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Review

Helminths of Erinaceus roumanicus (Eulipotyphla, Erinaceidae) in Mordovia (Russia) with an Overview of Helminth Fauna of Erinaceus spp. Inhabiting the Palaearctic Region

by
Alexander A. Kirillov
1,
Nadezhda Yu. Kirillova
1 and
Alexander B. Ruchin
2,*
1
Samara Federal Research Scientific Center RAS, Institute of Ecology of Volga River Basin RAS, 10 Komzina Street, 445003 Togliatti, Russia
2
Joint Directorate of the Mordovia State Nature Reserve and National Park “Smolny”, 30 Krasnaya Street, 430005 Saransk, Russia
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(3), 165; https://doi.org/10.3390/d14030165
Submission received: 3 February 2022 / Revised: 22 February 2022 / Accepted: 23 February 2022 / Published: 25 February 2022
(This article belongs to the Special Issue Diversity in 2022)
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Abstract

:
The helminth fauna of the Northern white-breasted hedgehog Erinaceus roumanicus was studied in the Republic of Mordovia (Russia) for the first time. In total, 9 species of helminths were found in 23 studied hedgehogs: Trematoda—Isthmiophora melis, Strigea strigis (metacercaria); Cestoda—Hymenolepis erinacei; Nematoda—Aonchotheca erinacei, Physaloptera clausa, Crenosoma striatum, Physocephalus sexalatus (juvenile), Agamospirura minuta (juvenile); and Acanthocephala—Nephridiorhynchus major. Four parasite species (the trematode I. melis, nematodes P. sexalatus, A. minuta, and the acanthocephalan N. major) were found in hedgehogs for the first time in Russia. An overview of the helminth fauna of four species of Erinaceus hedgehogs inhabiting the Palearctic region is given. A total of 54 parasite species were recorded across Erinaceus europaeus, E. roumanicus, E. concolor and E. amurensis: 14 trematodes, 6 cestodes, 27 nematodes, and 7 acanthocephalans. Among all the studied species of hedgehogs, E. europaeus (35 species) and E. roumanicus (36) have the richest helminth faunas. The diversity of the parasite communities of Erinaceus spp. is due to the wide distribution and varied diet of these mammals. Most of the helminths found in hedgehogs are transmitted along trophic chains. Hedgehogs are the final hosts for 39 species of parasites. For 15 helminth species, Erinaceus spp. are paratenic hosts. The majority of the hedgehog’s helminth fauna is formed by host-specific parasites, of which there are 13 species. Most of the hedgehog’s parasites in the Palaearctic are facultative (non-specific) species that parasitize in various vertebrate species. The helminth fauna of Erinaceus hedgehogs is most studied in Russia and Belarus, where 17 species of parasites are found in each country. The comparative analysis of the helminth faunas of Erinaceus spp. from various regions showed, on the one hand, the originality of the helminth fauna of each hedgehog species and, on the other, the similarity of the helminth fauna of these insectivores from various countries of the Palaearctic. These features are caused by similar lifestyles and diet peculiarities of every hedgehog species in various regions of the Palaearctic. A total of 12 of the 54 helminth species found in hedgehogs have medical and veterinary significance as causative agents of dangerous helminthiasis.

1. Introduction

Small terrestrial mammals, such as the Eulipotyphla and Rodentia, are important elements of ecosystems due to their high species diversity, fitness, and diet specializations. This animal group, due to its high abundance and wide distribution, is an integral part of any semi-aquatic or terrestrial biocenosis and it is of great practical importance [1,2,3,4,5]. Small wild animals are the main forage resource for predatory mammals, birds of prey, and some reptiles (mainly snakes) [6,7,8]. Small mammals are of great importance in rural environments as many are a source of parasites and some diseases of domestic animals and livestock [9,10,11,12,13,14].
Among Eulipotyphla, the Erinaceinae subfamily containing the well-known hedgehogs of Eurasia and Africa deserves special attention [15]. Hedgehogs are nocturnal and spend most of their active time foraging [16,17]. These omnivores have ecological plasticity that allows them to inhabit various biotopes. They are present in many habitat types (habitats) if their primary forage (invertebrates) and suitable nest sites are sufficiently available [18]. Hedgehogs are often found in urban and suburban environments [17].
Hedgehogs of the Erinaceidae family are widespread in the Palaearctic. Currently, four hedgehog species of the genus Erinaceus are known: Erinaceus europaeus Linnaeus 1758, Erinaceus roumanicus Barrett-Hamilton, 1900, Erinaceus concolor Martin, 1837 and Erinaceus amurensis Schrenk, 1858. Erinaceus roumanicus has only recently been defined as a valid species [15]. Three hedgehog species inhabit Western Palaearctic: E. europaeus, E. roumanicus, and E. concolor [19]. The Western European hedgehog E. europaeus inhabits the forest areas of Western and Central Europe (including the British Isles), Southern Fennoscandia, Estonia, and the north and central regions of European Russia [20,21,22,23,24,25].
The Northern white-breasted hedgehog E. roumanicus inhabits Central and Eastern Europe, the south of Western Siberia and the North Caucasus. Erinaceus roumanicus and E. europaeus are sympatric in central Europe (the Balkans, Poland, the Czech Republic, and Slovakia) and central regions of European Russia [22,23,25]. The northern border of the species range in Russia is at the level of 56° north latitude; in the south it is distributed to the Caucasus [25].
The Southern white-breasted hedgehog E. concolor is found in the Middle East, isolated from E. roumanicus by the Bosphorus Strait and the Caucasus Mountains [22,23]. Until recent times, E. roumanicus was considered to belong either to E. europaeus or to E. concolor, and it has only recently been identified as a valid species [18].
The only Erinaceus species inhabiting the Eastern Palearctic is the Amur hedgehog E. amurensis. Its range covers the Russian Far East, and northeastern China, Korea, and Japan [26].
Hedgehogs harbor a wide range of numerous zoonotic pathogens, parasitic infections, and bacterial diseases [15,27]. Species-specific endoparasites, such as lungworms Crenosoma striatum cause bronchitis and bronchopneumonia [28]. Nematodes (mainly Eucoleus spp. and Aonchotheca spp.) are prevalent lung and intestinal parasites [28,29].
Hedgehogs as final, intermediate, and paratenic hosts can be involved in the life cycles of helminths that parasitize other vertebrates. So, hedgehogs can be infected by Alaria alata (mesocercaria), Spirometra erinacei (plerocercoid), Physocephalus sexalatus (juvenile), and Trichinella spp., which are zoonotic parasites [30,31,32,33]. The epidemiological and epizootic potential of many parasites carried by hedgehogs determines the interest in their study of the parasite fauna of these animals.
The first attempts to collect data on the helminths of Erinaceus spp. inhabiting the Western Palaearctic were made by Pfaffle [34] and Rasmussen [35]. In these publications, there were almost no data about parasites of hedgehogs from Eastern Europe as much of that literature was not available via electronic databases. The purpose of this study is to review the helminth fauna of Erinaceus spp. inhabiting the Palaearctic region and systematize data about helminths of the hedgehogs according to recent conceptions.

2. Materials and Methods

2.1. Parasite Examination

For this study, we used road-killed specimens of Northern white-breasted hedgehog E. roumanicus collected in the Temnikov and Ichalki districts of the Republic of Mordovia (Russia) in the summer months of 2019–2021. All animal specimens were placed in 70% ethanol until they were used for dissection.
In total, we examined 23 carcasses of hedgehogs. Animals were studied by the method of complete helminthological dissection according to Ivashkin [36] and Anikanova [37]. Parasitic worms were collected and fixed in 70% ethanol. Cestodes, trematodes, and acanthocephalans were dehydrated in a graded ethanol series (70–96%), stained with aceto-carmine then cleared in clove oil, and mounted in Canada balsam. Nematodes were cleared in lactic acid and mounted in glycerin-jelly [36,37,38].
The identification of helminths was carried out at the Laboratory of Population Ecology of the Institute of Ecology of the Volga Basin of the Russian Academy of Sciences (Togliatti, Russia). The helminth species were identified according to publications of Genov [32], Sharpilo [39], Khokhlova [40] Moravec [41], and Kirillov [42]. The voucher specimens of parasitic helminths are stored in the helminth collection in the Institute of Ecology of Volga Basin of RAS—a branch of the Samara Federal Research Center of the Russian Academy of Sciences.
The recent helminth taxonomy is given according to Fauna Europaea (https://fauna-eu.org/, accessed on 22 January 2022) [43] and the Global Cestode database (http://out.easycounter.com/external/tapewormdb.uconn.edu, accessed on 22 January 2022) [44].

