. aegyptium (0.5%), Hy. scupense (1.3%), Hy. sp (1.2%), Haem. sulcata (0.7%), Haem. erina- cea (0.1%), Haem. inermis (0.1%), Haem. punc- tata (0.2%), Haem. concinna (0.1), B. annula- tus (1.2), and D. marginatus (6.1%) (Table 1). Rhipicephalus (69.3%) followed by Hyalomma (22.2%) were the predominant tick genus of hard ticks. With regards to the seasonal variation, the highest and lowest tick infestation was rec- ognized in spring and winter, respectively. The results show that out of soft ticks only Ar. persicus (91.8) and Ar. reflexus (8.2) were collected in this region (Table 2). All species of hard ticks were collected from sheep except Hy. Aegyptium and Haem. concinna. Collected species base on the hosts are shown in Table3. Some of the most important Alpha diversity indices including, Species richness, Shannon- Wiener index, Simpson index, Shannon Even- ness index (Equitability index), Buzas and Gib- son's evenness index, Berger-Parker dominance index, Menhinick richness index, and Margalef richness index were calculated (Table 4). Table 1. The frequency of hard ticks by gender in North Khorasan Province, Northeast of Iran during 2015–2019 Species Male Female Total % Rh. sanguineus 404 340 744 55.9 Rh. Bursa 87 91 178 13.4 Hy. marginatum 80 47 127 9.5 Hy. anatolicum 70 56 126 9.5 D. marginatus 41 40 81 6.1 Hy. scupense 8 10 18 1.3 B. annulatus 0 16 16 1.2 Hy. Sp 0 16 16 1.2 Haem. sulcata 4 6 10 0.7 Hy. Aegyptium 3 3 6 0.5 Hy. asiaticum 3 0 3 0.2 Haem. punctata 2 1 3 0.2 Haem. erinacea 0 1 1 0.1 Haem. inermis 0 1 1 0.1 Haem. concinna 1 0 1 0.1 Total of all specimens 703 628 1331 100 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2021, 15(2): 187–195 K Arzamani et al.: Biodiversity Indices and … 190 http://jad.tums.ac.ir Published Online: June 30, 2021 Table 2. The prevalence of soft ticks in North Khorasan Province, Northeast of Iran during 2015–2019 H o st V is it R h . sa n g u in e u s R h . B u rs a H y . m a rg in a tu m H y . a n a to li c u m D . m a rg in a tu s H y . sc u p e n se B . a n n u la tu s H y . sp H a e m . su lc a ta H y . a e g y p ti u m H y . a si a ti c u m H a e m . p u n c ta ta H a e m . e ri n a c e a H a e m . in e rm is H a e m . c o n c in n a T o ta l o f a ll s p e c im e n s Sheep 812 473 107 107 91 81 12 16 10 8 0 3 3 1 1 0 913 Goat 81 267 67 2 2 0 0 0 0 2 0 0 0 0 0 0 340 Cow 40 0 2 18 33 0 6 0 0 0 0 0 0 0 0 0 59 Turtle 2 0 0 0 0 0 0 0 0 0 6 0 0 0 0 0 6 Rumbomis 1 0 0 0 0 0 0 0 4 0 0 0 0 0 0 0 4 meriones 1 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 2 Hedgehog 5 4 2 0 0 0 0 0 0 0 0 0 0 0 0 1 7 942 744 178 127 126 81 18 16 16 10 6 3 3 1 1 1 1331 Table 3. Species and numbers of hard ticks on different host collected in North Khorasan Province, Northeast of Iran from 2015 to 2019 Species Male Female Total % Ar. persicus 59 76 135 91.8 Ar. reflexus 8 4 12 8.2 Total of all specimens 67 80 147 100 Table 4. Biodiversity and species richness indices of hard ticks in North Khorasan Province, North east of Iran from 2015 to 2019 Index Computation Amount specimens Total number of specimens 1478 Species richness (S) The number of species 17 Shannon-Wiener index (H’ ) 1.69 Simpson Index 0.294 Shannon Evenness Index (Equitability Index) H/ln (S) 0.595 Buzas and Gibson's Evenness Index 0.317 Berger-Parker Dominance Index 0.503 Menhinick Richness Index 0.442 Margalef Richness Index 2.19 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2021, 