PROOF COVER SHEET Journal acronym: TNAH Author(s): Article title: Article no: Enclosures: A. Diakou, E. Kapantaidakis and D. Youlatos Endoparasites of the European ground squirrel (Spermophilus citellus) (Rodentia: Sciuridae) in central Macedonia, Greece 825025 1) Query sheet 2) Article proofs Dear Author, he corresponding c 1. Please check these proofs carefully. It is the responsibility of the author n rmally provided. provid to check these and approve or amend them. A second proof is not normally rs, ev intro Taylor & Francis cannot be held responsible for uncorrected errors, evenn if introduced ve been added to the he article, it during the production process. Once your corrections have will be considered ready for publication. Y u should sh Please limit changes at this stage to the correctionn of errors. You not make ew material, or o delete existing material at insignificant changes, improve prose style, add new essential corrections corr this stage. 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(Please see http://journalauthors.tandf.co.uk/preparation/permission.asp.) Please check that any required acknowledgements have been included to reflect this. AQ1 Journal style puts taxonomic details in title; please confirm that these detailss are correct as inserted here. AQ2 Please confirm that Garmin address is correct as Olathe, KS, USA. AQ3 Please supply a g value for 1500 rpm. AQ4 Please supply a g value for 900 rpm. AQ5 Please supply a g value for 1500 rpm. AQ6 Please confirm that all of these are Entamoeba Eimeria. a and not E meria AQ7 Please insert the genus in full for each speciess to avoid con confusion between Eimeria and Entamoeba. AQ8 Please check the edit made to journal “Çiçek et al. 2010”. rnal ttitle for the reference f AQ9 Please provide cited date for the reference “Duszynski et al. 2001”. AQ10 Please provide missing volume num number for the reference Youlatos et al. 2007. ber fo Journal of Natural History, 2013 Vol. 00, No. 00, 1–12, http://dx.doi.org/10.1080/00222933.2013.825025 RESEARCH ARTICLE Endoparasites of the European ground squirrel (Spermophilus citellus) (Rodentia: Sciuridae) in central Macedonia, Greece AQ1 Q1 A. Diakoua* , E. Kapantaidakisa and D. Youlatosb a Laboratory of Parasitology and Parasitic Diseases, Faculty of Veterinary Medicine, Aristotle Ar University of Thessaloniki, Thessaloniki 54124, Greece; b Department of Zoology, gy, Schoo School of Biology, Aristotle University of Thessaloniki, Thessaloniki 54124, Greece 5 (Received 8 November 2012; final version received 17 April 2013) The European ground squirrel (Spermophilus citellus) is a small smal rodent categocat rized as vulnerable (IUCN). To investigate the parasitic in sitic fauna of this t is species spe Greece, faecal samples from 125 animals belonging to six different populations popu were examined by standard parasitological methods. Parasites Parasit s were found iin 118 of the animals (94.4%). Oocysts of the coccidia Eimeria were found in meria callospermophili callospermop 92 animals (73.6%), Eimeria citelli in 76 (60.8%), 8% Eimeria ia cynomysis c omy in 41 (32.8%), Eimeria spp. (17.6%), Cryptosporidium spp. in of Entamoeba spp. n 29 (23.2%), cysts c in 32 animals (25.6%) and eggs of the trematode atode Brachylaima chyl spp. in seven animals (5.6%). This is the first reportt of Entamoeba Cryptosporidium spp. and eba spp., C Brachylaima spp. in S. citellus. The possible impact of these findings on the health he possib status of S. citellus and the possible to domestic animals or public ossible significance sign health is discussed. 10 15 20 Keywords: Spermophilus us citellus; parasites; pa asites protozoa; trematoda; Greece Introduction The European ground round squirrel squirr or European souslik (Spermophilus citellus) is a small mammal belonging Rodentia and the family Sciuridae. It is a diurnal ing to the order or iving in colonies of individual burrows, usually in short grass open habitats animal, living tufek and V ralik 2005). The European ground squirrel is endemic to central (Kryštufek Vohralik outheastern Euro and southeastern Europe (Figure 1) (Kryštufek 1999; Kryštufek and Vohralik 2005; Ozkurt eett al. 22005), reaching its southernmost range in northern Greece, and has been categoriz categorized as vvulnerable according to the International Union for the Conservation of Natu Nature (Coroiu et al. 2008). Al Although the ecology, morphology and physiology of the European ground squirrel have been adequately studied (e.g. Fraguedakis-Tsolis 1977; Kryštufek 1993, 1995; Huber