J Arthropod-Borne Dis, June 2015, 9(1): 98–103 N Hajipour et al.: Hedgehogs (Erinaceus europaeus) … 98 Original Article Hedgehogs (Erinaceus europaeus) as a Source of Ectoparasites in Urban-suburban Areas of Northwest of Iran Nasser Hajipour 1, Mousa Tavassoli 1, *Tahmineh Gorgani-Firouzjaee 1, Soraya Naem 1, Behzad Pourreza 2, Kia Bahramnejad 1, Jafar Arjmand 1 1Department of Pathobiology, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran 2Department of Clinical Science, Faculty of Veterinary Medicine, Tehran University, Tehran, Iran (Received 29 Dec 2012; accepted 28 June 2014) Abstract Background: Hedgehogs are small, nocturnal mammals which become popular in the world and have important role in transmission of zoonotic agents. Thus, the present study aimed to survey ectoparasite infestation from April 2010 to December 2011 in urban and suburban parts of Urmia and Tabriz Cities, Northwest of Iran. Methods: A total number of 84 hedgehogs (40 females and 44 males) were examined. They have been carefully in- spected for ectoparasites and collected arthropods were stored in 70% ethanol solution. The identification of arthro- pods was carried out using morphological diagnostic keys. Results: The occurrence of ticks on hedgehogs was 23 (67.7%) with Rhipicephalus turanicus in Urmia and 11 (22%) as well as 1(2%) with Rh. turanicus and Hyalomma anatolicum anatolicum in Tabriz, respectively. One flea species, Archaeopsylla erinacei, was found with prevalence of 19 (55.9%) and 27 (54%) in Urmia and Tabriz Cities, respec- tively. Prevalence of infestation with Rh. turanicus and A. erinacei were not different (P> 0.05) between sexes of hedgehogs in two study areas. Highest prevalence of tick and flea infestation was in June in Urmia, whereas it was observed in August in Tabriz. Both tick and flea parasitizing hedgehogs showed seasonal difference in prevalence (P< 0.05) in Urmia, but it was not detected in Tabriz (P> 0.05). Conclusion: The result showed the high occurrence of ectoparasites in hedgehog population and according to the zoonotic potential of these animals as vector of some agents further studies are needed to investigate in different parts of Iran. Keywords: Ectoparasites, Hedgehog, Erinaceus europeus, Tick, Flea Introduction The European hedgehogs Erinaceus europaeus are widespread in rural, suburban and urban environment and have become popular as exotic pets. These animals belong to order Erinaceomorpha, family Erinaceidae and originally arrived from Europe, Asia and Africa (Rilley and Chomel 2005). Hedge- hogs are considered as host of a wide variety of different parasites and pathogens (Keymer et al. 1991, Riley and Chomel 2005). Be- sides, these animals can be a reservoir host for leishmaniasis and trichinellosis in some parts of the world (Yaghoobi-Ershadi and Javadian 1996, Pozio 2007). Hedgehogs can carry several tick and flea species (Beck 2007). Arthropod ectoparasites are a highly adapted group of invertebrates that live on the external body surfaces of animals and humans. Severe infestation with ectoparasites especially ticks can lead to ane- mia and weight loss (Pfaffle et al. 2009). Moreover, these arthropods can act as vec- tors of pathogenic agents, such as borreliasis, rickettsiasis and piroplasmosis, which cause serious diseases in humans and animals (Skuballa et al. 2007, Skuballa et al. 2010, Marie et al. 2012). These mammals are pre- *Corresponding author: Dr Tahmineh Gorgani- Firouzjaee, E-mail: t.gorgani@gmail.com http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 98–103 N Hajipour et al.: Hedgehogs (Erinaceus europaeus) … 99 sented with six species in three genera through- out parts of Iran (Etemad 1984). Several studies have been conducted on parasites of hedgehogs from different part of the world that reveal the high occurrence of parasite including the ectoparasites and endoparasite helminthes (Dziemian et al. 2010, Gaglio et al. 2010, Foldvari