15(2): 187–195 K Arzamani et al.: Biodiversity Indices and … 191 http://jad.tums.ac.ir Published Online: June 30, 2021 Fig. 1. Geographical locations of collected ticks of North Khorasan Province, Northeast of Iran Discussion Understanding the fauna species and geo- graphical distribution of ticks will provide ap- propriate strategies to control and prevention of the tick-borne diseases (28). North Khorasan Province is bordered with Turkmenistan. This province is a suitable area for agricultural pro- duction and animal husbandry (29). A consid- erable large number of sheep, goats, cows and so on graze on pastures of the province and therefore are at a greater risk of tick infesta- tion and their borne diseases (30). In this study, most of ticks were collected on the body of sheep, goats and cows, but some of other an- imals such as turtles, some rodents of Rhom- bomys and Meriones spp. and Hedgehog were infested with ticks. Most of ticks such as Ix- odes, Dermacentor, Rhipicephalus, Haemaphy- salis have at least three hosts. Telmadarraiy et al. have showed that Rh. sanguineus, Hy. mar- ginatum, Hy. anatolicum, Hy. asiaticum and Hy. dromedarii were known as the most frequent species which were positive for CCHF virus in endemic areas of Iran (23). Most of these proven vectors of CCHF in Iran were collect- ed and identified in North Khorasan in this study. In this present study, 17 species of ticks were identified including Rh. sanguineus, Rh. bursa, Hy. marginatum, Hy. anatolicum, Hy. asiaticum, Hy. aegyptium, Hy. scupense, hyalom- ma sp, Boophilus annulatus, Dermacentor mar- ginatus, Argas persicus, Ar. reflexus. It has been shown that the tick infestation on cattle included Haem. parva (33.8%), Dermacentor margina- tus (2.8%), Boophilus annulatus (21.1%), Haem. concinna (15.5%), Hy. marginatum (19.7%) and Rh. bursa (7%). Besides that, many studies on http://jad.tums.ac.ir/ J Arthropod-Borne Dis, June 2021, 15(2): 187–195 K Arzamani et al.: Biodiversity Indices and … 192 http://jad.tums.ac.ir Published Online: June 30, 2021 tick fauna have been conducted in different ar- eas of Iran. For instance, in West Azarbaijan, 7 genera and 15 species were identified includ- ing Rhipicephalus, Hyalomma and Orinthodoros and O. lahorensis, H. marginatum, H. asiaticum, Rh. bursa had the highest frequency (31). Na- bian et al. reported the presence of fourteen tick species were identified as Hy. anatolicum (5.23%), Hy. marginatum (20.34%), H. detritum (3.48%), Haemaphysalis punctate (12.79%), Haem. Parva (0.58%), Haem. concinna (0.58%), Haem. choldokovsky (6.97%), Ixodes ricinus (2.32%), Rh. sanguineus (19.76%), Rh. bursa (4.65%), Boophilus annulatus (9.88 %), Der- macentor niveus (6.39%), D. marginatus (1.74 %) and O. lahorensis (5.23%) in Ardabil, north west of Iran (18). In this research, the genera Rhipicephalus (69.3%) and Hyalomma (22.2%) were the most predominant ticks. Out of them Rh. sanguineus, Rh. bursa, Hy. marginatum and Hy. anatolicum had highest frequencies among hard ticks. A similar study was also reported from Meshkinshahr (a northwest area in Iran) in 2009 by Hosseini vasoukolaei et al. in which most of the ticks belonged to Rhipicephalus and Hyalomma genus (19). Based on the results of the Mazlum (1971) carry out on ticks Rh. bur- sa, Rh. sanguineus, Hy. anatolicum were the most common ticks in Iran that are widespread in various areas of the country (15). Nabian