et al. 1999; Millesi et al. 1999; Hut et al. 2002; Katona et al. 2002; Ozkurt et al. 2002; Hoffmann et al. 2003; Everts et al. 2004; Vaczi et al. 2006; Youlatos et al. 2007), investigations concerning the parasites of this species are scant (Stefanov et al. 2001; Golemansky and Koshev 2007, 2009). However, the role of parasitism in wildlife could be of great importance, especially in peripheral populations that are seriously *Corresponding author. Email: [email protected] © 2013 Taylor & Francis 25 30 35 2 A. Diakou et al. Figure 1. The range of Spermophilus us citellus cit in Europe, Eu according to IUCN. declining. This is the case for the species s in northern Greece, where populations are isolated by intense nse urbanization urbanization and habitat degradation, allowing little or no contact, viously ad ent unit between previously adjacent units. Such units are subject to inbreeding and vulnerine and extinction. extincti able to decline Therefore, their welfare and health are of outmost ance for for their thei protection and conservation. importance In this con xt, th context, the aim of the present study was to investigate the endoparasitic na of different differ fauna populations of S. citellus, for the first time in Greece, to enrich our edge of o the species’ health status and of potential threats to its conservation, as knowledge cons well as to consider any potential consequences of its parasites for domestic animals or h public health. Material and methods Study sites and animals The current study was confined to central Macedonia, Greece, where most of the populations of the species currently occur. For technical reasons, we initially located colonies of S. citellus in areas within the prefecture of Thessaloniki. The colonies 40 45 50 Journal of Natural History 3 Figure 2. The sampling sites tes of Spermophilus Spermoph citellus in central Macedonia, Greece (1: University Agriculture Farm, Army Ve Veterinary Hospital, 3: Axios – eastern coast, 4: arm, 2: C Arm Axios – western mound, 5: Anatoliko, 6: Aggelochori salt pits). Ag were identified byy the presence presenc of characteristic burrow entrances with signs of activd them (freshly excavated exc ity around soil, food remains and droppings). In this way, ntified and sampled six different populations from an equal number of areas we identified from central Macedon Macedonia (Figure 2). These populations were selected mainly because he distance distance between them, as well as natural (e.g. deep rivers, forested areas) and/or the anthropo enic ((e.g. highways, frequently used roads, extended urban areas) barriers anthropogenic assured their di differentiation. The number of sampled burrows per population varied betwe between 5 and 37 (Table 1). 55 60 Faecal samples Faecal samples were collected from the entrances of burrows. All the faecal pellets of a single entrance were considered an individual sample and were collected in a latex glove. As each burrow is used exclusively by one animal, each sample was considered to correspond to a single individual. For every burrow sampled, the exact location was recorded, using a portable GPS (Garmin etrex, Garmin Inc., Olathe, KS, USA). 65 Q2 AQ2 4 A. Diakou et al. Table 1. Spermophilus citellus sampling sites, number of burrows examined from each site and parasites found in each site. Sampling site 1. University Agriculture Farm No. of burrows sampled Parasites 36 Eimeria callospermophili E. citelli E. cynomysis Cryptosporidium spp. 2. C Army Veterinary Hospital 33 E. callospermophili E. citelli E. cynomysiss Cryptosporidium spp. 3. Axios – eastern coast 19 E. callospermophili lospe E. citelli cite i E. cynomysis ynom sis Eimeria spp. spp Entamoeba spp. sp Cryptosporidium spp. Cryp Brachylaima spp. B achyl 4. Axios – western mound 14 E. callospermophili E. E citelli E. cynomysis Eimeria spp Entamoeba spp. Cryptosporidium spp. 5. Anatoliko 188 E. callospermophili E. citelli E. cynomysis Eimeria spp. Entamoeba spp. Cryptosporidium spp. 6. Aggelochori salt pits 5 E. callospermophili Entamoeba spp. AQ7 Q7 Faecal al examination examin All faecal samples were examined using standard parasitological methods, i.e. zinc al sam ota sulphate flotation, Telemann sedimentation and Ziehl–Neelsen-stained smears as described before, with minor modifications (Henriksen and Pohlenz 1981; MAFF 1986; Thienpont et al. 1986). Initially the faecal material of each burrow was well mixed and homogenized. For the zinc sulphate flotation method, approximately 1 g of the homogenized faecal material was diluted with tap water