J Arthropod-Borne Dis, December 2019, 13(4): 369–377 Firoozfar F et al.: Faunistic Composition and … 369 http://jad.tums.ac.ir Published Online: December 31, 2019 Original Article Faunistic Composition and Spatial Distribution of Scorpions in North Khorasan Province Northeast of Iran Faranak Firoozfar1,2; *Abedin Saghafipour3; Hassan Vatandoost4; Mulood Mohammadi Bavani5; Masoumeh Taherpour2; Nahid Jesri6; Mahmood Yazdani1; Kourosh Arzamani1 1Vector-borne Diseases Research Center, North Khorasan University of Medical Sciences, Bojnurd, Iran 2Department of Public Health, Faculty of North Khorasan University of Medical Sciences, Bojnurd, Iran 3Department of Public Health, Faculty of Health, Qom University of Medical Sciences, Qom, Iran 4Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 5Department of Medical Entomology and Vector Control, School of Public Health, Urmia University of Medical Sciences, Urmia, Iran 6Remote Sensing and GIS Center, Shahid Beheshti University, Tehran, Iran (Received 16 Oct 2018; accepted 18 Dec 2019) Abstract Background: Scorpions pose one of the most important public health and medical problems in tropical and subtropi- cal regions of the world, especially in developing countries. This study was conducted to determine the fauna and spatial distribution of scorpions. Methods: In this descriptive study, scorpions were captured using ultra-violet (UV) light, pitfall traps and digging methods in North Khorasan Province, northeastern Iran in 2017. After being encoded, the collected scorpions were stored in plastic containers of 70% ethanol and then transferred to the medical entomology lab of Tehran University of Medical Sciences for species identification based on morphological keys. In addition, Arc GIS 9.3 software was utilized for mapping spatial distribution of scorpions. Results: Overall, 143 scorpions were captured and identified. All of collected scorpions belonged only to Buthidae family. They were also classified into four genera (Androctonus, Mesobuthus, Odontobuthus, Orthochirus) and five species: M. eupeus (59.44%), A. crassicauda (16.78%), O. doriae (12.59), M. (Olivierus) caucasicus (9.09%), and O. farzanpayi (2.10%). Furthermore, spatial distribution of scorpions was performed in this area. Conclusion: Regarding the diversity, high frequency and wide geographical distribution of scorpions and their long- term seasonal activity in this area, the probability of occurrence of scorpion sting is high. Therefore, in order to pre - vent the occurrence of this public health problem, health educational programs be implemented by health- care pro- viders in the area. Keywords: Scorpions; Spatial distribution; GIS; Iran Introduction Scorpions (Arachnida: Scorpions) are one of the oldest terrestrial arthropods, dating back to about 450 million years ago (1). These an- imals are nocturnal, meaning that they leave their shelter at night for hunting and other bi- ological activities but in daytime, they are hid- den in their sanctuaries including seams and gaps of walls, underground holes, undersides of rocks, under the leaves and shells of trees, etc. Scorpions have venomous stings that they use to capture insects and defend themselves against natural enemies (2). Scorpions feed on insects, spiders, mites and some small verte- brates, while some species of them are can- nibals (3, 4). These creatures often live in de- sert areas, but some of their species are found under rocks in mountainous and forest areas. Non-digger and semi-digger scorpions can en- ter human habitats (2). Although the scorpions do not transmit any *Corresponding author: Dr Abedin Saghafipour, E- mail: abed.saghafi@yahoo.com http://jad.tums.ac.ir/ J Arthropod-Borne Dis, December 2019, 13(4): 369–377 Firoozfar F et al.: Faunistic Composition and … 370 http://jad.tums.ac.ir Published Online: December 31, 2019 pathogens and parasitic agents to humans, they have always been one of human concerns due to their venomous and deadly stings, as well as scary appearance. Some species of scorpi- ons are medically important and cause rela- tively high mortality in some areas of the world (5). Therefore, scorpionism turns out to be one of the most important public health and med- ical issues in tropical and subtropical regions of the world, especially in developing coun- tries (6). In Iran, in addition to the anxiety and concern caused by scorpion sting, its high cost of treatment, and the resulting health-related consequences, deaths from scorpion stings are also reported annually (7). According to the Centers for Disease Control and Prevention (CDC) of Iranian Ministry of Health and Med- ical Education, approximately 40000–50000 cases of scorpionism occur annually in Iran (8, 9). Systematically in the world, the scorpions are classified into six super families, 13 fami- lies, 18 subfamilies and 10 tribes and more than 2,000 species (10, 11). A review of the previ- ously published articles in this regard showed that there are three families