et al. 2011, Pfaffle et al. 2011). Few studies have focused on prev- alence of hedgehog infestation in the most parts of Iran (Youssefi et al. 2011). Conse- quently, the present work was performed in order to determine and compare prevalence and intensity of infestation on hedgehogs in Northwest of Iran. Materials and Methods The study was carried out in two cities in northwestern region in Iran. Urmia has semi- humid climate, yearly mean rainfall is of about 350 mm with the maximum mean temperature of 28.3 °C in August and the minimum mean temperature of -5 °C in Jan- uary. Tabriz is arid, its mean rain fall is 330 mm, maximum temperature of 22 32.7 in July and the minimum mean temperature of - 2.8 in December. A total number of 84 hedgehogs (44 males and 40 females) were examined from April 2010 to December 2011 from Urmia (17 females and 17 males) and Tabriz (23 females and 27 males) Cities. For sampling, two study regions were divided to five parts (North, South, West, East and Center) and animals were searched by torchlight during night through parts of study regions espe- cially in grassland, parks and garden areas. Then, animals were captured by hands and maintained in plastic baskets and transferred to Parasitology Laboratory, Faculty of Vet- erinary Medicine, Urmia University, Urmia. About 22 hedgehogs were found dead fol- lowing road accidents and referred to Para- sitology laboratory. All data about sex and weight were recorded. Each individual was visually inspected for ectoparasites, then ar- thropods collected and stored in 70% ethanol solution. Fleas were cleared in 10% potas- sium hydroxide solution and mounted using routine technique. The ectoprasites mor- phologically were examined under the stereo microscope and identified using morpho- logical taxonomic keys (Beaucournu and Launay 1999, Walker et al. 2007). Statistics analysis The following parasitological parameters were evaluated: percentage prevalence, the mean intensity and the mean abundance (Bush et al. 1997). Chi-square and Fisher’s exact tests were used to test for differences in parasite prevalence in the hedgehog pop- ulation. Statistical comparisons were carried out using SPSS 16.0 statistical software. Dif- ferences were considered significant at P< 0.05 level. Results A total number of 37 ticks (23 males and 14 females) and 241 ticks (127 males and 114 females) were collected from hedgehogs in Urmia and Tabriz Cities, respectively. The occurrence of ticks in Urmia on hedgehogs was 23 (67.7%) with Rhipicephalus turanicus and tick infestation in Tabriz was 11 (22%) and 1 (2%) with Rh. turanicus and Hyalomma anatolicun anatolocum, respectively. Other ectoparasite that found was Archaeosylla erinacei with prevalence of 19 (55.9%) and 27 (54%) in Urmia and Tabriz Cities, respec- tively. There were significant differences in female and male ticks and fleas (P< 0.05) that collected from Tabriz but significant dif- ferences was observed only in flea in Urmia. All information about number of infestation with ticks and fleas are shown in Table 1. Prevalence with Rh. turanicus and A. erinacei were not different (P> 0.05) be- tween sexes of animals in two study areas (Table 2). http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 98–103 N Hajipour et al.: Hedgehogs (Erinaceus europaeus) … 100 Highest occurrence of infestation in both tick and flea was in June in Urmia. The sig- nificant variations were observed among seasons in both ectoparasite species (P< 0.05). In region two, highest prevalence of two parasite species was in August (Fig. 1). The significant differences were not seen among season in flea and tick population (P> 0.05). Overall, the intensity of ectoparasite was higher in Urmia than Tabriz in hedge- hog population. Table 1. Prevalence and intensity of ectoparasite species on hedgehogs Study area Parasite species Prevalence (%) Mean intensity (±SD) Mean abundance (±SD) Range Sex ra- tio Urmia