and passed through a sieve (No. 150) in a centrifuge tube. The tube was centrifuged at 1500 rpm for 3 min, then the supernatant fluid was discharged down to approximately 1 cm above the sediment and zinc sulphate (ZnSO4 · 7H2 O) solution 33.2% (weight/volume) was added to the sediment. After thorough dilution of the sediment, zinc sulphate solution was 70 AQ Q 75 AQ3 Journal of Natural History 5 added to just over the top of the tube and a cover slip was placed on the top of the Q AQ4 tube. After centrifugation at 900 rpm for 1 min, the cover slip was carefully removed, 80 AQ placed on a microscope slide and examined under the optical microscope at 100× and 400× magnification. For the Teleman sedimentation method, approximately 1 g of the homogenized faecal material was diluted in HCl 16%, passed through a sieve (No. 150) in a centrifuge tube, 5 ml ether was added and the content of the tube was AQ5 Q homogenized by vigorous shaking. After centrifugation at 1500 rpm for 3 min all the 85 AQ phases of the centrifuged material but the sediment were discharged. Drops of the sediment were examined under the optical microscope at 100× and 400× magnification. For the Ziehl–Neelsen-stained smears, faecal smears were prepared ed on glass slides, fixed by passing over the flame of a Bunsen burner and covered with th carbol– fuchsin solution that was kept warm for 5 min. The smears were then 90 hen decolourized decol with alcohol–acid mixture, rinsed with tap water and finally covered for 1–2 –2 min with Malachite green. After a last rinse with tap water, the smears were allowed to dry rs w 000 ) for the detection det and then examined under the microscope with oil lens (1000×) of Cryptosporidium spp. oocysts. sed on the morphology mo phol The identification of the parasites found was based of their 95 Duszyn reproductive elements in the faeces (Levine and Ivenss 1990; Duszynski et al. 2001; n was feasible feasible to species level for some Haralabidis and Diakou 2001). The identification fication to species sp cies level for all parasites parasites and to genus level for others. Identification ecropsy) or molecular m would require either adult parasites (after necropsy) techniques, both being beyond the scope of the present study. 100 Sporulation of coccidian oocysts ontained unsporulated unspor The faecal samples that contained coccidian oocysts were allowed to morpho ogic characteristics, necessary for identificasporulate to fully develop their morphological at purpose, the th faecal material was left in a solution of 2.5% tion of the species. For that p d (weight/volume) aqueous potassium dichromate (K2 Cr2 O7 ) at room temperature and 105 ay for the completion com l i of the sporulation (Boch and Supperer 1992). checked every day Resultss rasites were found in 118 of the 125 sampled animals (94.4%). Coccidia of the genus Parasites Eimeria were ere detected d in 116 of the animals (92.8%). More precisely, Eimeria callosperw found foun in 92 animals (73.6%), Eimeria citelli in 76 animals (60.8%), Eimeria 110 mophili was cynomy cynomysis in 41 animals (32.8%) and two unidentified species of the genus Eimeria in 22 aanimals (17.6%). In addition, two more protozoan genera were found: cysts of moe spp. in 32 animals (25.6%) and oocysts of Cryptosporidium spp. in 29 aniEntamoeba mals (23.2%). Finally, eggs of the trematode Brachylaima spp. were found in seven animals (5.6%). 115 All the sampled colonies were infected with parasites. Mixed infections with [more than one parasite species were common with various combinations of parasites. The most prevalent was the E. callospermophili and E. citelli co-infection, found in 34 animals (27.2%). The greatest variety of parasites, i.e. E. callospermophili, E. citelli, E. cynomysis, Cryptosporidium spp., Entamoeba spp. and Brachylaima spp., 120 was found in two animals (1.6%). The parasites found in the different sampling areas 6 A. Diakou et al. are presented in Table 1. In 20% of the Eimeria-positive samples, the oocysts were in abundance in the optic field (> 20 oocysts/o.f. in ×100 magnification). Discussion The range of the European ground squirrel is divided by the Carpathian Mountains into two main basins: the Pannonian and the Balkan. The northwestern area of its distribution (Pannonian basin) covers parts of the Czech Republic, Austria, Slovakia, Hungary, northern Serbia, Montenegro and western Romania, while the southeastern area of its range (Balkan basin) extends into parts of southern Serbia, Former rm Yugoslav Republic of Macedonia, northern