Author template for journal articles J Arthropod-Borne Dis, September 2017, 11(3): 371–382 M Mohammadi Bavani et al.: Spatial Distribution of … 371 http://jad.tums.ac.ir Published Online: September 08, 2017 Original Article Spatial Distribution of Medically Important Scorpions in North West of Iran Mulood Mohammadi Bavani 1, *Javad Rafinejad 1, *Ahmad Ali Hanafi-Bojd 1, Mohammad Ali Oshaghi 1, Shahrokh Navidpour 2, Farrokh Dabiri 3, Mehdi Badakhshan 3, Esmaeil Ghorbani 4, Masoomeh Bagheri 3 1Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 2Razi Reference Laboratory of Scorpion Research, Razi Vaccine and Serum Research Institute, Agricultural Research Education and Extension Organization, Karaj, Iran 3Department of Medical Entomology and Vector Control, School of Public Health, Urmia University of Medical Sciences, Urmia, Iran 4Disease Control Unit, Sareyn Health Center, Ardabil University of Medical Sciences, Sareyn, Iran (Received 3 Jan 2017; accepted 29 Aug 2017) Abstract Background: Scorpions are one of the most important medical arthropods in Iran. This study aimed to determine the fauna, spatial distribution and some morphological characteristics of these venomous arthropods in the study area. Methods: Scorpions were collected using Ultra Violet light, rock rolling and digging methods in West Azerbaijan, East Azerbaijan, and Ardabil Provinces during 2015–2016. The specimens were preserved in 75% ethyl alcohol and transferred to the laboratory for species identification and morphological studies. Results: Distribution maps were produced using ArcGIS 10.3. Totally, 368 specimens from two families of Buthidae (97.1%) and Scorpionidae (2.99%) were collected and identified as Mesobuthus eupeus (80.16%), Androctonus crassicauda (10.60%), M. caucasicus (4.89%), Hottentotta saulcyi (1.35%) and Scorpio maurus (2.99%). Conclusion: The presence of medically important species, including the deadly black one in northwestern Iran re- quires health educational and control programs for reduction of these public health problems. Keywords: Scorpions, Distribution, Morphology, GIS, Iran Introduction Scorpions are living fossils, and about 2000 species have been identified in the world sys- tematically classified in different families (1). Among them, Buthidae, with a universal dis- tribution, is the greatest family consisting of 81 genera and 570 species (2). Except for Hemiscorpius lepturus, all dangerous scor- pion species belong to this family (3). Scor- pion stings are a major public health prob- lem in subtropical and tropical countries (4) and some species can be lethal for human. Annually, nearly 1230000 cases of scorpion sting with a fatality rate of 27% are reported in different parts of the world (5). The most medically important species belong to Hotten- totta, Buthus, Tityus, Leiurus, Androctonus, Parabuthus, Centruroides and Mesobuthus genera (6). Scorpions' venom is a complex mixture containing peptides, enzymes, mucoproteins, free amino acids, nucleotides, lipids, amines, heterocyclic components, non-organic salts and low molecular-weight organic molecules. Peptides that affect ion channels including sodium, potassium, calcium and cholera chan- nel are called neurotoxin, and because of their effect on ion channels endanger human health and sometimes results in death (7). Two Iranian dangerous scorpions’ families i.e. Buthi- dae and Hemiscorpiidae have different ef- *Corresponding authors: Dr Javad Rafinejad, E- mail: jrafinejad@yahoo.com, Dr Ahmad Ali Hanafi- Bojd, E-mail: aahanafibojd@tums.ac.ir http://jad.tums.ac.ir/ mailto:jrafinejad@yahoo.com J Arthropod-Borne Dis, September 2017, 11(3): 371–382 M Mohammadi Bavani et al.: Spatial Distribution of … 372 http://jad.tums.ac.ir Published Online: September 08, 2017 fects on human; such that Buthidae species have mostly neurotoxic effect, but Hemiscor- piidae such as Hemiscorpius lepturus (local name: Gadim), causes cell death and hemo- lytic effect cause fatality rate in the country (8, 10). Because of the remarkable diversity in zo- ogeographic zones of Iran, there is a rich ar- thropod’s fauna that includes scorpions. Sev- eral dangerous species inhabit some areas across different parts of Iran, and some of them are lethal for human (11). Scorpion stings cases have been reported as exceeding 42500 annually in Iran, with a fatality rate of 44.7 per 100000. These figures put the country in the second place after Mexico concerning case fatality rate (11, 12). These numbers are not definitive and the actual numbers of scorpion sting and fatality rate are greater than the an- nual recorded figures. Olivier studied the scorpion fauna in Iran and described the black scorpion (Androcto- nus crassicauda) in Kashan City (13(. Since then, several studies have reported 4 fami- lies, 19 genera and 53 species of scorpions in Iran. Buthidae, consisting of 15 genera and 45 species, is the largest family )14, 31(. Mesobuthus eupeus, A. crassicauda, H. lepturus, Odontobuthus doriae, H. saulcyi, Hottentotta schach, Compsobuthus matthies- seni and M. caucasicus are the most medi- cally important species, while A. crassicau- da and H. lepturus are the most dangerous and deadly species to human in Iran )11, 32, 34(. Due to the larger extent and the importance of scorpions in the southern tropical areas of the country, most studies have been per- formed in this area. Therefore, faunistic, mor- phological, spatial distribution and ecologi- cal studies on these toxic arthropods have been neglected in other parts of the country. There is a few information concerning spe- cies composition, geographical distribution and the morphology of scorpions in the north- western corner of Iran. Report of an annual number of 1186 scorpions sting cases in this area )1( encouraged us to design and conduct this study. Therefore, this investigation con- ducted to clarify the current fauna, abundance, geographical distribution and some morpho- logical features of scorpions to provide iden- tification key and its control guideline in this region of the country. Materials and Methods Study area This study was conducted in West Azer- baijan, East Azerbaijan and Ardabil Provinc- es, all in North West part of Iran. These provinces cover an area of about 1007031 km², between 35◦58´–39◦46´N latitudes and 44◦03´–48◦55´E longitudes. They share bor- ders with Armenia and Republic of Azerbai- jan in the north, Kurdish inhabited area in Turkey and Kurdistan regional government in the west, Gilan Province in the east, and Zanjan and Kurdistan Provinces in the south. These provinces include 43 counties with a total population of 8053684 inhabited this area in various weather and environmental conditions. The region has both plains and mountains (Fig. 1). Specimen and data collection Fifty-four locations were selected and the scorpion collection and sampling procedure was carried out from Jun to Aug 2015–2016 during day and night periods using the stand- ard methods, i.e. rock-turning )35( (search- ing under the stones and rock etc.) and UV lights )36(. In addition, to capture burrowing scorpions, pouring water in holes, digging and rubber band technique were used in various scorpions’ habitats. Geographical location, latitude, longitude, altitude (using GPS), environmental temper- ature and relative humidity (using digital ther- mometer and hygrometer) were recorded dur- ing sampling. All samples were preserved in 75% ethyl alcohol and kept in the different http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2017, 11(3): 371–382 M Mohammadi Bavani et al.: Spatial Distribution of … 373 http://jad.tums.ac.ir Published Online: September 08, 2017 labeled plastic boxes according to their lo- calities, and then transferred to the School of Public Health, Tehran University of Medical Sciences, and Tehran, Iran. Morphological identification and analyses such as dentition of the pedipalp chela on movable finger, accessory granules under the terminal denticle on the pedipalp