Rhipicephalus turanicus Archaeosylla erinacei 23(67.7) 19(55.9) 10.47(±7) 7.78(±7.2) 4.35(±6.6) 7.08(±7.6) 1–25 2–34 1/1.15 1/ 2.52 Tabriz Rhipicephalus turanicus Hyalomma anatolicum anatolicum 11(22) 1(2) 27(54) 3.3(±1.3) 1(±0) 3.6(±1.7) 0.72(±1.5) 0.02(±0.1) 2(±0.2) 1–5 0–1 1–8 1/1.57 - 1/7.6Archaeosylla erinacei Table 2. Prevalence of ectoparasite infestation in relation to sex of the hedgehogs (n= 84) City species Sex of animals Significance Female Male Urmia (n=17) (n=17) P> 0.05Rhipicephalus turanicus Archaeopsylla erinacei 11(64.7) 12(70.6) 10(58.8) 9(52.9) Tabriz (n=23) (n=27) P> 0.05 Rhipicephalus turanicus Archaeopsylla erinacei 5(21.7) 6(26.08) 15(55.5) 12(44.5) Fig. 1. Infestation rate of hedgehog fleas and ticks collected from Urmia and Tabriz Cities, Iran Discussion In the present study, the ectoparasite prev- alence was observed in European hedgehogs (Erinaceus europaeus) in Northwest of Iran. A total number of 37 ticks with the species of Rh. turanicus (67.7%) were identified from Urmia. Of the hedgehogs sampled in Tabriz, 22% and 2% were infested with Rh. turanicus and H. anatolicum anatolicum, respectively. The result revealed that infes- tation rate with ticks was higher than in Urmia. Youssefi et al. (2011) found preva- lence of 75% for Rh. turanicus in hedgehogs (Erinaceus concolor) in north of Iran. At the investigation on identification of tick spe- cies, the presence of Rh. turanicus among ruminants confirmed in two ecologic regions in Iran (Rahbari et al. 2008). Besides in an- other study Rh. turanicus was found in West and East Azerbaijan (Nabian and Rahbari 2008). http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 98–103 N Hajipour et al.: Hedgehogs (Erinaceus europaeus) … 101 Seasonal variation was observed in hedge- hog population in Urmia, but not in Tabriz. The possible reason could be associated with climatic conditions. Rainfall was considered as the most important climatic factor that influenced the seasonal variation in parasite population. According to previous study by Nabian and Rahbari (2008), seasonal activity of ticks has been during the hot and humid months in the Western and Northwestern regions of Iran, which is resulted from several factors including increase of rainfall, temperatures and relative humidity. The re- sults of this study are similar to study carried out by Pfaffle et al. (2011) on tick popula- tions in hedgehogs. Moreover, seasonal var- iation in tick infestation on hedgehog had been shown in urban ecosystem of the city of Poznan, Poland (Dziemian et al. 2010). We observed no significant differences in the abundance of any arthropod between hedgehog sexes. The findings of other stud- ies were in accordance with our study (Gaglio et al. 2010, Pfaffle et al. 2011). Different molecular investigations were conducted on hedgehog ectoparasites which suggested the possibility of transmission of rickettsial agents by arthropods (Matsumoto et al. 2005, Harrus et al. 2010). Marie et al. (2011) showed that European hedgehogs (Erinaceus europeaus) were infested with Rh. sanguineus and Rickettsiae masssiliae was identified from ticks. This pathogen is a causative agent of spotted fever disease in humans. In addition, similar study on African hedgehog (Atelerix algirus) and desert hedgehog (Paraechinus aethiopicus) in Algeria indicated that exam- ined ticks including Rh. sanguineus and Haemaphysalis erinacei were positive for R. masssiliae (Khaldi et al. 2012). Therefore, it was concluded that horizontal transmission of Rickettsia between hedgehog and tick re- sults in hedgehog become potential reservoir host for these emergent pathogens and at this point of view, in environments which there are close communication between human and these animals, the risk factor of infection will increased for humans. Furthermore, Rh. turanicus can act as a vector for Rickettsia, Anaplasma, Theileria, Babesia, and Arbo- viruses (Psaroulaki et al. 