Greece, Bulgaria, southern Romania, ani Turkish Thrace, Moldova and Ukraine (Panteleyev 1998; Kryštufek 1999). Despite its relatively large range in central, eastern and southern Europe, popuast 10 years, with h lation numbers appear to have rapidly declined by > 30% in the last ssful reintroductio regionally extinct populations in Croatia and Germany and successful reintroductions wed tthat hat most re in Poland (Coroiu et al. 2008). However, Mat˘eju˚ et al. (2010) showed reinen the current popu troduction projects in central Europe had little success. Given population ations could be especially status of the species across Europe and its range, Greek populations important, as they are found at the periphery of the southern bord border of the range of ne in this area too oo ((Youlatos 2009). the species, and there is evidence of population decline Therefore, the health of these peripheral populations is fundamen fundamental for their survival, as well as for future action plans on protection and conservation of the species across tly rrelated to the hea Europe. In this context, parasitism is directly health of established populations and therefore, identifying and evaluating the parasitic load is important in understanding the health robustness of a given po population. luatin parasitism in wild animals: (1) the There are three main points when eva evaluating asites on the animal nim its self, (2) the importance of these effect and importance of the parasites nd, (3) the pos parasites to domestic animals and, possible impact on public health (Choquette mals, p arasites are aalmost always present but apparently in 1956). In free-living animals, parasites ittle damag e. Howev most cases are doing little damage. However, under certain circumstances the host– an be distur parasite relationship can disturbed and then a clinical condition develops. Such ay b circumstances may be malnutrition malnutrition, extreme weather conditions and co-existence of ns. In ca es of vulne other pathogens. cases vulnerable or threatened animal populations, the role of comes even mo parasites becomes more significant. esent study, the most prevalent parasites of S. citellus were the coccidian In thee pr present zoa of the the genus gen Eimeria (92.8%). The high percentage found in Greece is protozoa h th in accordance with the results of previous similar studies. In the Czech Republic and Slovakia coccidian oocyst were found in all (100%) of the examined European ground squir squirrels (Kviˇcerová 2008). In Bulgaria, Eimeria infection was found in 88.05% of S S. citellus, with the most prevalent species being E. citelli (92.7%) and E. callospermophili (66.6%) (Golemansky and Koshev 2009). Levine and Ivens (1990) described 19 species of Eimeria in Spermophilus spp. Of these species, E. callospermophili seems to be particularly common for the genus. Apart from S. citellus, this parasite has been reported in Spermophilus xanthophrymnus in Turkey (Çiçek et al. 2010), in Spermophilus richardsonii, Spermophilus townsendii, Spermophilus lateralis and Spermophilus elegans in North America (Stanton et al. 1992; Seville and Stanton 1993; Wilber et al. 1994) and in Spermophilus parryii in Alaska and Siberia (Seville et al. 2005). 125 130 135 140 145 150 155 160 165 Journal of Natural History 7 The identification and taxonomy of Eimeria spp. has traditionally been based on the morphology of the sporulated oocyst and the host where the examined species is found (Levine and Ivens 1990). In the present study, apart from the three identified Eimeria species, two more types of oocysts with different morphologies were detected in 22 animals. Unfortunately, the number of morphological characteristics of Eimeria spp. is limited whereas the number of species is large (Motriuk-Smith et al. 2011). Development and application of molecular methods for the precise identification of these parasites are planned and would solve this problem. Eimeria is a protozoan parasite with a direct life cycle that invades the epithelial cells of the small and large intestine where it reproduces. There are no dat data in the literature about the pathogenicity of Eimeria in European ground squirrels. Ge Generally, coccidiosis in sciurids seems to cause few or no clinical signs (Joseph 1975; Coh Cohn et al. ulgaris) signs 1986; Sainsbury and Gurnell 1995). However, in red squirrels (Sciurus vulgaris) nd eeven a fatal outcome utco such as loss of general condition, loss of appetite, diarrhoea and have been reported (Pellerdy 1954, 1974). nfecti n has not been b The immune response of Spermophilus spp. to Eimeria infection clarbot the parasite p ified. There is evidence that immunity depends on the species of both and d more than ad the host. Moreover, the fact that juveniles are infected adults due to ageer et al. 1994). 