et al. showed that Rh. sanguineus was the domi- nant tick species on body’s seep in Mazandaran Province, North of Iran (18). Rhipicephalus bur- sa and Rh. sanguineus are very important in terms of health and medicine in Iran because they have basic role in the transmission of path- ogens in sheep. The pathogens that are trans- mitted by these tick species are Babesia canis, Ba. equi, Ba. caballi, Theileria ovis, Anaplasma marginale and Rickettsia oina (32). The Hy- alomma ticks are most common ticks in Iran has been isolated from different domestic ani- mals. Mazloum studies indicated that Hy. ana- tolicum is one of the prevalent ticks in Iran. Hyalomma anatolicum can transmit many in- fectious agents of humans such as Theileria an- nulata, Theileria parva, Ba. caballi, Q fever and CCHF. Previous epidemiological studies in Khorasan Provinces have demonstrated that CCHF disease is one of endemic disease in this region (23, 25). It also has an important role in transmission of Theileria herci to sheep in Iran with regards to the seasonal variation, the highest and lowest tick infestation was rec- ognized in spring and winter, respectively (33). Other studies have been indicated the highest tick infestation distribution was spring and sum- mer (16, 34-35). In principle, ticks are most ac- tive in hot seasons and humidity. In these are- as due to livestock grazing season (spring and summer when the heat is suitable for com- plete life cycle of ticks) and putting them in the pasture, the tick distribution will be main- ly influenced by rainfall (36). Six Haemaphy- salis species have been recorded by different authors in Iran and three species of them have been reported previously from North Khorasan Province (37). In the current study we report five species of this genus, so all species of this genus which reported from Iran collected from North Khorasan Province. There are only lim- ited studies in Iran in which the authors calcu- lated the biodiversity indices of ticks. Further- more, to the best of our knowledge, there has not been any report on biodiversity of ticks in North Khorasan Province and this is the first work that provides a numerical index on bio- diversity of ticks in this region. The result showed tick’s species richness, Shannon diver- sity index and Simpson index in this area were higher than some other regions in the country (38-41). Conclusion The present study showed a high degree of diversity of ticks in North Khorasan Prov- ince, northeast of Iran. Some of the most med- ically and veterinary important spices of ticks were collected from this region. It is important to awareness of fauna and the distribution of ticks in order to apply effective tick control pro- http://jad.tums.ac.ir/ https://www.google.com/search?biw=1608&bih=827&q=Theileria+ovis&spell=1&sa=X&ved=0ahUKEwiDlOKMqNLQAhVhD8AKHbuWCbQQvwUIFygA&dpr=0.9 https://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=1&cad=rja&uact=8&ved=0ahUKEwjao6CgqNLQAhVGBsAKHRJuBbMQFggaMAA&url=https%3A%2F%2Fmicrobewiki.kenyon.edu%2Findex.php%2FAnaplasma_marginale&usg=AFQjCNHghiLzlwFmcVjdAtoLnKXTwfZoeQ https://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=1&cad=rja&uact=8&ved=0ahUKEwjao6CgqNLQAhVGBsAKHRJuBbMQFggaMAA&url=https%3A%2F%2Fmicrobewiki.kenyon.edu%2Findex.php%2FAnaplasma_marginale&usg=AFQjCNHghiLzlwFmcVjdAtoLnKXTwfZoeQ J Arthropod-Borne Dis, June 2021, 15(2): 187–195 K Arzamani et al.: Biodiversity