2006). Other arthropod species found in our study was A. erinacei with infestation rate of 55.8% and 54% in Urmia and Tabriz Cities, respectively. Highest prevalence was in May to June in Urmia but it was from August to September in Tabriz. There was no data about flea infestation on hedgehogs in Iran. In the Northern white-breasted hedgehog (Erinaceus roumanicus) in urban park of central Budapest, Hungary, 99.4% were in- fected with A. erinacei flea (Foldvari et al. 2011). In an epidemiological survey, which was done on European hedgehogs (Erinaceus europaeus) in Britain, two ectoparasites spe- cies A. erinace (8%) and Ixode s hexagonus (59%) were reported (Gaglio et al. 2010). According to Thamm et al. (2009), investi- gated hedgehogs had infestation with A. aerinacei and I. hexagonus which suggested there were association between ectoparasite infestation and urban environment. Mixed Infestation with A. erinacei and dog flea reported from pet animals and hedgehog in Germany (Visser et al. 2001). Similar to tick that mentioned above, flea have the ability of transmission of Rickettsial agents (Bitam et al. 2006). There was one report about human infestation with A. erinacei in the world (Pomykal et al. 1985). Based on the results, it was concluded that the occurrence of ectoparasites in hedgehog population was high in Urmia and Tabriz Cities and their ability in transmission of infectious agents should be noted. For these reasons, further studies are needed to investi- gate hedgehog ectoparasites in other parts of Iran. Conclusion The result of this investigation showed the http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 98–103 N Hajipour et al.: Hedgehogs (Erinaceus europaeus) … 102 high prevalence ectoparasites in hedgehog population and according to the zoonotic po- tential of these animals as vector of some agents further studies are needed to inves- tigate in different parts of Iran. Acknowledgements The authors would like to appreciate the staffs of Department of Parasitology, Faculty of Veterinary Medicine, Urmia University, for sincere assistance and support of this re- search. The authors declare that there is no conflict of interests. References Beck W (2007) EndoparasitismbeimIgel. Wien Klin Wochenscher. 119(3): 40–44. Beaucournu JC, Launay F (1999) Fleas (Siphonaptera) of France and Western Mediterranean. Paris Federation of Com- panies Sciences, France. Bitam I, Parola P, Dela-Cruz KD, Matsu- moto K, Baziz B, Rolin JM, Belkaid M, Raoult D (2006) First molecular detection of Rrickettsia felis in fleas from Algeria. Am J Trop Med Hyg. 74(4): 532–535. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecol- ogy on its own terms: Margolis et al. revisited. J Parasitol. 83: 45–52. Dziemian S, Pilacinska B, Bogawski P, Michalik J (2010) infestation of the Northern white-breasted hedgehog (Erinaceus roumanicus) with Ixodes ticks in urban ecosystems of the city of Poznan. Wiad Parazytol. 56(5): 41–47. Etemad E(1984) The Mammals of Iran. Chiroptera and Insectivore. Depart- ment of the Environment Press, Iran. Foldvari G, Rigo K, Jablonszky M, Biro G, Molnar V, Toth M (2011) Ticks and the city: Ectoparasite of the northern white-breasted hedgehog (Erinaceus roumanicus) in an urban park. Ticks Tick Borne Dis. 2(4): 231–234. Gaglio G, Allen S, Bowden L, Bryant M, Morgan ER (2010) Parasites of Euro- pean hedgehogs (Erinaceuseuropaeus) in Britain: epidemiological study and coprological test evaluation. Eur J Wild Res. 56: 839–844. Gilles J, Silaghi C, Just FT, Pradel I, Pfister K (2009) Polymeras chain reaction of Rickettsia felis-like organism in Archaeopsylla erinacei (Siphonapetra: Pulicidae) from Bavaria, Germany. J Med Entomol. 46(3): 703–707. Harrus S, Perlman A, Muncuoglu KY, Morick D, Baneth G (2010) Molecular detec- tion of Rickettsia massiliae, Rickettsia sibiricamongolitimonae and Rickettsia conoriiiseaelensis in ticks from Israel. Clin Microbiol Infect. 