of scorpions in Iran, including Buthidae, Scorpionidae, Hemiscor- pidae, identified in the form of 19 genera and 59 species (12-14). There is no information about scorpion fauna of this Province and there is a big gap in the case of spatial distribution of scorpions in this area, regarding the reports of annual scor- pion sting cases from North Khorasan health centers (15) and having no information about scorpions, therefore, we for the first conduct- ed a survey to determine scorpion fauna and their spatial distribution in North Khorasan Province, northeast of Iran. Materials and Methods Study area The North Khorasan Province has an ar- ea of 28179km2. It has 8 counties including Bojnurd, Shirvan, Esfarayen, Mane, Raz Jar- galan, Jajarm, Faruj and Garme. The popula- tion of this province is 811,572. Geograph- ically, this province has common borders with Turkmenistan in the north, Khorasan Razavi Province in the east and south, Semnan Prov- ince in the southwest, and Golestan Province in the west (16). Scorpion collection and identification In this descriptive study, all of urban and rural areas of North Khorasan Province were investigated by considering factors such as climatic conditions (such as temperature, hu- midity), geographical factors (such as eleva- tion, vegetation status, soil type, rainfall) and the different climate areas (desert, semi-desert, foothills and mountainous areas) during Jan– Dec 2017 (17). In each of the counties, two or three sites were selected as sampling loca- tions. Locations were selected in terms of be- ing plain or mountainous. Twenty-four loca- tions were determined for collecting scorpi- ons (Fig. 1). At each location, residential and non-residential areas were also taken into ac- count. Scorpions were captured using three methods: a): ultra-violet (UV) light, in which the researchers made a search for scorpions for two hours in probable scorpions’ habitats including under the stones, under the leaves and shells of trees. At night and daytime be- fore sunset (18). b): Pitfall traps in which plas- tic containers (with 8cm width and 1cm depth) were placed at stations located in the plains on a possible path of scorpion movement at a depth of 11cm of soil, and in order to draw scorpions, moist cotton was placed inside the traps (19). Ten traps were used at each loca- tion, amounting to a total of 80 traps and the scorpions were collected using iris forceps; and c): digging method by which the research- ers identified probable scorpions’ habitats (un- derground cavities drilled by scorpions) at sta- tions located in plain areas with soft soil and poured some water into their habitats in or- der to collect digger scorpions. Finally, scor- pions were collected with the use of an iris 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=0ahUKEwjbu82n-NbYAhUqIpoKHYxTDZMQFgglMAA&url=https%3A%2F%2Fwww.cdc.gov%2F&usg=AOvVaw347QtT6pi6CdNKfM8VFdw6 J Arthropod-Borne Dis, December 2019, 13(4): 369–377 Firoozfar F et al.: Faunistic Composition and … 371 http://jad.tums.ac.ir Published Online: December 31, 2019 forceps (20). For morphological identification, after being encoded, the collected scorpions were stored in plastic containers having 70% ethanol and then transferred to the medical entomology lab of Tehran University of Med- ical Sciences for species identification based on morphological keys (5). Statistical analysis Arc GIS 9.3 software was used for map- ping spatial distribution of scorpions. Results Overall, 143 scorpions were captured and identified. All collected scorpions belonged only to Buthidae family. Moreover, they were classified into four genera (Androctonus, Mes- obuthus, Odontobuthus, Orthochirus) and five species namely, M. eupeus (59.44%), A. crassicauda (16.78%), O. doriae (12.59), M. (Olivierus) caucasicus (9.09%), and O. far- zanpayi (2.10%) (Table 1). The highest fre- quency of scorpions (72.94%) belonged to desert areas. In addition, the majority of them (58.04%) were captured in areas with clay soil. The frequency of captured scorpion was ap- proximately similar in urban and rural areas (48.95% in urban areas versus 51.05% in ru- ral areas). Most of collected samples were gath- ered from outdoors areas (84.61%). The ma- jority of scorpion’s samples (70 of 143) were captured in summer (August) using ultra-vi- olet (UV) light (75.52%) method (Fig. 2). Mesobuthus eupeus Totally, 85 samples of M. eupeus (59.44% of the gathered specimens) were gathered. Ac- cording to its spatial distribution, these scor- pion species were collected from all 8 coun- ties in the province; that is, from Jajarm to Raz Jargalan (Table 1, Fig. 3). It was captured in different climate areas. The other ecologi- cal characteristics of this species have been presented in Table 2. These non-digger scor- pion species were collected in urban and ru- ral regions from desert and mountainous areas which had the altitude range of 850–2118m. In this study, 75.29% of the samples were col- lected from outside