Indices and … 193 http://jad.tums.ac.ir Published Online: June 30, 2021 grams and prevention of the disease in the re- gion. We declare that we have no conflict of interest. Acknowledgements The authors are grateful to the research dep- uty of North Khorasan University of Medical Science. This study received financial support from Vector-borne Diseases Research Center, North Khorasan University of Medical Scienc- es, Bojnurd, Iran (Project No: Code of Ethics: 91/390). The authors declare that there is no conflict of interest. References 1. Service MW (1980) A Guide to Medical En- tomology London and Basingstoke: Mac- millan Press. p. 226. 2. Kazimirova M, Stibraniova I (2013) Tick sal- ivary compounds: their role in modula- tion of host defenses and pathogen trans- mission. Front Cell Infect. Microbiol. 3: 43. 3. Jongejan F, Uilenberg G (2004) The global importance of ticks. Parasitology. 129: S3–14. 4. Demessie Y, Derso S (2015) Tick Borne Hemoparasitic Diseases of Ruminants: A Review. Adv Biol Res. 9: 210–224. 5. Smith T, Kilbourne FL (1893) (Investiga- tors into the nature, causation, and pre- vention of Texas or southern cattle fe- ver. Bull Bur Anim Ind. 1: 301. 6. Guglielmone GA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG (2010) The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida) of the world: a list of valid species names. Zootaxa. 2528: 1–28. 7. Szabó MPJ, Castro MB, Ramos HGC, Gar- cia MV, Castagnolli KC, Pinter A (2007) Species diversity and seasonality of free- living ticks (Acari: Ixodidae) in the nat- ural habitat of wild Marsh deer (Blasto- cerus dichotomus) in Southeastern Bra- zil. Vet Parasitol. 143: 147–154. 8. Yu Z, Wang H, Wang T, Sun W, Yang X, Liu J (2015) Tick-borne pathogens and the vector potential of ticks in China. Para- site vectors. 148: 24. 9. Grech-Angelini S, Stachurski F, Lancelot R, Boissier J, Allienne JF, Marco S, Maes- trini O, Uilenberg G (2016) Ticks (Acari: Ixodidae) infesting cattle and some other domestic and wild hosts on the French Mediterranean island of Corsica. Para- site vectors. 9: 582. 10. ElGhali A, Hassan SM (2012) Ticks infest- ing animals in the Sudan and southern Su- dan: Past and current status. J Vet Res. 79: 431–437. 11. Sertse T, Wossene A (2007) A study on ec- toparasites of sheep and goats in eastern part of Amhara region, northeast Ethio- pia. Small Ruminant Res. 69: 62–67. 12. Mamak N, Gençer L, Ozkanlar YE, Ozçelik S (2006) Determination of tick species and treatment of cows, sheep and goats in the Sivas-Zara region, Turkiye. Parazitol Derg. 30: 209–212. 13. Delpy L (1936) Note sur les Ixodides dugen- re Hyalomma (Koch). Ann Parasitol Hum Comp. 14: 206–245. 14. Abbasian L (1961) Records of tick (Aca- rina: Ixodidae) occurring in Iran and their distributional data. Acarologia. 3: 546– 559. 15. Mazlum Z (1971) Different Ticks occur- ring in Iran (geographical distribution, seasonal activities, hosts), Bull. Faculty of Veterinary. 27: 1–32. 16. Razmi GR, Glinsharifodini M, Sarvi S (2007) Prevalence of ixodid ticks on cat- tle in Mazandaran Province, Iran. Kore- an J Parasitol. 45: 307–310. 