1994) However, Golemansky developed immunity has not been proven (Wilber th E. callospermophili callospermop and Koshev (2009) found heavier infection with and E. cynomysis ( in subadult and juvenile S. citellus and Seville and Stanton (1993) found greater variety an in adults. Taking into consideration, of Eimeria species in juvenile S. richardsonii than an heavy infectio on the one hand, the high prevalencee and infection with Eimeria spp. found in er hand, the t potential pathogenicity of the parasite the present study, and on the other ulations of o S. citellus in Greece, it can be suggested and the evidence of declining populations resent a threat threa for ground squirrels and a risk for the stathat this infection could represent n the study area. rea. More investigations towards this end are bility of the populations in p currently underway, as thiss may affect populations of the species that inhabit generally n central cen ral Greece. favourable habitats in ium is another anoth her genus of the subclass Coccidia. It has a direct life cycle Cryptosporidium omes infected by ingestion or inhalation of the oocysts found in food, and the host becomes e vironment in general. It is a parasite of the epithelial cells of the gaswater and thee environment inal tract trac (less comm trointestinal commonly of the respiratory tract) and is an important cause trointestinal illness ill of gastrointestinal for humans and animals (Dubey et al. 1990). Without having ict host host specificity, Cryptosporidium species are recognized to differ principally in strict hos range rang but some genotypes are considered zoonotic (Hunter and Thompson their host 2005). t present study, Cryptosporidium spp. was found in 23.2% of the examined aniIn the als. To T the authors’ best knowledge, this is the first report of this parasite in S. citellus. mals. eve 35.5% of the S. suslicus examined by direct immunofluorescence assay in However, Poland were shedding Cryptosporidium oocysts (Kloch and Bajer 2012). Moreover, Cryptosporidium parvum has been found in 16% of the Spermophilus beecheyi examined in California (USA), where two different genotypes were circulating within a single host population (Atwill et al. 2001). In a more recent survey, the parasite was found in two more Spermophilus species (Spermophilus beldingi and Spermophilus lateralis) in California and the phylogenetic analyses of the isolates revealed that Spermophilus squirrels shed novel Cryptosporidium species (Pereira et al. 2010). As cross-species transmission of Cryptosporidium spp. is a fact (Monis and Thompson 2003), molecular 170 175 180 185 190 195 200 205 210 215 8 A. Diakou et al. characterization of isolates of this parasite would be useful in the investigation of the possible transmission of the S. citellus genotypes to other animal species or humans. Entamoeba is also a protozoan parasite with a direct life cycle. It parasitizes the intestines of animals and humans and includes non-pathogenic and pathogenic species. The reports of Entamoeba infection in sciurids are scant. The species reported in Spermophilus are Entamoeba muris and Entamoeba citelli. The cystic form of Entamoeba citelli (Becker 1926) is about 15 μm in diameter with eight nuclei and a thick cystic wall. In the present study, the Entamoeba sp. cysts, found in morphologically good condition in very dry faeces, had all the characteristics described at for Entamoeba citelli. This parasite has been also reported in S. tridecemlineatus, 987 S. townsendii, S. beldingi and S. lateralis (Becker 1926; Davis 1969; Rickard 1987), o the healt and this is the first report for S. citellus. The significance of this parasite to health status of the sciurids is not known, as there are no relative published data. Brachylaima is a trematode parasite of the intestines of mammalss an and birds. It has d in termediate ho an indirect life cycle with land snails and slugs as first and second intermediate hosts ously repor (Yamaguti 1958; Butcher 2003). This parasitic trematode has been previ previously reported tulus (López-D arias et al. from two species of the family Sciuridae, Atlantoxerus getulus (López-Darias ledge, this repo 2008) and Sciurus carolinensis (Kennedy 1988). To our knowledge, report is a new ection is rrelated elate to the fact that host