human dwellings such as under stones and bark of trees, on the farm, around the houses, in deserts, old homes, and grasslands. The others (24.71%) were caught inside human habitats (storage place, under car- pets, under furniture, inside wardrobes). Fig. 1. (A) The study area in North Khorasan Province, Northeast of Iran, (B) study area based on altitude http://jad.tums.ac.ir/ J Arthropod-Borne Dis, December 2019, 13(4): 369–377 Firoozfar F et al.: Faunistic Composition and … 372 http://jad.tums.ac.ir Published Online: December 31, 2019 Table 1. Spatial distribution of scorpions captured in northeast of Iran Species Location Longitude (Decimal degree) Latitude (Decimal degree) M. eupeus M. caucasicus O. farzanpay A. crassicauda O. doriae Total County Altitude (m) N % N % N % N % N % N % Garme 2118 56.290284° 36.985493° 15 17.65 - 0.00 3 100 6 25.00 4 22.22 28 19.58 Esfarayen 1244 57.496673° 37.066677° 16 18.82 3 23.08 - 0.00 5 20.82 3 16.67 27 18.88 Mane 850 56.741207° 37.662061° 13 15.29 - 0.00 - 0.00 5 20.82 3 16.67 21 14.68 Bojnurd 1070 57.314313° 37.470214° 18 21.18 - 0.00 - 0.00 1 4.17 1 5.55 20 13.99 Raz jargalan 1279 57.109775° 37.932390° 10 11.77 - 0.00 - 0.00 4 16.68 5 27.27 19 13.29 Faruj 1200 58.098205° 37.085118° 5 5.88 7 53.84 - 0.00 2 8.34 1 5.56 15 10.49 Shirvan 1097 57.927618° 37.409236° 5 5.88 - 0.00 - 0.00 1 4.17 1 5.56 7 4.90 Jajarm 1000 56.371311° 36.963614° 3 3.53 3 23.08 - 0.00 - 0.00 - 0.00 6 4.19 Total - 57.101294° 37.471000° 85 59.44 13 9.09 3 2.10 24 16.78 18 12.59 143 100 Table 2. Some ecological characteristic of scorpions captured in northeast of Iran Scorpion species Ecological characteristic Different climate areas Type of soil Time of capture Season of capture Deserts Mountains Semi desert Foothills Sandy Clay Night N (%) Day N (%) Spring Summer Autumn Winter M. eupeus 62 (72.94) 13 (15.30) 3 (3.53) 7 (8.23) 49 (57.65) 36 (42.35) 69 (81.18) 16 (18.82) 8 74 2 1 A. crassicauda 22 (91.66) - - 2 (8.34) 3 (12.50) 21 (87.50) 17 (70.83) 7 (29.17) 5 18 1 - O. doriae 18 (100) - - - 2 (11.11) 16 (88.89) 12 (66.67) 4 (33.33) 2 13 1 - M. caucasicus 7 (53.84) - 3 (23.08) 3 (23.08) 3 (13.08) 10 (76.92) 7 (53.8) 6 (46.2) 2 11 - - O. farzanpayi 3 (100) - - - - 3 (100) 3 (100) - - 3 - - http://jad.tums.ac.ir/ J Arthropod-Borne Dis, December 2019, 13(4): 369–377 Firoozfar F et al.: Faunistic Composition and … 373 http://jad.tums.ac.ir Published Online: December 31, 2019 0 25 50 75 Ja n u a ry F e b ru a ry M a rc h A p ri l M a y Ju n e Ju ly A u g u st S e p te m b e r O c to b e r N o v e m b e r D e c e m b e r S c o r p io n f r e q u e n c y Fig. 2. Average monthly scorpion collection, northeast of Iran, 2017 Fig. 3. Spatial distribution of captured scorpions, northeast of Iran, 2017 Androctonus crassicauda Overall, 24 samples (16.78% of the collect- ed specimens) from all of counties were cap tured from deserts and foothills areas with the exception of Jajarm County at an altitude of http://jad.tums.ac.ir/ J Arthropod-Borne Dis, December 2019, 13(4): 369–377 Firoozfar F et al.: Faunistic Composition and … 374 http://jad.tums.ac.ir Published Online: December 31, 2019 10m (Fig. 3). This species was collected both at indoor and outdoor human dwellings. This species was mostly caught in clay soil at nights and during the summer (Table 2). Odontobuthus doriae This digger scorpion species wascollect- ed in all North Khorasan counties except Ja- jarm County (Fig. 3). This species was caught only outside human settlements and in plain and desert areas. The majority of this species was captured in clay soil at nights and during the summer (Table 2). Mesobuthus caucasicus This species was gathered in Jajarm, Faruj and Esfarayen Countries from desert, semi-de- sert and foothill areas with an altitude range of 1000 to 1244m (Fig. 3). The other ecolog- ical characteristics of this species have been presented in Table 2. Orthochirus farzanpayi This scorpion species was captured only in Garme County; the highest area of North Khorasan Province with three specimens (Fig. 3). This species was collected in desert area and in sandy soil at nights and during the summer. (Table 1, 2). Discussion The results of the present investigation indicate that five scorpion species were iden- tified in the studied areas. All of collected species belonged to Buthidae family, which is in agreement with the results of research carried out in other regions of Iran. Accord- ing to studies conducted in Taibad County of Razavi Province, Darmian County of South Khorasan, Sistan, and Baluchestan (southeast- ern Iran), Kerman and Shiraz (southern Iran), most of captured scorpion species were of Buthidae family as well (21-23). Factors such as the high adaptability of species in this family due to different climatic conditions have led to their extensive geographical distribution in different regions, as species of this family have been widely dispersed in different areas of the world and Iran (21). Based on GIS find- ings, the members of this family