J Arthropod-Borne Dis, March 2017, 11(1): 36–41 Z Zarei et al.: Wild Rodent Ectoparasites … 36 http://jad.tums.ac.ir Published Online: March 14, 2017 Original Article Wild Rodent Ectoparasites Collected from Northwestern Iran Zabihollah Zarei 1, Mehdi Mohebali 1,2, Zahra Heidari 1, Eshrat Beigom Kia 1, Amrollah Azarm 3, Hasan Bakhshi 4, Jaber Davoodi 5, Hamid Hassanpour 1, Manizhe Roohnavaz 1, Mahya Khodabakhsh 6, *Zakkyeh Telmadarraiy 7 1Department of Medical Parasitology and Mycology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 2Centers for Research of Endemic Parasites of Iran (CREPI), Tehran University of Medical Sciences, Tehran, Iran 3Department of Medical Entomology and Vector Control, Faculty of Medical Sciences, University of Tarbiat Modarres, Tehran, Iran 4Malaria and Vector Research Group, Biotechnology Research Center, Pasteur Institute of Iran, Tehran, Iran 5Department of Veterinary Parasitology, Islamic Azad University Abhar Branch, Abhar, Iran 6Department of Veterinary Internal Diseases, Faculty of Veterinary Medicine, Tehran University, Tehran, Iran 7Department of Medical Entomology and Vector Control, Tehran University of Medical Sciences, Tehran, Iran (Received 28 July 2015; accepted 7 Feb 2016) Abstract Background: Rodents play an important role as reservoir of some pathogens, and the host of some ectoparasites as well. These ectoparasites can transmit rodents’ pathogens to human or animals. The aim of this study was to assess the distribution and infestation load of ectoparasites on rodents in Meshkin-Shahr District, northwestern Iran. Method: Rodents were captured using baited live traps in spring 2014 from Meshkin-Shahr District and were trans- ferred to the laboratory for identification to the species level. Their ectoparasites were collected, mounted and identi- fied. Results: Three rodent species including Meriones persicus (74%), Mus musculus (16.9%) and Cricetulus migrato- rius (9%) were identified. Among all rodents, 185 specimens (90.69%) were infested with a total of 521 ectopara- sites. Overall, 10 arthropods species were collected, including fleas (97.6%), one mite (1.6%) and one louse species (0.6%) as follows: Xenopsylla nubica, X. astia, X. buxtoni, X. cheopis, Nosopsyllus fasciatus, N. iranus, Cten- ocephalides felis, Ctenophthalmus rettigismiti, Ornithonyssus sp and one species of genus Polyplax. The most prev- alent ectoparasites species was X. nubica (89%). Conclusion: Nearly all rodent species were infested with Xenopsylla species. Monitoring of ectoparasites on infested rodents is very important for awareness and early warning towards control of arthropod-borne diseases. Keywords: Rodent, Ectoparasites, Iran Introduction Rodents play important roles in disease transmission via their urine, feces, bite and transmission of pathogenic agents through ec- toparasites (Williams et al. 1997). Some viral, bacterial and protozoal agents as well as hel- minthes resulting in leishmaniasis, Crimean- Congo Haemorrhagic Fever (CCHF), plague, leptospirosis, salmonellosis, rat-bite fever, Omsk hemorrhagic fever, anaplasmosis, ehr- lichiosis, murine typhus, theileriosis and babesi- osis can be transmitted by rodents to other an- imals orhumans when they are in close con- tact (Williams et al. 1997, Tsuji et al. 2001, Motevalli-Hagghi et al. 2002, Telmadarraiy et al. 2007, Kia et al. 2009, Tajedin et al. 2009, Eisen and Gage 2012, Nateghpour et *Corresponding author: Dr Zakkyeh Telmadarraiy, E-mail: ztelma@yahoo.co.in, telmadarraiy@tums. ac.ir J Arthropod-Borne Dis, March 2017, 11(1): 36–41 Z Zarei et al.: Wild Rodent Ectoparasites … 37 http://jad.tums.ac.ir Published Online: March 14, 2017 al. 2013). Fleas (Siphonaptera) and Ixodid ticks (Acari: Ixodidae) are the major vectors of important pathogens threatening human and animals (Goz et al. 2016). Some ectoparasites of medical and vet- erinary importance were found and reported from rodents in different parts of Iran (Mohe- bali et al. 1997, Kia et al. 2001, Telmadar- raiy et al. 2004, Shayan and Rafinejad 2006, Hanafi-Bojd et al. 2007, Telmadarraiy et al. 2007, Sharifi et al. 2008, Shoorijeh et al. 2008, Kia et al. 2009, Tajedin et al. 2009, Nateghpour et al. 2013, Zendehfili et al. 2014, Telmadarraiy et al. 2015). In those studies some rodents species such as Meriones lybi- cus, M. persicus, M. hurrianae, Tateraindica, Mus musculus, Rattus rattus, R. norvegicus, Nesokia indica, Microtus socialis, Gerbillus nanus, Glis glis, Apodemus sylvaticus and soon were studies and the ectoparasite spe- cies were included Pulex irritans, Xenopsyl- la cheopis, X. astia, X. buxtoni, X. nubica, X. conformis, Nosopsyllus