2.2. Literature Data Collection

A comparative review of the helminth fauna of Erinaceus spp. is based on the analysis of literature data on parasitic worms in hedgehogs inhabiting the Palearctic, as well as on the results of the authors’ research in the Middle Volga region (Russia). We searched scientific literature on the hedgehog helminths using international databases: Web of Science Core Collection, Scopus, Google Scholar, and eLIBRARY.ru (Russian scientific electronic library). To find studies on hedgehog parasites, we used the following search strings: Topic: [(“Helminths” or “Parasites” or “Trematodes” or “Cestodes” or “Nematodes” or “Acanthocephalans”) and (“hedgehog” or “Erinaceus” or “Erinaceus europaeus” or “Erinaceus roumanicus” or “Erinaceus concolor” or “Erinaceus amurensis” or “Erinaceidae”)]. We used both Russian and English characters to enter our search strings in the Russian database eLIBRARY.ru.
A certain number of articles for our review were taken from former USSR parasitological literature in Russian, not indexed in electronic databases. Literature sources were collected in public libraries: National Library of Russia (St. Petersburg), M. Gorky Scientific Library of St Petersburg University, and Samara Regional Universal Scientific Library. The analysis of literary sources was conducted between 1904 and 2021. We also used review papers on the helminths of the former USSR and adjacent countries [30,32,33,42,45,46,47,48,49,50,51,52].

2.3. Data Analysis

To characterize the infection of hedgehogs with parasitic worms, the following indices were used: the prevalence of infection (P, %), the intensity range (IR, specimens), and the mean abundance (MA).
The similarity between the helminth fauna of Erinaceus spp. was evaluated using the Jaccard similarity index (Cj) [53]. The degree of similarity is the following: 0–0.33—low; 0.34–0.66—medium; and 0.67–1—high. The similarity dendrogram of the helminth faunas of hedgehogs was created using the unweighted pair group method with arithmetic average (UPGMA) and the Morisita index as a distance measure in PAST 2.17 [54]. The cluster is representative when the cophenetic correlation coefficient is above 0.70. Statistical data processing was performed using the software package Microsoft Excel (2016).

3. Results

3.1. Helminths of Erinaceus roumanicus in Mordovia (Russia)

We found nine helminth species in twenty-three hedgehogs from the Republic of Mordovia, including two trematodes, one cestode, five nematodes, and one acanthocephalan (Table 1).
The overall infestation of hedgehogs by helminths was 100%, the index of helminth mean abundance was 118.5. The intensity range of hedgehog infection by helminths was from 17 to 514 specimens.

3.2. Checklist of Helminths of Erinaceus spp. in the Palaearctic

As a result of the analysis of the scientific literature, 125 articles and 9 monographs were identified, which contained data regarding the parasitic worms of the Erinaceus spp. inhabiting the Palaearctic region. Studies of the hedgehog helminth fauna were carried out in 30 countries. Currently, the helminth fauna of 4 hedgehog species of Erinaceus genus includes 54 records: 14 trematodes, 6 cestodes, 27 nematodes, and 7 acanthocephalans (Table 2).
In addition, Mariacher [76] noted in E. europaeus an unidentified acanthocephalan species in Italy. Liatis [87] registered unidentified species of trematode and acanthocephalan in E. roumanicus in Greece.
Thirteen species of parasites are host-specific parasites of hedgehogs: the trematodes B. erinacei, B. aetechini, B. mackoi, cestode H. erinacei, nematodes A. erinacei, E. tenuis, P. erinacei, C. striatum, C. lofocara, P. clausa, R. plagiostoma, acanthocephalans N. major, and O. erinacei.
Other species of helminths are facultative (or accidental) parasites of hedgehogs. Thus, the trematodes N. truncatum, R. exasperatum, nematodes P. winchesi, Porrocaecum sp. (juv.) and S. rytipleurites parasitize other insectivore species. The nematode T. retortaeformis is a host-specific parasite of lagomorphs. Host-specific rodent parasites are the trematode B. recurva, the nematode C. hepaticum, and the acanthocephalan M. moniliformis. Small rodents are the obligate hosts of larval stages of the cestodes V. mustelae and C. globifera. The obligate hosts of the trematode D. dendriticum, the nematode H. contortus and the larval stage of the cestode T. hydatigena, are ungulates. Host-specific parasites of carnivores are the trematode I. melis and the nematode E. aerophilus. The nematode T. spiralis and larval stages of the trematode A. alata, cestodes Mesocestoides sp., S. erinacei, nematodes T. nativa, P. sexalatus, A. strongylina, S. lupi parasitize many species of vertebrates. The acanthocephalan P. cylindraceus is a common parasite of passerine birds. Agamospirura minuta is a common parasite of reptiles (mainly lizards). The metacercaria S. falconis, S. sphaerula and S. strigis commonly parasitize amphibians and colubrid snakes. The trematodes Brachylaima sp., Dicrocoelium sp., the nematodes Trichuris sp., Monovaria sp., Ancylostoma sp., Gongylonema sp., Spirura sp., the acanthocephalans P. gracilis (juv.), Plagiorhynchus sp. and S. picae (juv.) are accidental parasites of hedgehogs.
Most of the helminths (39 species) parasitize Erinaceus spp. in the Palearctic in mature forms. Fifteen species of parasites were noted in hedgehogs at the larval stage (Table 2). It should be noted here that the nematode T. spiralis was found in hedgehogs both at the adult (in the intestinal lumen) and larval (musculature) stages. Only one common helminth species, the nematode P. clausa, was found in all four hedgehog species studied in the Palearctic (Table 2). Nine species of helminths were found in three species of hedgehogs (the trematode B. erinacei, the cestode H. erinacei, the nematodes A. erinacei, Aonchotheca sp., E. aerophilus, C. striatum, S. rytipleurites, Porrocaecum sp., juv., and acanthocephalan N. major). Twelve helminth species parasitize two species of hedgehogs (the trematodes Brachylaima sp., I. melis, A. alata (msc.), S. strigis (mtc.), the metacestode Mesocestoides sp., the nematodes Capillariidae sp., E. tenuis, C. hepaticum, T. spiralis, C. lofocara, the acanthocephalans M. moniliformis and P. cylindraceus). Another 32 species of parasites are found in only a single hedgehog species (Table 2).
The greatest diversity was observed in hedgehog nematodes, represented by 28 species from 14 families: Capillariidae (7), Spirocercidae (3), Trichinellidae (2), Trichostrongylidae (2), Crenosomatidae (2), Spiruridae (2), Ascarididae (1), Trichuridae (1), Strongyloididae (1), Physalopteridae (1), Rictulariidae (1), Ancylostomatidae (1), Gongylonematidae (1), and Seuratidae (1) plus spirurid larva A. minuta. The trematode composition in Erinaceus spp. is less diverse, of which there are 14 species from 7 families: Dicrocoeliidae (4), Brachylaimidae (3), Strigeidae (3), Echinostomatidae (1), Plagiorchiidae (1), Troglotrematidae (1), and Diplostomidae (1). Cestodes and acanthocephalans are insignificantly represented in the helminth faunas of Erinaceus hedgehogs. Six species of cestodes from four families were registered in hedgehogs: Taeniidae (3), Diphyllobothriidae (1), Hymenolepididae (1), and Mesocestoididae (1). Acanthocephalans in the helminths of Palaearctic hedgehogs are represented by seven species from four families: Plagiorhynchidae (3), Oligacanthorhynchidae (2), Centrorhynchidae (1), and Moniliformidae (1).
Host-specific helminths of hedgehogs are widespread in the Palearctic region. The nematode C. striatum was found in Erinaceus spp. in 20 countries; the cestode H. erinacei and nematode A. erinacei in 17; the nematode P. clausa in 15; the trematode B. erinaceid in 10; the acanthocephalan N. major in 9. The parasite of carnivores E. aerophilus, which often parasitizes hedgehogs, was recorded in 11 countries (Table 2). Other parasite species are less common in hedgehogs. A total of 22 species of helminths were recorded each in 2–8 countries. Twenty-five species of helminths are each found in only one country where hedgehog parasites were studied (Table 2).