17. Rahbari S, Nabian S, Shayan P (2007) Pri- mary report on distribution of tick fauna in Iran. Parasitol Res. 101(Suppl): S175– S177. http://jad.tums.ac.ir/ https://www.ncbi.nlm.nih.gov/pubmed/?term=Yu%20Z%5BAuthor%5D&cauthor=true&cauthor_uid=25586007 https://www.ncbi.nlm.nih.gov/pubmed/?term=Wang%20H%5BAuthor%5D&cauthor=true&cauthor_uid=25586007 https://www.ncbi.nlm.nih.gov/pubmed/?term=Wang%20T%5BAuthor%5D&cauthor=true&cauthor_uid=25586007 https://www.ncbi.nlm.nih.gov/pubmed/?term=Sun%20W%5BAuthor%5D&cauthor=true&cauthor_uid=25586007 https://www.ncbi.nlm.nih.gov/pubmed/?term=Yang%20X%5BAuthor%5D&cauthor=true&cauthor_uid=25586007 https://www.ncbi.nlm.nih.gov/pubmed/?term=Liu%20J%5BAuthor%5D&cauthor=true&cauthor_uid=25586007 https://www.ncbi.nlm.nih.gov/pubmed/?term=Grech-Angelini%20S%5BAuthor%5D&cauthor=true&cauthor_uid=27842608 https://www.ncbi.nlm.nih.gov/pubmed/?term=Stachurski%20F%5BAuthor%5D&cauthor=true&cauthor_uid=27842608 https://www.ncbi.nlm.nih.gov/pubmed/?term=Lancelot%20R%5BAuthor%5D&cauthor=true&cauthor_uid=27842608 https://www.ncbi.nlm.nih.gov/pubmed/?term=Boissier%20J%5BAuthor%5D&cauthor=true&cauthor_uid=27842608 https://www.ncbi.nlm.nih.gov/pubmed/?term=Allienne%20JF%5BAuthor%5D&cauthor=true&cauthor_uid=27842608 https://www.ncbi.nlm.nih.gov/pubmed/?term=Marco%20S%5BAuthor%5D&cauthor=true&cauthor_uid=27842608 https://www.ncbi.nlm.nih.gov/pubmed/?term=Maestrini%20O%5BAuthor%5D&cauthor=true&cauthor_uid=27842608 https://www.ncbi.nlm.nih.gov/pubmed/?term=Maestrini%20O%5BAuthor%5D&cauthor=true&cauthor_uid=27842608 https://www.ncbi.nlm.nih.gov/pubmed/?term=Uilenberg%20G%5BAuthor%5D&cauthor=true&cauthor_uid=27842608 http://www.scopus.com/scopus/search/submit/author.url?author=Sertse%2c+T.&origin=resultslist&authorId=16032378400&src=s http://www.scopus.com/scopus/search/submit/author.url?author=Wossene%2c+A.&origin=resultslist&authorId=16032051900&src=s http://www.ncbi.nlm.nih.gov/sites/entrez?Db=pubmed&Cmd=Search&Term=%22Mamak%20N%22%5BAuthor%5D&itool=EntrezSystem2.PEntrez.Pubmed.Pubmed_ResultsPanel.Pubmed_RVAbstractPlus http://www.ncbi.nlm.nih.gov/sites/entrez?Db=pubmed&Cmd=Search&Term=%22Gen%C3%A7er%20L%22%5BAuthor%5D&itool=EntrezSystem2.PEntrez.Pubmed.Pubmed_ResultsPanel.Pubmed_RVAbstractPlus http://www.ncbi.nlm.nih.gov/sites/entrez?Db=pubmed&Cmd=Search&Term=%22Ozkanlar%20YE%22%5BAuthor%5D&itool=EntrezSystem2.PEntrez.Pubmed.Pubmed_ResultsPanel.Pubmed_RVAbstractPlus http://www.ncbi.nlm.nih.gov/sites/entrez?Db=pubmed&Cmd=Search&Term=%22Oz%C3%A7elik%20S%22%5BAuthor%5D&itool=EntrezSystem2.PEntrez.Pubmed.Pubmed_ResultsPanel.Pubmed_RVAbstractPlus http://www.ncbi.nlm.nih.gov/sites/entrez?Db=pubmed&Cmd=Search&Term=%22Oz%C3%A7elik%20S%22%5BAuthor%5D&itool=EntrezSystem2.PEntrez.Pubmed.Pubmed_ResultsPanel.Pubmed_RVAbstractPlus javascript:AL_get(this,%20'jour',%20'Turkiye%20Parazitol%20Derg.'); https://www.ncbi.nlm.nih.gov/pubmed/?term=Razmi%20GR%5BAuthor%5D&cauthor=true&cauthor_uid=18165714 https://www.ncbi.nlm.nih.gov/pubmed/?term=Glinsharifodini%20M%5BAuthor%5D&cauthor=true&cauthor_uid=18165714 https://www.ncbi.nlm.nih.gov/pubmed/?term=Sarvi%20S%5BAuthor%5D&cauthor=true&cauthor_uid=18165714 https://www.ncbi.nlm.nih.gov/pubmed/18165714 https://www.ncbi.nlm.nih.gov/pubmed/18165714 J Arthropod-Borne Dis, June 2021, 15(2): 187–195 K Arzamani et al.: Biodiversity Indices and … 194 http://jad.tums.ac.ir Published Online: June 30, 2021 18. Nabian S, Rahbari S, Shayan P, Haddadza- deh HR (2007) Current status of tick fau- na in north of Iran. Iran. J Parasitol. 2: 12–17. 19. Hosseini vasoukolaei, N, Telmadarraiy Z, Vatandoost H, Yaghoobi Ershadi MR, Hosseini vasoukolaei M, Oshaghi MA (2010) Survey of tick species parasiting domestic ruminants in Ghaemshahr Coun- ty, Mazandaran Province, Iran. Asian Pac J Trop Med. 3: 804–806. 