medus, N. fasciatus, Polyplaxs pinulosa, P. gerbilli, Rhipicepha- lus sp, Hyalomma sp, Boophilus sp, Laelaps nuttalli, L. ciccuminata, And rolaelaps her- maphrodita, Paracheylaelaps pyriformis, Der- manysus sanguineus, D. americanus, Orni- thonyssus bacoti, Haplopleura captiosa, Hae- molaelaps glasgowi, Echinolaelaps echidni- nusand some other species. Because of high climatic diversity in Iran and numerous ecological niches of rodents, there is a considerable potential for survey on their ectoparasites to find the vulnerabil- ity of vector-borne zoonoses in the country. There was no comprehensive study on the rodent and their ectoparasites in northwest of Iran. Therefore, the aim of this study was to assess the distribution and infestation level of ectoparasites on rodents in selected sites in Meshkin-Shahr County located in northwest of the country. This will help us in monitoring ectoparasites infestation to alerting and early warning to possibility for control of arthropod- borne diseases in northwestern part of Iran. Materials and Methods Study area Meshkin-Shahr County (38° 26′N 47° 45′E) is one of the counties located in Ardebil Prov- ince (Fig. 1). The province is considered the coldest province in Iran. Large parts of the province are forested and green. Neighbor- ing the Caspian Sea and the Republic of Azerbaijan, the province is of great econom- ic significance as well as splendid natural beauty and numerous sights. Meshkin-Shahr County is located at an elevation of 1,341 meters above sea level, the whole district occupying the foot-hills of Sabalan Moun- tain. The weather is extremely cold in the winter (down to -27 °C) and warm during the summer (up to 40 °C). Many tourists come to the region for its cool climate. Rodent collection Rodents were live trapped at different lo- calities including Altisiluo, Khiav, Abiz, Our, Oudkandi and Magandeh. Rodent’s collec- tion was carried out on various occasions and different places like indoor places, farms, roadsides and other places in spring 2014. Live traps were randomly set in different afore- mentioned habitats baiting with favorable food of rodents according to the season. These traps were set at different parts of selected regions of the district from 11:00 AM to the next day. Ectoparasites collection Captured rodents were transported rapidly to the laboratory of Meshkin-Shahr Research Station and their ectoparasites were isolated using brushing on the fur or by a fine forceps immediately after transporting. Collected ec- toparasites were stored in 70% ethanol for preservation and identification. Rodents and ectoparasites identification Different morphological criteria were used for identification of rodents in the species lev- J Arthropod-Borne Dis, March 2017, 11(1): 36–41 Z Zarei et al.: Wild Rodent Ectoparasites … 38 http://jad.tums.ac.ir Published Online: March 14, 2017 el by preparation of rodent skulls, mounting of ectoparasites, identification of rodents (Etemad 1976) and ectoparasites (Strandt- mann and Wharton 1958). Ectoparasites spec- imens were fixed in between microscope slides and cover glass and confirmation of some species was carried out according to standard methods provided. Results A total of 204 rodents were identified in 3 species including Meriones persicus (74%), Mus musculus (16.9%), and Cricetulus migra- torius (9%). Among them, 185 (90.69%) were infested with 521 ectoparasites. The ectopar- asites of the rodents were comprised mites, fleas and lice (Fig. 2). Totally, 10 species were captured in this study including eight fleas (97.6%), one mite (1.6%) and one species of genus Polyplax (0.6%) species as follows: X. nubica, X. astia, X. buxtoni, X. cheopis, Nosopsyllus fasciatus, N. iranus, Ctenocephalides felis, Ctenoph- thalmus rettigismiti, Ornithonyssus sp, and Polyplax sp (Table 1). Table 1. Details of collected ectoparasites from caught rodents. These ectoparasites were collected in spring 2014 from Meshkin-Shahr District located in northwest part of Iran (%)TotalTotalFemaleMaleEctoparasites 89465134331Xenopsylla nubica 21138X. astia 2.41275Nosopsyllus fasciatus 0.4211Xenopsylla buxtoni 1.91028Xenopsylla cheopis 0.6321Ctenocephalides felis 0.9431Nosopsyllus iranus 0.6321Ctenophthalmus rettigi smiti 1.6835Ornithonyssus sp 0.6312Polyplax sp Fig 1. Location of Ardebil Province. This province is located in Northwest part of Iran and is bordered with Republic of Azerbaijan. Meshkin-Shahr County is one of the counties of the province. Fig 2. Some collected ectoparasites; A: Xenopsylla nubica, B: X. nubica, C: Nosopsyllus fasciatus, D: Ctenocephalides felis, E: X. cheopis, F: X. astia, G: Ctenophthalmus