3.3. Comparative Analysis of the Helminth Fauna of Erinaceus spp.

Among all the studied species of hedgehogs, E. europaeus and E. roumanicus have the richest helminth faunas. The helminth communities of the Northern white-breasted hedgehog in the Palaearctic include 36 species: 8 trematodes, 5 cestodes, 18 nematodes, and 5 acanthocephalans. The helminth fauna of E. roumanicus was studied in 10 European countries (Table 2). The helminth fauna of E. europaeus consists of 35 species: 10 trematodes, 3 cestodes, 18 nematodes, and 4 acanthocephalans. The parasitic worms of E. europaeus were studied in 17 countries. A significantly smaller number of parasite species was found in E. concolor: two trematodes, one cestode, seven nematodes, and two acanthocephalans. The helminths in E. concolor were studied in five countries. Only four nematode species were recorded in E. amurensis, inhabiting the eastern Palearctic. Parasites of this hedgehog species were studied in two countries (Table 2).
The helminth faunas of E. europaeus and E. roumanicus have an average degree of similarity according to the Jaccard index (0.37). The helminth compositions of E. roumanicus; E. concolor, E. europaeus; and E. concolor are less similar—0.30 and 0.24. The parasite fauna of E. amurensis has minimal similarity with the helminths of other Erinaceus hedgehogs: E. europaeus (0.08), E. concolor (0.07), and E. roumanicus (0.05).
The greatest richness of the helminth fauna in hedgehogs was in Russia and Belarus, where 17 species of parasites were found in each country (Table 2, Figure 1). Thirteen species of parasites were found in hedgehogs both in Italy and in Ukraine. Twelve species of parasitic worms were recorded in hedgehogs from the Czech Republic. Eleven helminth species were reported in hedgehogs in the UK, Germany, and Bulgaria, respectively; and, there were a reported 10 speciesin Spain and 9 speciesin Switzerland (Table 2, Figure 1).
The helminth communities in hedgehogs are relatively less diverse in Portugal, Greece, and Iran, where seven species of parasites were registered in each country. Six species of parasitic worms were noted in hedgehogs in Moldova, Turkey, and Poland, respectively; and, five helminth species were noted in Denmark, Slovakia, and Georgia. Four species of parasites were found in E. concolor from Armenia. Three helminth species were noted in hedgehogs in France, Serbia, and Japan, respectively. In the other seven countries, data on hedgehog parasites included only 1–2 species (Table 2, Figure 1).
Nematodes are found in Erinaceus spp. in all countries except Austria and Lithuania. Cestodes and trematodes were observed in hedgehogs in 20 and 18 studied regions, respectively. Acanthocephalans were found in Erinaceus spp. in 12 countries (Figure 1).
Half of the helminth species found in hedgehogs are widely distributed in the world; parasites have a cosmopolitan (13 species) and Palaearctic distribution (14 species). The distribution of eight species is limited to Europe. Seven species of hedgehog helminths have a Holarctic distribution. For 12 helminths, identified only to the genus level, distribution has not been established (Table 2).
We carried out a comparative analysis of the helminth faunas of Erinaceus spp. from various regions of the Palaearctic. The similarity dendrogram of the helminth faunas in four hedgehog species from various countries is shown in Figure 2.
The cophenetic correlation coefficient is 0.875, which confirms the validity of the cluster. As a result of the clustering analysis, the considered hedgehog species were divided into 10 groups, with the most similar helminth fauna (Figure 2). The first group is formed by the helminth faunas of E. europaeus from Lithuania and E. concolor from Armenia and Georgia. The greatest similarity in the first group was observed in the helminth fauna of E. concolor from Armenia and Georgia (0.44). The second group is formed by the helminth fauna of E. europaeus from Finland, Ireland, and France. Here, the greatest similarity was noted for hedgehog parasites from Finland and Ireland (0.67).
The third single-species group is formed by helminths of E. roumanicus from Moldova and Bulgaria (0.33). The fourth cluster is formed by the helminths of E. europaeus from the southern European countries: Spain, Portugal, and Italy. Between them, the greatest similarity was noted in the parasite composition of hedgehogs from Spain and Portugal (0.56) (Figure 2).
The fifth largest group is formed by the helminth faunas of three hedgehog species from 14 countries of the Western Palearctic (Figure 2). In this group, a high degree of similarity was noted for the parasite faunas of E. roumanicus and E. europaeus, from the same habitats in the Czech Republic (0.91), Poland (0.91), and Slovakia (0.89) (Figure 2).
The first five clusters are combined into one large group. Five separate single-species groups adjoin it (Figure 2). The sixth and the seventh clusters are formed by the helminth fauna of E. amurensis from China and Japan. The eighth cluster was formed by the parasite fauna of E. europaeus from Belgium. The ninth group is formed by E. concolor helminths in Syria. The helminth fauna of hedgehogs from clusters six to nine minimally overlaps with the parasite faunas of all other groups. The tenth and final cluster is formed by the helminth fauna of E. europaeus from Austria, which does not show any similarity with any others (Figure 2).