20. Asadollahi Z, Razi Jalali MH, Alborzi A, Hamidinejat H, Pourmahdi Boroujeni M, Sazmand A (2014) Study of cattle ixodid ticks in Khoozestan Province, South-West of Iran. Acarina. 22: 157–160. 21. Ramezani Z, Chavshin AR, Telmadarraiy Z, Edalat H, Dabiri F, Vatandoost H, Zarei Z, Beik-Mohammadi M (2014) Ticks (Ac- ari: Ixodidae) of livestock and their sea- sonal activities, northwest of Iran. Asian Pac J Trop Dis. 4: 754–757. 22. Ganjali M, Dabirzadeh M, Sargolzaie M (2014) Species Diversity and Distribu- tion of Ticks (Acari: Ixodidae) in Zabol County, Eastern Iran. J Arthropod Borne Dis. 8: 219–223. 23. Telmadarraiy Z, Chinikar S, Vatandoost H, Faghihi F, Hosseini-Chegeni, A (2015) Vectors of Crimean Congo Hemorrhag- ic Fever Virus in Iran. J Arthropod Borne Dis. 9: 137–147. 24. Chinikar S, Ghiasi SM, Moradi M, Goya MM, Shirzadi MR, Zeinali M, Meshkat M, Bouloy M (2010) Geo graphical dis- tribution and surveillance of Crimean- Congo hemorrhagic fever in Iran. Vector Borne Zoonotic Dis. 10: 705–708. 25. Chinikar S, Ghiasi SM, Naddaf S, Piazak N, Moradi M, Razavi MR (2012) Sero- logical evaluation of Crimean-Congo hem- orrhagic fever in humans with high-risk professions living in enzootic regions of Isfahan Province of Iran and genetic anal- ysis of circulating strains. Vector Borne Zoonotic Dis. 12: 733–738. 26. Estrada-Pena A, Bouattour A, Camicas JL, Walker AR (2004) Ticks of Domestic animals in the mediterranean. A guide to the identification of species. Bioscience reports. London, UK. 27. Biodiversity Calculator. Retrieved Novem- ber 5, 2019. Available at: https://www.alyoung.com/labs/biodiver sity_calculator.html 28. Inci A, Yildirim A, Duzlu O, Doganay M, Aksoy S (2016) Tick-Borne Diseases in Turkey: A Review Based on One Health Perspective. PlOS Negl Trop Dis. 10: e0005021. 29. Ghorbani M, Jafari F (2013) Wheat risk diversification in North Khorasan Prov- ince: A risk profile analysis. African J Economics. 1: 162–169. 30. Razmi GR, Naghibi A, Aslani MR, Fathi- vand M, Dastjerdi K (2002) An epide- miological study on ovine babesiosis of Khorasan Province, Iran. Vet Parasitol. 108: 109–115. 31. Yakhchali M, Hosseine A (2006) Preva- lence and ectoparasites fauna of sheep and goats flocks in Urmia suburb, Iran. Veterinarskio Arhiv. 76: 431–442. 32. Jongejan F, Ringenier M, Putting M, Ber- ger L, Burgers S, Kortekaas R (2015) Novel foci of Dermacentor reticulatus ticks infected with Babesia canis and Babesia caballi in the Netherlands and in Belgium. Parasite Vectors. 8: 232. 33. Nourollahi Fard SR, Khalili M (2011) PCR- Detection of Coxiella burnetii in Ticks Collected from Sheep and Goats in South- east Iran. Iran J Arthropod Borne Dis. 5: 1–6. 34. Nasiri A, Telmadarraiy Z, Vatandoost H, Chinikar S (2010) Tick Infestation rat of sheep and their distribution in Abdanan County, Ilam Province, Iran, 2007–2008. Iran J Arthropod Borne Dis. 4: 56–60. 