chela mov- able finger (AGMF), rows of denticles on the pedipalp chela movable finger (RDMF), pectinal teeth (PT) were done when observed under stereomicroscope using standard Ira- nian scorpion identification keys )12,14(. ArcGIS 10.3 was used to produce the dis- tribution maps of the collected species. Results In total, 368 scorpions were collected and identified. They belonged to two families, five genera and five species: M. eupeus (80.16%), A. crassicauda (10.60%), M. (Olivierus) cau- casicus (4.89%), S. maurus (2.99%) and H. (Buthotus) saulcyi (1.35%) (Fig. 4). Except for S. maurus (Scorpionidae), other species belonged to the Buthidae family. Table 1 shows the species composition and sex ratio of the scorpions collected from different counties of the study area. Morphological characteristics of scorpions M. eupeus (Fig. 3A). In total, 295 spec- imen (80.16% of the collected samples ( of this species were captured in the 34 localities of all three provinces (West Azerbaijan, East Azerbaijan and Ardabil Provinces), (Fig. 2A). This non-digger species belongs to the family of Buthidae may be regarded as a com- plex species. The variation in color pattern was observed from north to the south so that the northern specimens near the Aras River had darker spots and stripes on their cara- pace and mesosomal segments than others. This species was found in all the three pro- vinces with a wide distribution from Parsabad in the North, to Tekab in the South, and from Urmia in the West to Namin in the East (Fig. 2A). This species was found in different local- ities and habitats with different climates in urban and rural area including under stones and bark, on the farm and plow, near houses, in cemetery, dilapidated homes and grasslands. This species was collected from plains and mountainous area with an altitude range be- tween 188 to 2180m. The sex ratio for this species was 1:1.10 in favor of females. Pectineal teeth (Fig. 4C, F) were between 21/22–30/32 for males and 16/17–23/25 for females; the number of ac- cessory granules under the terminal denticle on the pedipalp chela movable finger (Fig. 5C) was 4 for both sexes but seldom had they 0, 2, 3 and 5 granules. Rows of denticles on the pedipalp chela movable finger (Fig. 4I) were 12–14. A. crassicauda (Fig. 3C). Totally, 39 spec- imen from 9 localities of two provinces (West Azerbaijan and East Azerbaijan) (Fig. 2B) were collected, comprising 10.6% of all captured scorpions. This species inhabited indoors of build- ings and hospitals, under stones, inside soil, sand and cemetery stones in plain and moun- tain areas at an altitude ranging from 690 to 1473m. This is the second most common and deadly scorpion species collected in some coun- ties, but was absent in the Ardabil Province. Pectinal teeth (Fig. 4B, E) were 31/32– 34/35 for males and 23/24–26/27 for females. Rows of denticles on the pedipalp chela mov- able finger (Fig. 4H) were 15–16 for females and 13–16 for males. The sex ratio was 1:0.39 in favor of males. The numbers of granules under the end granule (Fig. 5B) were 3, but sometimes in a few specimens only one was observed, like those of M. eupeus, this is uncommon. M. caucasicus (Fig. 3F). In total, 18 spec- imens (4.89% of all collected samples) of this species were captured in 9 locations of two http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2017, 11(3): 371–382 M Mohammadi Bavani et al.: Spatial Distribution of … 374 http://jad.tums.ac.ir Published Online: September 08, 2017 provinces (West Azerbaijan and East Azer- baijan) (Fig. 2C) in mountainous areas with a height of 690–2180m. This species always seek shelter under stones and inside the wooden roofs of rural houses. Pectinal teeth (Fig. 4A and 4D) and number of rows of denticles on the pedipalp chela movable finger (Fig. 4G) were 26/28– 31/29 and 22/23–23/24 and 11–14 and 12– 13 for males and females, respectively. The sex ratio was 1:0.2 in favor of males. The numbers of granules under the end granule