4. Discussion

The first study of the helminth fauna of E. roumanicus in Mordovia has noted nine species of parasites (Table 1). Most of the helminths (6 species) found in the hedgehogs of Mordovia parasitize at the mature stage. Three species (the trematode S. strigis, the nematodes P. sexalatus, and A. minuta) were found at the larval stage. Hedgehogs are paratenic and/or intermediate hosts for these parasites. Five species are host-specific parasites of hedgehogs: the cestode H. erinacei, the nematodes A. erinacei, P. clausa, C. striatum and the acanthocephalan N. major. Another four species are accidental (or unusual) parasites of hedgehogs.
Before our research, 13 species of helminths were noted in hedgehogs (E. europaeus + E. roumanicus) in European Russia (Table 2). Our studies of the helminth fauna of E. roumanicus in the Republic of Mordovia have added four species to the list of parasites in Russian hedgehogs: the trematode I. melis, the nematodes P. sexalatus (juv.), A. minuta (juv.), and the acanthocephalan N. major. According to both authors’ and literature data, 17 species of helminths parasitize Erinaceus hedgehogs in Russia [49,52,104,106,107,108], this study.
We have also added one species to the list of helminths of the Palearctic hedgehogs, A. minuta (juv.). At the present stage of research, the fauna of parasitic worms of Erinaceus spp. in the Palaearctic includes 54 species. Analysis of the helminth faunas of Erinaceus spp. showed that the richest species composition is in E. europaeus and E. roumanicus, less diverse in E. concolor, and extremely few helminths were found in E. amurensis. The degree of helminthological study of various hedgehog species in a particular region of the Palaearctic is of great importance here. Most helminthological studies have been carried out in Europe on the parasites of E. europaeus and E. roumanicus. There are very few articles on the helminths of E. concolor and E. amurensis (Table 2).
The following are some remarks on the taxonomy of parasites found in hedgehogs. The species Capillaria ovoreticulata Laubmeier, 1985 is diagnosed predominantly in hedgehogs in Germany and the UK. As Pfaffle [59] rightly noted, A. erinacei (former Capillaria erinacei) and C. ovoreticulata are morphologically difficult to distinguish. Since both species are very hard to distinguish, most authors refer to them as Capillaria spp. Meanwhile, Moravec [41] classifies this species as invalid because the description of the species has not been published [148]. We agree with the opinion of Moravec [41]. Molecular genetic studies are needed to confirm the validity of Capillaria ovoreticulata.
The finding of the cestode Mathevotaenia parva (Janicki, 1904) in hedgehogs in the Czech Republic is erroneous [99]. The cestode has been described as Davainea parva Janicki, 1904 in Erinaceus sp. from Cyprus [149], but this is a mistake since only one hedgehog species, Hemiechinus auritus (Gmelin, 1770) inhabits this island. According to Binkiene [102], H. erinacei is the only known species of cestodes parasitizing hedgehogs of Erinaceus genus, while Mathevotaenia cestodes can be detected in Hemiechinus, Paraechinus, and Atelerix hedgehogs only.
The findings of Nematollahi [140] in E. concolor, a parasite of the lungs and bronchi of small ruminants Mullerius capillaris (Mueller, 1889) (Protostrongylidae) and host-specific rodent parasite, Hymenolepis diminuta (Rudolphi, 1819) (Hymenolepididae), are also erroneous. Most likely, the authors dealt with common hedgehog parasites C. striatum and H. erinacei, previously recorded in hedgehogs in northern and northwestern Iran [85].
The diet and lifestyle of hedgehogs affect their helminth species composition. Hedgehogs get most of their helminths through food. Hedgehogs are omnivorous animals. But invertebrates are important food sources, including beetles (adult and larvae), earthworms, caterpillars and moth larvae, slugs, and snails [57,150,151]. In addition, the diet of hedgehogs includes amphibians; small reptiles; small mammals; birds, their young, and their eggs; and carrion [57].
The revealed helminth fauna confirms the omnivorous diet of Erinaceus hedgehogs. Hedgehogs get all species of trematodes and cestodes (except parasite larvae), acanthocephalans, as well as most species of nematodes (except nematodes with a direct life cycle) by eating invertebrates, which are intermediate and paratenic hosts of helminths.
The trematode I. melis develops with the involvement of the gastropod Lymnaea stagnalis (Linnaeus, 1758). Amphibians and freshwater fish are additional hosts for the parasite [152,153]. Infection of hedgehogs can occur both through gastropods and by eating amphibians [42,49,153,154].
The development of H. erinacei cysticercoids can occur in the intestinal villi of the final hosts, hedgehogs, and then pass into the intestine, where they grow to maturity [155]; and with the involvement of intermediate hosts, beetles Nicrophorus humator (Gleditsch, 1767), Nicrophorus vespillo (Linnaeus, 1758), Oiceoptoma thoracicum (Linnaeus, 1758) and Geotrupes stercorarius (Linnaeus, 1758) [156].
The mesocercariae A. alata and Strigea spp. hedgehogs probably also survive by feeding on amphibians, which are mesocercarial hosts of parasites [157]. It is less likely that hedgehogs become infected with these trematodes through aquatic gastropods, the intermediate hosts of diplostomids and strigeids, because the probability of encounters with terrestrial frogs and toads is much higher than with mollusks inhabiting the water.
The infection of Erinaceus spp. by the metacestodes V. mustelae, T. hydatigena, C. globifera, S. erinacei, and Mesocestoides sp. occurs through accidental ingestion of cestode eggs along with food [158].
Hedgehogs, as intermediate and paratenic hosts, are involved in the life cycles of helminths and can transmit infective parasite larvae along the food chains to the final hosts, birds of prey, and mammals. They potentially can become prey to red foxes (Vulpes vulpes (Linnaeus, 1758)), badgers (Meles meles (Linnaeus, 1758)), and other species of mustelid, wild boars (Sus scrofa Linnaeus, 1758), eagle owls (Bubo bubo (Linnaeus, 1758)) and tawny owls (Strix aluco Linnaeus, 1758) [16,62,159,160,161]. The involvement of hedgehogs as intermediate and paratenic hosts in the helminth life cycles plays an important role in the distribution and conservation of parasites in the wild; and it increases the infection probability of the final hosts (carnivores and birds of prey).
Hedgehogs become infected with the specific parasite P. clausa by eating the beetles of the family Scarabaenidae [32]. At the larval stage, P. clausa is a common parasite of reptiles, mainly lizards. Reptiles are paratenic hosts of the nematode. In the Middle Volga region, we found the parasite in the final host—E. roumanicus, in paratenic hosts—insectivores (Sorex araneus Linnaeus, 1758), and reptiles [51,108,162,163,164,165].
The common food of Erinaceus spp. is mollusks (mainly slugs and snails)—intermediate hosts of the highly specific parasite of hedgehogs, the nematode C. striatum [3,166]. So, the mollusks Radix balthica (Linnaeus, 1758), Morlina glabra (Rossmassler, 1835), Succinea putris Linnaeus, 1758, Urticicola umbrosus (Pfeiffer, 1828), Arion circumscriptus Johnston, 1828, Malacolimax tenellus (Muller, 1774) and Tandonia rustica (Millet, 1843) are registered as intermediate hosts of the nematode [167].
The close contact between hedgehogs and soil and forest litter causes their infection with capillariids, nematodes with a direct lifestyle. The nematode E. aerophilus can be transmitted to hedgehogs directly, as well as when eating earthworms [130]. The development of A. erinacei is associated with the terrestrial environment and it can happen both directly and with the involvement of paratenic hosts: terrestrial gastropods and earthworms Lumbricus terrestris Linnaeus, 1758 and Aporrectodea rosea (Savigny, 1826) [130,166,168].
The host-specific hedgehog’s parasite, N. major, also develops with the involvement of intermediate hosts, represented by terrestrial Isopoda and Coleoptera. Paratenic hosts, such as fish, amphibians, reptiles, and mammals, may be involved in the life circle of acanthocephalans [40,169].
A comparative analysis of the helminth species composition in Erinaceus spp. from various countries showed, on the one hand, the originality of the parasite faunas of each hedgehog species and, on the other, the similarity of the helminth communities of Erinaceus spp. from various regions of the Palaearctic. The originality of the helminth fauna of hedgehogs is achieved by parasitizing them with accidental or non-specific helminths or locally distributed helminths. Thus, in E. europaeus and E. roumanicus, 15 species of parasites were noted in each, which are not found in other species of hedgehogs. The trematode B. recurva was found only in E. concolor, and the nematode Monovaria sp. in E. amurensis (Table 2). As a result, the average and low degree of similarity index of the helminth faunas of various species of Erinaceus was noted according to the Jaccard index.
The similarity of the helminth fauna of hedgehogs in certain studied regions is defined as a wide distribution of specific helminth species of Erinaceus spp. (C. striatum, H. erinacei, A. erinacei, P. clausa, and others) and the geographical proximity of study areas. Thus, the highest similarity was noted in the helminth composition of various hedgehog species from the same territory: E. europaeus and E. roumanicus from the Czech Republic, Poland, and Slovakia; as well as hedgehogs from Serbia and Slovakia (0.75–0.86), Germany and Switzerland (0.70), the Czech Republic and Germany (0.70) (Figure 2).
A high similarity in the helminth fauna of hedgehogs from countries far from each other was noted only when comparing the parasites of one species of hedgehogs (in E. europaeus from Finland and Ireland—0.67). As a rule, the helminth faunas of various species of hedgehogs from distant countries have a low similarity (E. europaeus from Spain and E. roumanicus from Russia—0.50, E. europaeus from Russia and E. roumanicus from Bulgaria—0.30) (Figure 2).
A total of 12 of the 54 helminth species found in hedgehogs in the Palaearctic have medical and veterinary significance as potential pathogens of dangerous helminthiasis. These include the trematodes A. alata (causes alariosis in humans and domestic animals), D. dendriticum (dicrocoeliosis in humans and domestic ruminants, dogs, and cats), the cestode S. erinacei (spirometrosis and sparganosis in humans and domestic animals), Mesocestoides sp. (mesocestidosis in domestic and wild carnivores), T. hydatigena (taeniasis and cysticercosis in dogs and wild carnivores), the nematodes E. aerophilus (pulmonary capillariasis in humans and wild carnivorous and omnivorous mammals), T. spiralis and T. nativa (trichinellosis in humans and domestic and wild mammals), Ph. sexalatus (physocephalosis in domestic pigs and wild boars), H. contortus (haemonchosis of ruminants), A. strongylina (ascaropsosis in domestic pigs and wild boars) and S. lupi (spirocercosis in domestic and wild carnivores) [170,171,172,173,174,175,176,177]. It should be noted that transmission of these parasites to humans and domestic animals from hedgehogs is unlikely. However, the involvement of hedgehogs in the life cycles of dangerous helminth species increases the possibility of transmission of parasites to their final hosts. In this way, hedgehogs contribute to the conservation of zoonotic foci in the wild.