35. Asgarian F, Enayati AA, Amouei A, Yazda- ni Charati J (2011) Fauna, Geographical Distribution and Seasonal Activity of Hard http://jad.tums.ac.ir/ https://acarina.utmn.ru/journal/authors-list/172682/ https://acarina.utmn.ru/journal/authors-list/172683/ https://acarina.utmn.ru/journal/authors-list/172684/ https://acarina.utmn.ru/journal/authors-list/172685/ https://acarina.utmn.ru/journal/authors-list/172686/ https://acarina.utmn.ru/journal/authors-list/172687/ http://www.sciencedirect.com/science/article/pii/S2222180814607210 http://www.sciencedirect.com/science/article/pii/S2222180814607210 http://www.sciencedirect.com/science/article/pii/S2222180814607210 http://www.sciencedirect.com/science/article/pii/S2222180814607210 http://www.sciencedirect.com/science/article/pii/S2222180814607210 http://www.sciencedirect.com/science/article/pii/S2222180814607210 http://www.sciencedirect.com/science/article/pii/S2222180814607210 http://www.sciencedirect.com/science/article/pii/S2222180814607210 http://www.sciencedirect.com/science/journal/22221808 http://www.sciencedirect.com/science/journal/22221808 http://www.sciencedirect.com/science/journal/22221808/4/supp/S2 https://www.alyoung.com/labs/biodiversity_calculator.html https://www.alyoung.com/labs/biodiversity_calculator.html https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5158090/ http://www.scopus.com/scopus/search/submit/author.url?author=Yakhchali%2c+M.&origin=resultslist&authorId=15074298700&src=s http://www.scopus.com/scopus/search/submit/author.url?author=Hosseine%2c+A.&origin=resultslist&authorId=15074140800&src=s J Arthropod-Borne Dis, June 2021, 15(2): 187–195 K Arzamani et al.: Biodiversity Indices and … 195 http://jad.tums.ac.ir Published Online: June 30, 2021 Ticks from Sari Township in 2007–2008. J Mazandaran Univ Med Sci. 21: 25–33. 36. Urquhart GM, Armour J, Duncan JL, Dunn AM, Jennings FW (1996) Veterinary par- asitology, 2nd ed. Glasgow, Scotland: Wiley-Black Well. 37. Hosseini-Chegeni A, Telmadarraiy Z, Sali- mi M, Arzamani K, Banafshi O (2014) A record of Haemaphysalis erinacei (Ac- ari: Ixodidae) collected from Hedgehog and an identification key for the species of Haemaphysalis occurring in Iran. Persian J Acarol. 3(3): 203–215. 38. Shemshad K, Rafinejad J, Kamali K, Piazak N, Sedaghat MM, Shemshad M (2012) Species diversity and geographic distri- bution of hard ticks (Acari: Ixodoidea: Ixodidae) infesting domestic ruminants, in Qazvin Province, Iran. Parasitol Res. 110: 373–380. 39. Farahi A, Ebrahimzade E, Nabian S, Hanafi- Bojd AA, Akbarzadeh K, Bahonar A (2016) Temporal and spatial distribution and species diversity of hard ticks (Aca- ri: Ixodidae) in the eastern region of Cas- pian Sea. Acta Trop. 164: 1–9. 40. Sofizadeh A, Akbarzadeh K, Telmadarraiy Z, Gorganli-Davaji A (2019) Distribution and Biodiversity of Hard Ticks (Acarina: Ixodidae) in Golestan Province. Sjsph. 16(4): 411–424. 41. Fazeli-Dinan M, Asgarian F, Nikookar SH, Ziapour SP, Enayati A (2019) Defining and comparison of biodiversity compo- nents of hard ticks on domestic hosts at Highland, Woodland and Plain in North- ern Iran. Trop Biomed. 36: 114–130. http://jad.tums.ac.ir/ https://www.ncbi.nlm.nih.gov/pubmed/?term=Farahi%20A%5BAuthor%5D&cauthor=true&cauthor_uid=27519473 https://www.ncbi.nlm.nih.gov/pubmed/?term=Ebrahimzade%20E%5BAuthor%5D&cauthor=true&cauthor_uid=27519473 https://www.ncbi.nlm.nih.gov/pubmed/?term=Nabian%20S%5BAuthor%5D&cauthor=true&cauthor_uid=27519473 https://www.ncbi.nlm.nih.gov/pubmed/?term=Hanafi-Bojd%20AA%5BAuthor%5D&cauthor=true&cauthor_uid=27519473 https://www.ncbi.nlm.nih.gov/pubmed/?term=Hanafi-Bojd%20AA%5BAuthor%5D&cauthor=true&cauthor_uid=27519473 https://www.ncbi.nlm.nih.gov/pubmed/?term=Akbarzadeh%20K%5BAuthor%5D&cauthor=true&cauthor_uid=27519473 https://www.ncbi.nlm.nih.gov/pubmed/?term=Bahonar%20A%5BAuthor%5D&cauthor=true&cauthor_uid=27519473 https://www.ncbi.nlm.nih.gov/pubmed/27519473