on movable finger (Fig. 5A) were 4 in all specimens. S. maurus (Fig. 3D). This digger species belongs to the family of Scorpionidae and was found only in Givi (Ardabil Province), Mahabad and Miandoab (West Azerbaijan Province) (Fig. 2D) Counties at the heights of 1286, 1404 and 1431m, but this species was not collected from East Azerbaijan Prov- ince. The sex ratio was 1:10 in favor of females. H. saulcyi (Fig. 3E). This species has limited distribution in the region in which it was collected. We collected it only from two sites of Sardasht County, West Azerbaijan Province, at the heights of 1286, 1404 and 1431m (Fig. 2E). This species was not caught in the Ardabil and East Azerbaijan Provinces. Only the females of this taxon were captured. Pectinal teeth (Fig. 5D), the number of dens row on movable finger (Fig. 5E) and granules under the end (Fig. 5F) were 24/25– 26/27 and 14–15, and 4, respectively. Table 1. Species composition and spatial distribution of scorpions collected in northwest of Iran Species Total(N) M. eupeus A. crassicauda M. caucasicus S. maurus H. saulcyi Location M a le (N ) F e m a le (N ) M a le (N ) F e m a le (N ) M a le (N ) F e m a le (N ) M a le (N ) F e m a le (N ) M a le (N ) F e m a le (N ) M a le (N ) F e m a le (N ) Parasad 18 20 - - - - - - - - 18 20 Germi 4 6 - - - - - - - - 4 6 Namin 27 16 - - - - - - - - 27 16 Ardabil 4 8 - - - - - - - - 4 8 Meshkinshahr 17 21 - - - - - - - - 17 21 Givi - - - - - - 1 - - - 1 - Khakhal 3 7 - - - - - - - - 3 7 Khodaafarin 10 14 - - - - - - - - 10 14 Ahar 3 3 - - - - - - - - 3 3 Mianeh 5 8 - - - - - - - - 5 8 Hashtrood 1 - - - - - - - - - 1 - Bonab - - 2 2 1 - - - - - 3 2 Marand 3 - - - 1 - - - - 3 - Jolfa 9 6 2 - 2 - - - - - 13 6 Malakan - - - - 1 - - - - - 1 - Tabriz - - - - 3 1 - - - - 3 1 Maraghe - - 1 - - - - - - - 1 Khoi 2 1 4 2 - - - - - - 6 3 Makoo 2 2 1 1 - - - - - - 4 3 Salmas 3 5 - - 3 1 - - - - 6 6 Urmia 27 36 17 6 3 1 - - - - 47 43 Mahabad - 1 - - - - - 1 - - - 2 Miandoab - - - - 1 - 1 9 2 9 Sardasht - - 1 - - - - - - 5 3 3 Tekab 2 1 - - - - - - - - 2 1 Total 140 155 28 11 15 3 1 10 - 5 186 182 http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2017, 11(3): 371–382 M Mohammadi Bavani et al.: Spatial Distribution of … 375 http://jad.tums.ac.ir Published Online: September 08, 2017 Fig. 1. Study area in north west of Iran http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2017, 11(3): 371–382 M Mohammadi Bavani et al.: Spatial Distribution of … 376 http://jad.tums.ac.ir Published Online: September 08, 2017 Fig. 2. Spatial distribution of collected scorpions from northwestern Iran. (A) Mesobuthus eupeus, (B) Androctonus crassicauda, (C) Mesobuthus Caucasicus, (D) Scorpio maurus, (E) Hottentotta saulcyi. http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2017, 11(3): 371–382 M Mohammadi Bavani et al.: Spatial Distribution of … 377 http://jad.tums.ac.ir Published Online: September 08, 2017 Fig. 3. Collected scorpions’ species form north west of Iran: (A) Mesobuthus euepeus, (B) Hottentotta saulcyi under UV light, (C) Androctonus crassicauda, (D) Scorpio maurus, (E) Hottentotta saulcyi, (F) Mesobuthus caucasicus Fig. 4. Morphological characteristic of medically important collected scorpions from north west of Iran. (A–C) Pectinal teeth of adult male, (A) Mesobuthus caucasicus, (B) Androctonus crassicauda, (C) Mesobuthus eupeus; (D– F) Pectinal teeth of adult female. (D) Mesobuthus caucasicus, (H) Androctonus crassicauda, (F) Mesobuthus eupeus. (G–I) Rows of denticles on the pedipalp chela movable finger. (G) Mesobuthus caucasicus, (H) Androctonus crassicauda, (I) Mesobuthus eupeus http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2017, 11(3): 371–382 M Mohammadi Bavani et al.: Spatial Distribution of … 378 http://jad.tums.ac.ir Published Online: September 08, 2017 Fig. 5. (A–C) Number of accessory granules under the terminal denticle on the pedipalp chela movable finger. (A) Mesobuthus caucasicus, (B) Androctonus crassicauda, (C) Mesobuthus