5. Conclusions

The helminth fauna of the Northern white-breasted hedgehog Erinaceus roumanicus was studied for the first time in the Republic of Mordovia (Russia). In total, we found nine species of helminths in hedgehogs. Of them, four species were noted in Russian hedgehogs for the first time: the trematode I. melis, nematodes P. sexalatus (juv.), A. minuta (juv.), and the acanthocephalan N. major.
According to our research and literature data, the helminth fauna of Erinaceus spp. in the Palaearctic includes 54 species: 14 trematodes, 8 cestodes, 27 nematodes, and 7 acanthocephalans. Among all the studied species of hedgehogs, E. europaeus (35 species) and E. roumanicus (36) have the richest helminth faunas. The diversity of the parasite communities of Erinaceus spp. is due to the wide distribution and varied diet of these mammals. Most of the helminths found in hedgehogs are transmitted to them along trophic chains. Hedgehogs are the final hosts for 39 species of parasites. For 15 helminth species, Erinaceus spp. are paratenic and/or intermediate hosts. The base of the hedgehog helminth fauna is formed by host-specific parasites, of which there are only 13 species. Most of the hedgehog parasites in the Palaearctic are facultative (non-specific) species that parasitize in various vertebrates. The comparative analysis of the helminth faunas of Erinaceus spp. from various countries showed, on the one hand, the originality of the helminth fauna of each hedgehog species and, on the other, the similarity of the helminth fauna of these insectivores from various regions of the Palearctic. These features are caused by similar lifestyles and diet peculiarities of every hedgehog species in various regions. A total of 12 of the 54 helminth species found in hedgehogs in the Palaearctic region have medical and veterinary significance as causative agents of dangerous helminthiasis, including the trematodes D. dendriticum, A. alata, the cestodes T. hydatigena, S. erinacei, Mesocestoides sp., and the nematodes E. aerophilus, T. spiralis, T. nativa, H. contortus, P. sexalatus, A. strongylina and S. lupi.

Author Contributions

Conceptualization, A.B.R. and A.A.K.; methodology, A.A.K. and N.Y.K.; formal analysis, A.A.K. and A.B.R.; investigation, A.A.K. and N.Y.K.; writing—original draft preparation, A.A.K., N.Y.K. and A.B.R.; writing—review and editing, A.A.K. and A.B.R.; project administration, A.B.R.; funding acquisition, A.B.R. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

All applicable international, national, and institutional guidelines for the use and care of wild animals were followed. Our research was conducted in compliance with the ethical standards of humane treatment of animals according with the recommended standards of the Directive of the European Parliament and of the Council of the European Union of 22 September 2010 “On the protection of animals used for scientific purposes” (EU Directive 2010/63/EU). No animal was killed with the aim of helminth sampling for our study. The material for parasitological research was obtained as a result of fieldwork on accounting for the number of wild animals. They are regularly held according to the research topics of the Federal State Budgetary Institution “Reserved Mordovia” (“Zapovednaya Mordovia”) in 2018–2022. The research theme and handling procedures with wild animals were approved by the Ministry of Natural Resources and Ecology of Russia.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