was captured in all the counties and habitats with different climatic areas, and ecologic conditions in urban and rural areas outside human dwell- ings such as under stones and bark of trees, on the farm, around the houses, in deserts, old homes and grasslands. In line with previous studies in different areas of Iran, in the current research, M. eu- peus was the dominant species in the study area (22, 24). Additionally, in the present study A. crassicauda were gathered from all of coun- ties in deserts and foothill areas except for Jajarm County. This species was collected both at indoor and outdoor human dwellings. Furthermore, this species was mostly collect- ed in clay soil during the summer season and at nights. This species has been reported in most provinces of Iran such as Bushehr, Sem- nan, Khuzestan, Ilam, West Azarbaijan, Kur- distan, Khorasan Razavi, South Khorasan, Kerman, Kermanshah and Sistan and Balu- chistan (25), all of which verify the results of this research. The other scorpion species col- lected in this present study was M. caucasi- cus. It in terms of frequency, it ranked sec- ond among the collected scorpions in North Khorasan Province. This is also in line with the results of previous studies carried out in other areas of Iran such as West Azerbaijan, Sistan and Baluchestan, Isfahan, Khorasan, Tehran, and Semnan provinces (26). The pres- ence of this scorpion species in the current study can be confirmed by previous reports of this species in Razavi Khorasan and Sis- tan and Baluchestan provinces, in all of which the study areas had climatic conditions simi- lar to that of the current study. In the present study, O. farzanpayi was found with very low frequency only in Garme County. This spe- cies was collected in mountainous areas and in sandy soil at nights and during summer. http://jad.tums.ac.ir/ J Arthropod-Borne Dis, December 2019, 13(4): 369–377 Firoozfar F et al.: Faunistic Composition and … 375 http://jad.tums.ac.ir Published Online: December 31, 2019 The size of adult O. farzanpayi is 3 centime- ters and often distributed in desert and dry areas. Spatial distribution of this scorpion spe- cies was reported in plain and flat regions of Hormozgan and South Khorasan provinces (south and east of Iran) and has been previ- ously proven (27). Odontobuthus doriae as a digger scorpion species was captured in all North Khorasan counties except in Jajarm County. This species was caught only outside human settlements and in plain and desert ar- eas. The majority of this species was captured in clay soil at nights and during summer. This digger scorpion is able to dig a cavity up to 40 centimeters deep within the earth. Data of the current research indicated that the scorpion activity started in March, and reached its peaked in August when the weath- er was favorable, leading to a gradual increase in the frequency of scorpion species. This find- ing was corroborated by others (21, 22). The presence of suitable environmental conditions for the emergence of species has caused the presence of scorpion species to reach its peak in the study area in August. Therefore, due to the high incidence of scorpions in the envi- ronment in Aug, the scorpion sting cases al- so tend to increase, which call for an urgent need to implement training programs by health- care providers in an effort to prevent scorpi- onism in this month. In this investigation, most of scorpions were collected at night. This in agreement with the results of re- search carried out in other regions of Iran such as South Khorasan Province (22, 28). According to the scientific fact that scorpi- ons are nocturnal creatures, this finding is the- oretically expected. Therefore, personal pro- tection against scorpion stings at night be undertaken. To the current authors’ knowledge, among the limitations of this study mention can be made of the potential risks of scorpi- on stings and the problems of collecting scor- pions in mountainous areas. Conclusion We captured five scorpions’ species in- cluding M. eupeus, M. caucasicus, O. dori- ae, A. crassicauda and O. farzanpayi, among which the first four species are among most medically important scorpions in Iran that M. eupeus is responsible for most scorpion en- venomation in this province and A. crassi- cauda is considered as most deadly one, our results showed the geographical distribution of medically important scorpions, so this in- formation are useful to produce monovalent antivenom for scorpion sting treatment. Health education programs are implemented by health- care providers in order to prevent the occur- rence of this health problem especially dur- ing the seasonal activity of scorpions in this area. Acknowledgements The authors are grateful to the research deputy of North Khorasan University of Med- ical Sciences. This study was financially sup- ported by North Khorasan University of Med- ical Sciences in Bojnurd, Iran (code No. 94/ P/ 829). 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