eupeus, (D–F) Hottentotta saulcyi adult female. (D) Pectinal teeth, (E) Rows of denticles on the pedipalp chela movable finger, (C) Number of accessory granules under the terminal denticle on the pedipalp chela movable finger Discussion In this study, 368 specimens were collect- ed comprising five species that include M. eupeus, A. crassicauda, O. caucasicus, S. maurus and H. saulcyi. Buthidae is the larg- est family of scorpions in the world, as well as in Iran, and this species was documented as the largest family of the collected scorpi- ons in this study. Buthidae was the largest family (97.1% of total), and M. eupeus and A. crassicauda are the most medically abun- dant species in the northwestern quarter of the country. Similar to our results, some re- cent investigation have reported Buthidae as the largest family comprising 88.5% of all the species, and A. crassicauda and M. eupeus as the most abundant, medically important spe- cies (32, 37(. The genus Hemiscorpius has the first fa- tality rate in Iran, followed by the genus An- droctonus. Although we could not find any species of the first genus, A. crassicauda was collected from East Azerbaijan and West Azer- baijan. Two cases of death probably from this black deadly scorpion were reported from the study area (38(. Hence, health staffs should be familiar and well educated to know scor- pions' morphology and ecology, educate the community on how to prevent and treat scor- pion’s sting. In our study, the family Buthidae com- prises 97.1% of all collected specimen, among which M. eupeus was the most prevalent and included 80.16% of all specimen, and this species is regarded as the most medically im- portant scorpion species in the region. This is because of the wider geographical distribution of M. eupeus, which accounts for the majority of scorpion envenomation in this part of Iran. This species is considered as most com- mon scorpion in all parts of Iran, including the Northwestern regions, and inhabits areas under stones, tree barks, construction debris, in the roof of old buildings and inside beetle nests (as observed in this study). These spe- cies have about 14 members through its geo- graphical distribution area, and this species can be a complex species (39, 40(. There are six members, however, only one member of the species (Mesobuthus eupeus eupeus) has been reported in our study area) 39(. These studies were limited to one or two counties in the north west of Iran and had not covered the entire area (39(. In comparison, morphological diversity of this species was recognized in our study, at least in coloration pattern, so that the color of northern species near the Aras River was http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2017, 11(3): 371–382 M Mohammadi Bavani et al.: Spatial Distribution of … 379 http://jad.tums.ac.ir Published Online: September 08, 2017 darker (in Carapace and Mesosoma) than those found in the central and southern parts, for examples: Urmia and Tekab. To prove these differences, molecular experiments should be done. The second most prevalent species, A. cras- sicauda, is the most dangerous and deadly scor- pion in Iran, especially the northwestern parts, such that (this study) its sting cause local pain and autonomic stimulation and fatal cardio- vascular problems, particularly in children, and needs special attention because its domestic activity is moving towards human shelters )32(. Other collected species included M. cauca- sicus, H. saulcyi and S. maurus, among them, the first and second are classified as belong- ing to Iranian medically important species. Mesobuthus caucasicus is regarded as the third medically important species due to its wide dispersion and low density in the region. H. saulcyi is considered as the fourth medically important species in the region due to its lim- ited distribution. Studies were conducted in Zanjan Prov- ince that shares long borders with our study area and have collected A. crassicauda, H. saulcyi, Hottentotta