The work was carried out on the theme of research of the Institute of Ecology of the Volga River Basin—a branch of the Samara Federal Research Center of the Russian Academy of Sciences “Structure, dynamics and sustainable development of ecosystems in the Volga River Basin” No 1021060107217-0-1.6.19.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Hiutu, O.; Norrdahl, K.; Koprimäki, E. Competition, predation and interspecific synchrony in cyclic small mammal communities. Ecography 2004, 27, 197–206. [Google Scholar] [CrossRef]
  2. Rutovskaya, M.V.; Aleksandrov, A.N.; Podshivalina, V.N.; Soboleva, A.S.; Glushenkov, O.V. Habitat conditions of Desmana moschata (Talpidae, Eulipotyphla, Mammalia) in the buffer zone of the Prisurskiy State Nature Reserve (Russia). Nat. Conserv. Res. 2020, 5, 36–46. [Google Scholar] [CrossRef]
  3. Bashinskiy, I.V. Beaver impact on water coverage of forest-steppe territories (Penza region, European Russia). Nat. Conserv. Res. 2021, 6, 88–97. [Google Scholar] [CrossRef]
  4. Lazutkin, A.N. Long-term monitoring of red-backed voles number in Magadan Nature Reserve in 1980–2021. Proc. Mordovia State Nat. Res. 2021, 29, 319–325. [Google Scholar]
  5. Yakimova, A.E.; Gaidysh, I.S. The species composition and abundance of terrestrial small mammals in the Finnish-Russian Friendship Nature Reserve. Nat. Conserv. Res. 2021, 6, 127–136. [Google Scholar] [CrossRef]
  6. Gremyachikh, V.A.; Kvasov, D.A.; Ivanova, E.S. Patterns of mercury accumulation in the organs of bank vole Myodes glareolus (Rodentia, Cricetidae). Biosyst. Div. 2019, 27, 329–333. [Google Scholar] [CrossRef]
  7. Lebedinskii, A.A.; Noskova, O.S.; Dmitriev, A.I. Post-fire recovery of terrestrial vertebrates in the Kerzhensky State Nature Biosphere Reserve (Central Volga Region, Russia). Nat. Conserv. Res. 2019, 4, 45–56. [Google Scholar] [CrossRef]
  8. Vekhnik, V.A. Comparative analysis of biology and ecology of Glis glis (Gliridae, Rodentia) in the Zhiguli State Nature Reserve (Russia) and adjacent territories. Nat. Conserv. Res. 2020, 5, 1–20. [Google Scholar] [CrossRef]
  9. Poulin, R.; Morand, S. The diversity of parasites. Quart. Rev. Biol. 2000, 75, 277–293. [Google Scholar] [CrossRef]
  10. Balestrieri, A.; Gazzola, A.; Formenton, G.; Canova, L. Long-term impact of agricultural practices on the diversity of small mammal communities: A case study based on owl pellets. Environ. Monit. Assess 2019, 191, 725. [Google Scholar] [CrossRef] [PubMed]
  11. Ahissa, L.; Akpatou, B.K.; Bohoussou, H.K.; Kadjo, B.; Koné, I. Species composition and community structure of terrestrial small mammals in Tanoé-Ehy Swamp Forest (South-East Ivory Coast): Implication for conservation. Nat. Conserv. Res. 2020, 5, 53–63. [Google Scholar] [CrossRef]
  12. Kononova, M.I.; Prisniy, Y.A. Helminthes of mouse-like rodents in the Belogorye State Nature Reserve (Russia). Nat. Conserv. Res. 2020, 5, 11–18. [Google Scholar] [CrossRef]
  13. Kirillova, N.; Ruchin, A.; Kirillov, A. Helminths in myomorph rodents (Rodentia, Myomorpha) from the National Park “Smolny” and its surroundings (European Russia). Forests 2021, 12, 1510. [Google Scholar] [CrossRef]
  14. Romashov, B.V.; Odoevskaya, I.M.; Romashova, N.B.; Golubova, N.A. Ecology of trichinellosis transmission in the Voronezh State Nature Reserve and adjacent areas, Russia. Nat. Conserv. Res. 2021, 6, 1–15. [Google Scholar] [CrossRef]
  15. Hutterer, R. Order Erinaceomorpha. In Mammal Species of the World: A Taxonomic and Geographic Reference, 3rd ed.; Wilson, D.E., Reeder, D.M., Eds.; Johns Hopkins University Press: Baltimore, MD, USA, 2005; pp. 220–311. [Google Scholar]
  16. Reeve, N.J. Hedgehogs; T & AD Poyser Natural History: London, UK, 1994; pp. 3–313. [Google Scholar]
  17. Rautio, A.; Isomursu, M.; Valtonen, A.; Hirvela-Koski, V.; Kunnasranta, M. Mortality, diseases and diet of European hedgehogs (Erinaceus europaeus) in an urban environment in Finland. Mammal Res. 2016, 61, 161–169. [Google Scholar] [CrossRef]
  18. Jourde, P. Le Hérisson d’Europe; Delachaux et Niestlé: Paris, France, 2013; pp. 3–207. [Google Scholar]
  19. Aulagnier, S.; Haffner, P.; Mitchell-Jones, A.J.; Moutou, F.; Zima, J. Mammals of Europe, North Africa and the Middle East; A and C Black Publishers: London, UK, 2009; pp. 3–272. [Google Scholar]
  20. Holz, H. Studies on European hedgehogs. Z. Zool. Syst. Evolut. 1978, 16, 148–165. [Google Scholar] [CrossRef]
  21. Krystufek, B. The distribution of hedgehogs (Erinaceus L., 1758, Insectivora, Mammalia) in Western Yugoslavia. Biosistematika 1983, 9, 71–78. [Google Scholar]
  22. Seddon, J.M.; Santucci, F.; Reeve, N.J.; Hewitt, G.M. Caucasus Mountains divide postulated postglacial colonization routes in the white-breasted hedgehog, Erinaceus concolor. J. Evol. Biol. 2002, 15, 463–467. [Google Scholar] [CrossRef]
  23. Sommer, R.S. When east meets west: The sub-fossil footprints of the west European hedgehog and the northern white-breasted hedgehog during the Late Quaternary in Europe. J. Zool. 2007, 273, 82–89. [Google Scholar] [CrossRef]
  24. Amori, G. Erinaceus europaeus. The IUCN Red List of Threatened Species 2016: E.T29650A2791303. 2016. Available online: https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T29650A2791303.en (accessed on 13 February 2020).
  25. Bogdanov, A.S.; Bannikova, A.A.; Pirusskii, Y.M.; Formozov, N.A. The first genetic evidence of hybridization between west European and northern white-breasted hedgehogs (Erinaceus europaeus and E. roumanicus) in Moscow Region. Biol. Bull. 2009, 6, 760–765. [Google Scholar] [CrossRef]
  26. Cassola, F. Erinaceus amurensis (errata version published in 2017). The IUCN Red List of Threatened Species 2016: E.T40604A115174360. 2016. Available online: https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T40604A22325640.en (accessed on 20 January 2022).
  27. Riley, P.Y.; Chomel, B.B. Hedgehog zoonoses. Emerg. Infect. Dis. 2005, 11, 1–5. [Google Scholar] [CrossRef] [PubMed]
  28. Keymer, I.F.; Gibson, E.A.; Reynolds, D.J. Zoonoses and other findings in hedgehogs (Erinaceus europaeus): A survey of mortality and review of the literature. Vet. Rec. 1991, 128, 245–252. [Google Scholar] [CrossRef] [PubMed]
  29. Egli, E. Comparison of Physical Condition and Parasite Burdens in Rural, Suburban and Urban Hedgehogs Erinaceus europaeus: Implications for Conservation. Master’s Thesis, Bern University, Bern, Switzerland, 2004. [Google Scholar]
  30. Andreyko, O.F. Parasites of Mammals of Moldova; Stiintsa: Kishinev, Moldova, 1973; pp. 3–186. [Google Scholar]
  31. Fameree, L.; Cotteleer, C.; Van den Abbeele, O. Epidemological and sanitary importance of Trichinosis in wild animals in Belgium—A summary of investigations 1979–1981. Schweiz. Arch. Tierheilkd. 1982, 124, 401–412. [Google Scholar] [PubMed]
  32. Genov, T. Helminths of Insectivores and Rodents in Bulgaria; Bulgarian Academy of Sciences Publishing House: Sofia, Bulgaria, 1984; pp. 3–348. [Google Scholar]
  33. Bychkova, E.I.; Akimova, L.N.; Degtyarik, S.M.; Yakovich, M.M. Helminths of Vertebrates and Man in Belarus; Belarusskaya Nauka Publishing House: Minsk, Belarus, 2017; pp. 3–316. [Google Scholar]
  34. Pfaffle, M.P.; Bolfíkova, B.C.; Hulva, P.; Petney, T. Different parasite faunas in sympatric populations of sister hedgehog species in a secondary contact zone. PLoS ONE 2014, 9, e114030. [Google Scholar] [CrossRef] [Green Version]
  35. Rasmussen, S.L.; Hallig, J.; van Wijk, R.E.; Petersen, H.H. An investigation of endoparasites and the determinants of parasite infection in European hedgehogs (Erinaceus europaeus) from Denmark. Int. J. Parasitol. Par. Wildl. 2021, 16, 217–227. [Google Scholar] [CrossRef]
  36. Ivashkin, V.M.; Kontrimavichus, V.L.; Nasarova, N.S. Methods of the Collection and Studies of Helminths of Land Mammals; Nauka: Moscow, Russia, 1971; pp. 3–123. [Google Scholar]
  37. Anikanova, V.S.; Bugmyrin, S.V.; Ieshko, E.P. Methods of the Collection and Studies of Helminths of Small Mammals; Karelian Scientific Center of RAS: Petrozavodsk, Russia, 2007; pp. 3–145. [Google Scholar]