rettigismiti, H and I: N. iranus J Arthropod-Borne Dis, March 2017, 11(1): 36–41 Z Zarei et al.: Wild Rodent Ectoparasites … 39 http://jad.tums.ac.ir Published Online: March 14, 2017 Discussion In the present investigation, three rodent species including Meriones persicus, Mus musculus and Cricetulus migratorius were caught in Meshkin-Shahr District located in Ardebil Province, northwest of Iran during spring 2014. Study on these rodents is essential as they have an important role as host of many para- sitic agents (Darvish et al. 2015). Out of 204 collected rodents, M. persicus was the most prevalent species in that area (74%). In the former investigations, occurrence of this ro- dent has been revealed in Central Asia, Trans- caucasia, Turkey and Pakistan (Carleton and Musser 2005). Moreover, in northwest of Iran, this species was found in Maku and Urumiyeh located in West Azerbaijan Prov- ince as well as Jolfa located in East Azerbai- jan Province (Lay 1967). In a recent inves- tigation in northwest part of Iran, this spe- cies has been found in Kordasht, Sufian and Tabriz (East Azerbaijan Province) as well Zanjan County in Zanjan Province (Darvish et al. 2015). This species is introduced as a probable reservoir for visceral leishmaniasis in Iran (Shojaei and Mohebali 2005). The presence of this species in Meshkin-Shahr District is consistent with the above men- tioned investigations. Furthermore, we could find Mus musculus in our investigation. This species has been found in almost all parts of the country (Etemad 1976). Another species C. migratorius, has been captured in Mesh- kin-Shahr and reported with high titers of Leishmania antibody in Meshkin-Shahr (Mohe- bali et al. 1995, 1997). Ectoparasites play an important role in transmitting some diseases to human and do- mestic animals (Williams et al. 1997, Eisen and Gage 2012). Therefore, study on ecto- parasites will help investigators to evaluate the possibility of pathogens transmission in a given area. In this study, the most prevalent (89%) ec- toparasite was X. nubica. This species has been introduced as the vector of plague in Mauritania (Eisen and Gage 2012). Among other flea species collected in this study X. astia, X. buxtoni, X. cheopis and N. fasciatus are introduced as the vectors of plague in Southeast Asia and the Western Pacific, Iran, Libya, Mauritania, East Africa, Southern Af- rica and South America (Eisen and Gage 2012). In Meshkin-Shahr County, M. persicus was the dominant rodent species, while 7 species of ectoparasites were identified as: X. ger- billi, X. nuttalli, N. fasciatus, Stenopnia tripecti- nata, Ornitonyssus bacoti, Trichoecius rom- boutsi and Haemaphysalis sp. (Mohebali et al. 1997). Comparing with their study we could not capture Alactage elater rodent species, while the common ectoparasite in both stud- ies is N. fasciatus. In another study in Germi, Ardebil Prov- ince, two species of rodents were trapped: M. persicus and Microtus socialis with the frequency of 90.4% and 9.6%, respectively (Kia et al. 2010). The frequency of M. persi- cus is in concordance with our result. Alt- hough we did not find M. socialis in the pre- sent investigation, but two other species, i.e., C. migratorius and M. musculus species were trapped in our study. Other investigations carried out in west of Iran reported some ectoparasite including Pulex irritans, X. buxtoni, Nosopsyllus me- dus, Polyplax spinolosa, Rhipicephalus sp, Hyalomma sp, Lealaps nuttalli, Dermanysus sanguineus and Ornithonussus bacoti (Telma- darraiy et al. 2007). The difference between this study with our investigation may be due to the host and climate. The importance of ectoparasites has encouraged investigators to study on other animals like hedgehogs (Goz et al. 2016). In a most recent investigation carried out on 21 hedgehogs ectoparasites in east part of Turkey (northwest of Iran), R. turanicus and A. erinacei were detected, also, J Arthropod-Borne Dis, March 2017, 11(1): 36–41 Z Zarei et al.: Wild Rodent Ectoparasites … 40 http://jad.tums.ac.ir Published Online: March 14, 2017 infestation rate for ticks and fleas was detect- ed as 66.6% and 100%, respectively (Goz et al. 2016). We could not collect these ecto- parasites on the caught rodents. This is ex- pected to be so, because A. erinacei is the ectoparasite of hedgehogs, cats and dogs (Pomycal 1985). Conclusion Five flea species identified in this study are introduced as the vectors of plague in different foci of the disease around the world, so it is recommended to do a sero- logical study for plague in rodents and their ectoparasite in this area. 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