17(2): 176–179. Keymer IF, Gibson EA, Reynolds DJ (1991) Zoonoses and other findings in hedge- hogs (Erinaceus europaeus): a survey of mortality and review of the litera- ture. Vet Rec. 128(11): 245–249. Khaldi M, Socolovschi C, Benyettou M, Barech G, Biche M, Kernif T, Raoult D, Parola P (2012) Rickettsiae in ar- thropods collected from the north Af- rican hedgehog (Atelerixalgirus) and the desert hedgehog (Paraechinus aethiopicus) in Algeria. Comp Immunol Microbiol Infect Dis. 35(2): 117–122. Marie JL, Davoust B, Socolovschi C, Raoult D, Parola P (2012) Molecular detec- tion of rickettsial agents in ticks and fleas collected from a European hedge- hog (Erinaceus europaeus) in Mar- seilles, France. Comp Immunol Microbiol Infect Dis. 35(1): 77–79. Matsumoto K, Ogawa M, Brouqui P, Raoult D, Parola P (2005) Transmission of Rickettsia massiliae in the tick, Rhipicephalus turanicus. Med Vet Entomol. 19: 263–270. http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 98–103 N Hajipour et al.: Hedgehogs (Erinaceus europaeus) … 103 Nabian S, Rahbari S (2008) Occurrence of soft and hard ticks on ruminants in Zagros Mountainous areas of Iran. Iran J Arthropod-Borne Dis. 2(1): 16–20. Pfäffle M, Petney T, Elgas M, Skuballa Jb, Tarashewski H (2009) Tick induced blood loss leads to regenerative anaemia in the European hedgehog (Erinaceus europaeus). J Parasitol. 136: 443–452. Pfaffle M, Petney T, Skuballa J, Tarashewski H (2011) Comparative population dy- namics of a generalist (Ixodes ricinus) and specialist tick (I. hexagonus) spe- cies from European hedgehogs. Exp Appl Acarol. 54: 151–164. Pfaffle MP (2011) Influence of parasites on fitness parameters of the European hedgehog (Erinaceus europaeus). [PhD dissertation]. Berlin University, Germany. Pomykal J (1985) A case of infestation of humans with fleas Archaeopsylla erinacei (Siphonaptera, Pulicidae). Folia Parasitol. 32(4): 348. Pozio E (2007) World distribution of Trichinella spp. infections in animals and humans. Vet Parasitol. 149: 3–21. Psaroulaki A, Ragiadakou D, Kouris G, Pa- padopoulos B, Chaniotis B, TselentisY (2006) Ticks, tick-borne Rickettsiae, and Coxiella burnetii in the Greek Island of Cephalonia. Ann NY Acad Sci. 1078: 389–399. Rahbari S, Nabian S, Shayan P, Seddighian M (2008) Detection of different spe- cies of Rhipicephalus ticks in some parts of Iran. J Vet Res. 63(4): 195–198. Riley PY, Chomel BB (2005) Hedgehog Zoonoses. Emerg Infect Dis. 11(1): 1–5. Skuballa J, Oehme R, Hartelt K, Petney T, Bucher T, Kimmig P, Taraschewski H (2007) European hedgehogs as hosts for Borrelia spp., Germany. Emerg In- fect Dis. 13(6): 952–953. Skuballa J, Petney T, Pfaffle M, Taraschewski H (2010) Molecular Detection of Anaplasma phagocytophilum in the Eu- ropean hedgehog (Erinaceus europaeus) and its Ticks. Vector-Borne Zoonot. 10(10): 1055–1057. Thamm S, Kalko EKV, Wells K (2009) Ectoparasite infestations of hedgehogs (Erinaceus europaeus) are associated with small-scale landscape structures in an urban–suburban environment. Eco Health. 6: 404–413. Visser M, RehbeiN S, Wiedemann C (2001) Species of flea (Siphonaptera) infest- ing pets and hedgehogs in Germany. J Vet Med. 48: 197–202. Walker AR, Bouattour A, Camicas JL, Es- trada-Pena A, Horak IG, Latif AA, Pegram RG, Preston PM (2007) Ticks of Domestic Animals in Africa: a Guide to Identification of Species. Bi- oscience Reports Scotland, UK. Yaghoobi-Ershadi MR, Javadian E (1996) Epidemiological study of reservoir hosts in an endemic area of zoonotic cutaneous leishmaniasis in Iran. Bull World Health Organ. 74(6): 587–590. Yakhchali M, Hosseine A (2006) Prevalence and ectoparasites fauna of sheep and goats flocks in Urmia suburb, Iran. Veterinarski Arhiv. 76 (5): 431–442. Youssefi MR, RahimiMT, Hosseini SM, Darvishi MM (2011) First report of Rhipicephalus turanicus from hedge- hog (Erinaceus concolor) in north of Iran. World J Zool. 6(4): 401–403. http://jad.tums.ac.ir Published Online: July 16, 2014