  38. Zander, R.H. Four water-soluble mounting media for microslides. Phytoneuron 2014, 32, 1–4. [Google Scholar]
  39. Sharpilo, V.P. Parasitic Worms of Reptiles of Fauna of USSR; Naukova Dumka: Kiev, Ukraine, 1976; pp. 3–287. [Google Scholar]
  40. Khokhlova, I.G. Acanthocephalans of Terrestrial Vertebrates of the USSR Fauna; Nauka: Moscow, Russia, 1986; pp. 3–278. [Google Scholar]
  41. Moravec, F. Review of capillariid and trichosomoidid nematodes from mammals in the Czech Republic and the Slovak Republic. Acta Soc. Zool. Bohem. 2000, 64, 271–304. [Google Scholar]
  42. Kirillov, A.A.; Kirillova, N.Y.; Chikhlyaev, I.V. Trematodes of Terrestrial Vertebrates of the Middle Volga Region; Cassandra: Togliatti, Russia, 2012; pp. 3–329. [Google Scholar]
  43. Fauna Europaea. Available online: https://fauna-eu.org/ (accessed on 22 January 2022).
  44. Global Cestode Database. Available online: http://out.easycounter.com/external/tapewormdb.uconn.edu (accessed on 22 January 2022).
  45. Andreyko, O.F. Overview of helminth fauna of insectivores (Insectivora) of the USSR and neighbouring countries. Par. Anim. Plan. 1973, 9, 3–34. [Google Scholar]
  46. Movsesyan, S.O.; Chubarian, F.A.; Nikoghosian, M.A. Trematodes of the Fauna of South of the Low Caucasus; Nauka: Moscow, Russia, 2004; pp. 3–279. [Google Scholar]
  47. Movsesyan, S.O.; Chubarian, F.A.; Nikoghosian, M.A. Cestodes of the Fauna of South of the Low Caucasus; Nauka: Moscow, Russia, 2006; pp. 3–331. [Google Scholar]
  48. Kostyunin, V.M. Helminth Fauna of Terrestrial Vertebrates in the Middle Volga Region; Nizhny Novgorod State Pedagogical University Publish: Nizhny Novgorod, Russia, 2010; pp. 3–225. [Google Scholar]
  49. Kirillova, N.Y. Helminths of Small Mammals of the Samarskaya Luka. Fauna and Ecology; Lambert Academic Publishing: Saarbrucken, Germany, 2011; pp. 3–251. [Google Scholar]
  50. Movsesyan, S.O.; Nikoghosian, M.A.; Petrosian, R.A.; Kuznetsov, D.N. Nematodes and Acanthocephalans of the Fauna of South of the Low Caucasus; KMK: Moscow, Russia, 2017; pp. 3–445. [Google Scholar]
  51. Kirillov, A.A.; Kirillova, N.Y.; Krasnobayev, Y.P.; Vekhnik, V.P. Parasitic Worms of Small Mammals in Zhiguli State Nature Reserve; Committee of RAS for the Conservation of Biological Diversity, A.N. Severtzov Institute of Ecology and Evolution of RAS: Moscow, Russia, 2017; pp. 3–81. [Google Scholar]
  52. Kirillov, A.A.; Kirillova, N.Y.; Chikhlyaev, I.V. Parasites of Vertebrates in the Samara Region; Polyar: Togliatti, Russia, 2018; pp. 3–304. [Google Scholar]
  53. Magurran, A.E. Measuring Biological Diversity; Blackwell Publishing: Oxford, UK, 2004; pp. 3–256. [Google Scholar]
  54. Hammer, O.; Harper, D.A.T.; Ryan, P.D. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 2001, 4, 9. [Google Scholar]
  55. Matsaberidze, G.V. Helminths of Micromammals in Eastern Georgia (Fauna, Ecology, Zoogeography). Ph.D. Thesis, Tbilisi State University, Tbilisi, Georgia, 1966. [Google Scholar]
  56. Reeve, N.J.; Huijser, M.P. Mortality factors affecting wild hedgehogs: A study of records from wildlife rescue centres. Lutra 1999, 42, 7–24. [Google Scholar]
  57. Robinson, I.; Routh, A. Veterinary care of the hedgehog. Practice 1999, 21, 128–137. [Google Scholar] [CrossRef]
  58. Gaglio, G.; Allen, S.; Bowden, L.; Bryant, M.; Morgan, E.R. Parasites of European hedgehogs (Erinaceus europaeus) in Britain: Epidemiological study and coprological test evaluation. Eur. J. Wildl. Res. 2010, 56, 839–844. [Google Scholar] [CrossRef]
  59. Pfaffle, M.P. Influence of Parasites on Fitness Parameters of the European Hedgehog (Erinaceus europaeus). Ph.D. Thesis, Karlsruhe Institute of Technology (KIT), Karlsruhe, Germany, 2010. [Google Scholar]
  60. Whiting, I. Prevalence of endoparasites in the European hedgehog (Erinaceus europaeus) within regions of the East Midlands. IATL Reinvent. Inter. J. Undergrad. Res. 2012. Available online: https://warwick.ac.uk/fac/cross_fac/iatl/reinvention/archive/bcur2012specialissue/whiting/ (accessed on 26 January 2022).
  61. Wright, I. Parasites affecting wild European hedgehogs: Disease potential and zoonoses. Comp. Anim. 2014, 19, 642–646. [Google Scholar] [CrossRef]
  62. Cottarel, P. Epidemiogie Descriptive de L’infestation Parasitaire du Herisson d’Europe (Erinaceus europaeus) en soin dans un Centre de Sauvegarde du sud de la France. Ph.D. Thesis, l’Universite Claude-Bernard, Lyon, France, 2016. [Google Scholar]
  63. Schütze, H.R. Nachweis, Vorkommen, entwicklung und behandlung wichtiger parasiten des igels (Erinaceus europaeus L.). Der Praktische Tierarzt. 1980, 61, 142–146. [Google Scholar]
  64. Timme, A. Causes of disease and death among hedgehogs (Erinaceus europaeus L.) during 1975 to 1979. Der Praktische Tierarzt. 1980, 61, 744–748. [Google Scholar]
  65. Barutzki, D.; Laubmeier, E.; Forstner, M. Endoparasitic infestation of wild hedgehogs and hedgehogs in human care with a contribution to therapy. Tierarztl. Prax. 1987, 15, 325–331. [Google Scholar]
  66. Laux, A. Extensitat und intensitat des endoparasitenbefalls beim igel. Angew. Parasitol. 1987, 28, 137–141. [Google Scholar]
  67. Kutzer, E. Parasitosen des igels. In Veterinärmedizinische Parasitologie, 4th ed.; Boch, J., Supperer, R., Eds.; Parey: Berlin/Heidelberg, Germany, 1992; pp. 771–776. [Google Scholar]
  68. Epe, C.; Ising-Volmer, S.; Stoye, M. Parasitological fecal studies of equids, dogs, cats and hedgehogs during the years 1984–1991. DTW. Deutsche Tierärz. Wochenschr. 1993, 100, 426–428. [Google Scholar]
  69. Döpke, C. Kasuistische Auswertung der Untersuchungen von Igeln (Erinaceus europaeus) im Einsendungsmaterial des Instituts für Pathologie von 1980 bis 2001. Ph.D. Thesis, Tierärztliche Hochschule, Hannover, Germany, 2002. [Google Scholar]
  70. Beck, W. Endoparasiten beim igel. Wien. Klinisch. Wochenschr. 2007, 119, 40–44. [Google Scholar] [CrossRef]
  71. Kögel, B. Untersuchungen zu Igelpfleglingen Ausgewählter Deutscher Igelstationen und Erfolge der Therapie aus den Jahren 1984 bis 2006. Ph.D. Thesis, Tierärztliche Hochschule, Hannover, Germany, 2009. [Google Scholar]
  72. Lambert, D. Parasitosen und Mykosen des Igels, 2nd ed.; Pro Igel e.V., Arbeitskreis Igelschutz Berlin e.V.: Berlin, Germany, 2019; pp. 3–149. [Google Scholar]
  73. Giannetto, S.; Niutta, P.P.; Giudice, E. Parasitological research on the hedgehog (Erinaceus europaeus) in Sicily. Pests Anim. 1993, 47, 1433–1436. [Google Scholar]
  74. Ribas, A.; Filipucci, M.G.; Casanova, J.C. Parasitic helminthes of small mammals in Elba island. Hystrix—Ital. J. Mammal. 2003, 14, 793–796. [Google Scholar]
  75. Poglayen, G.; Giannetto, S.; Scala, A.; Garippa, G.; Capelli, G.; Scaravelli, D.; Brianti, E.; Reeve, N.J. Helminths found in hedgehogs (Erinaceus europaeus) in three areas of Italy. Vet. Rec. 2003, 152, 22–24. [Google Scholar] [CrossRef] [PubMed]
  76. Mariacher, A.; Santini, A.; Del Lesto, I.; Tonon, S.; Cardini, E.; Barone, A.; Eleni, C.; Fichi, G.; Perrucci, S. Endoparasite infections of the European hedgehog (Erinaceus europaeus) in Central Italy. Animals 2021, 11, 3171. [Google Scholar] [CrossRef]
  77. Feliu, C.; Blasco, S.; Torres, J.; Miquel, J.; Casanova, J.C. On the helminthfauna of Erinaceus europaeus Linnaeus, 1758 (Insectivora, Erinaceidae) in the Iberian Peninsula. Res. Rev. Parasitol. 2001, 61, 31–37. [Google Scholar]
  78. Baer, J.-G. Contribution a la faune helminthologique de Suisse. Rev. Suiss. Zool. 1928, 35, 27–41. [Google Scholar] [CrossRef]
  79. Burgisser, H. Compte-rendu sur les maladies des animaux sauvages de 1975 a 1982. Schw. Arch. Tierheilk. 1983, 125, 519–527. [Google Scholar]
  80. Liesegang, A.; Lehmann, M.C. Haufigkeit von krankheit und abgangsursachen bei igeln. Schweiz. Arch. Tierheil. 2003, 145, 589–591. [Google Scholar] [CrossRef]
  81. Slapeta, J.R. Endoparasites of hedgehogs in the Czech Republic. Veterinarstvi 1999, 49, 248–252. [Google Scholar]
  82. Mizgajska-Wiktor, H.; Jarosz, W.; Pilacinska, B.; Dziemian, S. Helminths of hedgehogs, Erinaceus europaeus and E. roumanicus from Poznan region, Poland—Coprological study. Wiad. Parazytol. 2010, 56, 329–332. [Google Scholar]