record for Brachylaima spp. This trematode infection 008), which aactt as an intermediate S. citellus often feeds on land snails (Coroiu et al. 2008), host. This parasite was found only in Axios – eastern coast (site N No. 3; Figure 2), where ggs of this pa seven of the 19 examined animals (36.8%) excreted eggs parasite in their faeces. logy of the parasite arasite iis beyond the aim of the Although the investigation of the epizootiology n was limited limi present study, the fact that this infection to only one population is interesting. This isolated occurrence could bee due to incidental infection of the particular ransmiss on b population, failure of infection transmission because of short dispersal movements, bers of snail and/or predation of higher numbers snails acti acting as intermediate hosts (Helicidae) ampling sites. Since the species B. criibi has been incicompared with the rest of the sampling mans, iin n Australia (B dentally identified in humans, (Butcher and Grove 2001), its presence in ons relate the site requires furtherr investigatio investigations related to human health. The small number of helminth parasites found in S. citellus is consistent with the rids, which in general findings in sc sciurids, indicate that this family is parasitized at a lower level than predicted (Moran (Morand and Poulin 1998). Moreover, the relatively limited variation of the parasiticc fauna found iin the present study could be attributed to the fact that our tricted to non-i study wass re restricted non-invasive faecal examination. Eventually, necropsies would asitic species, but euthanasia is not an option, because of the vulnerable reveal more pa parasitic us o status of S. ci citellus.. R Reports of helminth parasites in S. citellus are scant. Stefanov et al. (2001) reported four helminth species, the cestodes Hymenolepis magaloon and enia m Ctenotaenia marmotae and the nematodes Streptopharus kutasii and Trichostrongylus is from Bulgaria. colubriformis, Despite the asocial behaviour of S. citellus, transmission of parasites is facilitated between individuals due to the density of the colonies, which was relatively high in all the sampled sites. Furthermore, the resistance of the reproductive elements of the parasites to the environmental conditions is also a factor that contributes to the infection of the animals. In Greece, S. citellus inhabits low vegetation, relatively dry habitats that are exposed to intense heat and solar radiation, especially during summer months. Under such conditions, particularly resistant helminth eggs and protozoan cysts and 220 Q6 AQ6 225 230 235 240 245 250 255 260 Journal of Natural History 9 oocysts are vital for their survival. This may explain the very good condition of the parasitic elements found in the present study, despite the dry faeces often examined. This study provides the first report on the parasitic fauna for S. citellus in Greece. 265 The high prevalence and in some cases heavy infection of the animals with Eimeria should be further investigated to evaluate the significance of the specific parasite to the population health status and conservation. Close monitoring of the animals and regular parasitological examinations would provide additional information towards this end. The species of Eimeria and most probably Entamoeba reported in this study 270 are exclusive parasites of sciurids. In this way, no expected risk for domestic animals ra and public health exists. On the other hand, Cryptosporidium spp. and Brachylaima pin of the spp. may possibly affect other animals and humans. In every case, genotyping parasites found in S. citellus would provide data for more accurate identificat identification and ecies de would facilitate the investigation of any probable genetic relation to species derived 275 e, ssimilar investigations gati from other wild or domestic animals and humans. Furthermore, on hosts that share the same habitats with S. citellus would be necessary for any conllus iin Greece an sideration of actions plans for the conservation of S. citellus and across Europe. Acknowledgements We are particularly grateful to Col. K. Terpsidis and nd Lt Col. G. Emmanouil for granting permission to work in the area of the C Army Veterinary yV ry Hospital. We also express our gratitude to the Managing Authority of the Axios Delta for granting os D ti permission to work in the Area under their supervision. Great thankss go to S. Vareltzidou, L. Albanou and L.M. Rammou for Va working together in the field. 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