zagrosensis, O. doriae, M. eupeus and S. maurus. Among them, four species including M. eupeus, A. crassicauda, H. saulcyi and S. maurus are common be- tween this province and our study region (29(. In addition, in Turkey which have long borders with Western Azerbaijan Province disclosed the presence of L. quinquestriatus, M. gibbosus and M. eupeus of the family Buthi- dae, among which M. eupeus and A. crassi- cauda are common in our study )41, 44(. The polyvalent antivenom in Iran is pro- duced by the Razi Vaccine, Serum, and Re- search Institute against the 6 medically im- portant scorpion species: M. eupeus, A. cras- sicauda, O. and H. saulcyi. Granules under the terminal denticle on the pedipalp chela movable finger were 4 (Fig. 3L) for all specimens, however, many varia- tions were observed in our study. Rows of denticles on the pedipalp chela movable fin- ger (Fig. 3I) were 11, but a range of 12–14 was observed in our study, and these varia- tions show that probably there are more than one types of this species in northwestern prov- inces of Iran. This requires the necessity of molecular experiments to clarify which kind of this species is present in these areas. Only females of H. saulcyi were cap- tured with pectinal teeth of 24/25–26/27, but the female specimen from Turkey and Iraq had 26–28 pectinal teeth and Iranian females' specimens had 27–28. The number of gran- ules on the tip of the movable finger was 3–5 (in Turkey and Iraq specimens), in Iran was 4 and sometimes was absent (45, 46(. How- ever, in our study, all collected specimens had 4 granules and 14–15 rows of denticles on Che- la movable finger. The number of pectinal teeth was inves- tigated to distinguish between the genders of scorpions (46(. The number of pectinal teeth (PT) of A. crassicauda was 30 and 24 in males and females of this scorpion, respectively (47(. These findings were in contrast with our study where PT varied between 31/32–34/35 for males and 23/24–26/27 for females. A study conducted in Zarrindasht Coun- ty, Fars Province of Iran, showed sex ratios (male to female) of S. maurus, M. caucasi- cus and M. eupeus to be 1:5.73, 1:0.31 and 1:0.55, respectively. Similarly, our study rec- orded the sex ratio of M. eupeus and M. cau- casicus in favor of males. Males of captured scorpions were more prevalent than females, but for S. maurus this ratio was in favor of females (1:10) than males (48(. Conclusion There are four medically important scor- pion species including M. eupeus, A. cras- sicauda, M. caucasicus and H. saulcyi in north- western Iran, among them, A. crassicauda is the most deadly scorpion in the study area. Hence, residents should be careful of its sting, http://jad.tums.ac.ir/ J Arthropod-Borne Dis, September 2017, 11(3): 371–382 M Mohammadi Bavani et al.: Spatial Distribution of … 380 http://jad.tums.ac.ir Published Online: September 08, 2017 especially in children. Another medically important, but not dead- ly, species is M. eupeus which inhabited all studied provinces. Species composition and spatial distribution of scorpions, clarified in the northwestern provinces of Iran will be useful to assign the appropriate share of mon- ovalent antivenom to the area and will re- duce the public health problem and mortality due to scorpion sting because of quick ac- cess to treatment. Acknowledgements This article is a part of the dissertation for fulfillment of doctoral degree in Medical Entomology and Vector Control. This study was financially supported by the Research Deputy, Tehran University of Medical Sci- ences (Project No. 31093). The authors' deep gratitude goes to the health staffs of West Azerbaijan, East Azerbaijan and Ardabil Prov- inces for their collaboration and positive ap- petite. Thanks also go out to all the health staffs of selected counties involved in field support for this study. The authors declare that there is no conflict of interest. References 1. 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