  83. Jarosz, W.; Dziemian-Zwolak, S.; Zwolak, R.; Mizgajska-Wiktor, H. Do small mammals contribute to the dissemination of zoonotic helminths in human environment? Study of rodents and hedgehogs. Ann. Parasitol. 2016, 62, 51. [Google Scholar]
  84. Viktorov, L.V.; Golovin, O.V.; Savinov, V.A. Materials on the helminth fauna of insectivorous mammals of the Kalinin oblast. Proceed. Kalinin State Pedag. Inst. 1964, 31, 289–292. [Google Scholar]
  85. Naem, S.; Pourreza, B.; Gorgani-Firouzjaee, T. The European hedgehog (Erinaceus europaeus), as a reservoir for helminth parasites in Iran. Vet. Res. Forum 2015, 6, 149–153. [Google Scholar] [PubMed]
  86. Fuentes, M.V.; Saez, S.; Trellis, M.; Cruz, J.; Sarmento, P.; Casanova, J.C.; Torres, J.; Feliu, C.; Esteban, J.G. Helminthofauna of small mammals (Insectivora, Rodentia) collected in tbe Serra da Malcata (Portugal). Rev. Iber. Parasitol. 2003, 63, 89–92. [Google Scholar]
  87. Liatis, T.K.; Monastiridis, A.A.; Birlis, P.; Prousali, S.; Diakou, A. Endoparasites of wild mammals sheltered in wildlife hospitals and rehabilitation centres in Greece. Front. Vet. Sci. 2017, 4, 220. [Google Scholar] [CrossRef] [Green Version]
  88. Hildebrand, J.; Adamczyk, M.; Laskowski, Z.; Zalesny, G. Host-dependent morphology of Isthmiophora melis (Schrank, 1788) Luhe, 1909 (Digenea, Echinostomatinae)—Morphological variation vs. molecular stability. Parasites Vectors 2015, 8, 481. [Google Scholar] [CrossRef] [Green Version]
  89. Karasev, N.F. Helminths of mammals in Berezinsky Nature Reserve. Berez. Nat. Res. 1970, 1, 155–179. [Google Scholar]
  90. Karasev, N.F. Ecological analysis of helminth fauna of mammals in Berezinsky Nature Reserve. Berez. Nat. Res. 1972, 2, 159–181. [Google Scholar]
  91. Melnichenko, E.D.; Panasenko, N.A. To the helminth fauna of some insectivorous mammals of the Middle Dnieper region. Vestn. Zool. 1979, 5, 79–81. [Google Scholar]
  92. Iskova, N.I.; Sharpilo, V.P.; Sharpilo, L.D.; Tkach, V.V. Catalogue of Helminths of Ukraine. Trematodes of Terrestrial Vertebrates; Naukova Dumka: Kiev, Ukraine, 1995; pp. 3–93. [Google Scholar]
  93. Lowenstein, M.; Prosl, H.; Loupal, G. Parasitosen des igels und deren bekampfung. Wien. Tierärzt. Monatssch. 1991, 78, 127–135. [Google Scholar]
  94. Casanova, J.C.; Ribas, A. Description of Brachylecithum mackoi n. sp. (Digenea: Dicrocoeliidae) from the European hedgehog, Erinaceus europaeus (Insectivora: Erinaceidae). J. Parasitol. 2004, 90, 793–796. [Google Scholar] [CrossRef]
  95. Shimalov, V.V. Helminth fauna of insectivorous mammals in the “Bugsky” landscape reserve (Belarus). Bull. Brest Univ. Nat. Sci. Ser. 2008, 30, 104–111. [Google Scholar]
  96. Boag, B.; Fowler, P. The prevalence of helminth parasites from the hedgehog Erinaceus europaeus in Great Britain. J. Zool. 1988, 215, 379–382. [Google Scholar] [CrossRef]
  97. Bunnell, T. The incidence of disease and injury in displaced wild hedgehogs (Erinaceus europaeus). Lutra 2001, 44, 3–14. [Google Scholar]
  98. Pantchev, N.; Globokar-Vrhovec, M.; Beck, W. Endoparasites from indoor kept small mammals and hedgehogs. Laboratory evaluation of fecal, serological, and urinary samples (2002–2004). Tieraerztl. Prax. 2005, 33, 296–306. [Google Scholar]
  99. Prokopic, J. Vysledky helmintologickeho vyzkumu nasich jezku. Věst. Českosl. Zool. Spol. 1957, 21, 97–111. [Google Scholar]
  100. Pavlovic, I.; Savic, B. Helminth fauna of the northern white-breasted hedgehog (Erinaceus roumanicus) in Serbia. J. Parasit. Dis. 2017, 41, 605–606. [Google Scholar] [CrossRef]
  101. Furmaga, F. Materials to the helminth fauna of hedgehogs Erinaceus roumanicus Barrett-Hamilton. Acta Parasitol. 1961, 9, 441–445. [Google Scholar]
  102. Binkiene, R.; Miliute, A.; Stunženas, V. Molecular data confirm the taxonomic position of Hymenolepis erinacei (Cyclophyllidea: Hymenolepididae) and host switching, with notes on cestodes of Palaearctic hedgehogs (Erinaceidae). J. Helminthol. 2019, 93, 195–202. [Google Scholar] [CrossRef] [PubMed]
  103. Merkusheva, I.V. Intestinal worm infection of the west European hedgehog (Erinaceus europaeus) in Belarus. Proceed. Acad. Sci. BSSR. Biol. Ser. 1966, 4, 119–121. [Google Scholar]
  104. Artyukh, E.S. Helminth fauna of useful and harmful wild mammals (rodents, insectivores and bats) of the Middle Trans-Volga region. Proceed. Kuibyshev Agric. Inst. 1950, 10, 31–39. [Google Scholar]
  105. Davydova, O.E.; Pimenov, N.V.; Vasilevytch, F.I. Some results of the helminthological and bacteriological investigations of insectivores (Insectivora: Erinaceidae) and rodents (Rodentia: Sciuridae) on the territory of the urban forest area of megapolis under conditions of anthropogenic pressure. Int. J. Pharmac. Res. Allied Sci. 2016, 5, 75–84. [Google Scholar]
  106. Vlasov, E.A. Helminths of Wild Mammals in the Central Chernozem State Nature Reserve (Fauna, Ecology and Pathogen Significance). Ph.D. Thesis, Kursk State University, Kursk, Russia, 2016. [Google Scholar]
  107. Kirillova, N.Y. Helminth fauna of insectivores (Insectivora) from the Samarskaya Luka. Bull. Samara Sci. Cent. Rus. Acad. Sci. 2004, 6, 334–340. [Google Scholar]
  108. Kirillova, N.Y.; Kirillov, A.A. Overview of helminths in small mammals in the Zhiguli State Reserve. Nat. Conserv. Res. 2017, 2, 24–37. [Google Scholar] [CrossRef] [Green Version]
  109. Davydov, O.N. Data to helminth fauna of insectivores in Ukrainian SSR. In Problems of Parasitology; Markevitch, A.P., Ed.; Naukova Dumka: Kiev, Ukraine, 1963; pp. 182–183. [Google Scholar]
  110. Cirak, V.Y.; Senlik, B.; Aydogdu, A.; Selver, M.; Akyol, V. Helminth parasites found in hedgehogs (Erinaceus concolor) from Turkey. Prevent. Vet. Med. 2010, 97, 64–66. [Google Scholar] [CrossRef]
  111. Youssefi, M.R.; Rahimi, M.T.; Halajian, A.; Moosapour, A.A.; Nikzad, R.; Nikzad, M.; Ramezanpour, S.; Ebrahimpour, S. Helminth Parasites of eastern European hedgehog (Erinaceus concolor) in Northern Iran. Iran. J. Parasitol. 2013, 8, 645–650. [Google Scholar]
  112. Casanova, J.C.; Miquel, J.; Fons, R.; Molina, X.; Feliu, C.; Mathias, M.L.; Torres, J.; Libois, R.; Santos-Reis, M.; Collares-Pereira, M.; et al. On the helminthfauna of wild mammals (Rodentia, Insectivora and Lagomorpha) in Azores archipelago (Portugal). Vie Milieu/Life Environ. 1996, 46, 253–259. [Google Scholar]
  113. Macchioni, G. Infestione del riccio (Erinaceus europaeus L., 1758) da larve di Mesocestoides lineatus (Goeze, 1782). Ann. Fac. Med. Vet. Pisa 1966, 19, 325–339. [Google Scholar]
  114. Haigh, A.; O’Keeffe, J.; O’Riordan, R.M.; Butler, F. A preliminary investigation into the endoparasite load of the European hedgehog (Erinaceus europaeus) in Ireland. Mammalia 2013, 78, 103–107. [Google Scholar] [CrossRef] [Green Version]
  115. Mituch, J. Beitrag zur erkenntnis der helminthenfauna des igels (Erinaceus europaeus romanicus Bar.-Hamilton, 1900). Stud. Helminthol. 1964, 1, 101–104. [Google Scholar]
  116. Andreyko, O.F. About nematodes of insectivores in the Prut-Dniester interfluve. In Parasites of Vertebrates; Spassky, A.A., Ed.; Stiintsa: Kishinev, Moldova, 1969; pp. 146–155. [Google Scholar]
  117. Vasiljev, V.V. Parasite fauna of rodents and insectivores from surroundings of Leningrad. Proceed. Leningr. State Univ. Biol. Ser. 1949, 101, 73–81. [Google Scholar]
  118. Kirillova, N.Y.; Kirillov, A.A. Ecological and faunistic analysis of helminths of insectivorous mammals (Insectivora) from the Samarskaya Luka. Bull. Samara Sci. Cent. Rus. Acad. Sci. 2004, 3, 92–100. [Google Scholar]
  119. Kirillova, N.Y.; Kirillov, A.A. Nematodes (Nematoda) of small mammals from the Samarskaya Luka. Bull. Samara Sci. Cent. Rus. Acad. Sci. 2011, 13, 114–122. [Google Scholar]
  120. Manasyan, Y.S. Helminths of Micromammals in Armenia. Ph.D. Thesis, Yerevan State University, Yerevan, Armenia, 1992. [Google Scholar]
  121. Movsesyan, S.O.; Nikoghosian, M.A.; Petrosian, R.A.; Vlasov, E.A.; Kuznetsov, D.N. Nematodes of rodents of Armenia. Ann. Parasitol. 2018, 64, 173–180. [Google Scholar] [PubMed]
  122. Epe, C.; Coati, N.; Schnieder, T. Results of parasitological examinations of faecal samples from horses, ruminants, pigs, dogs, cats, hedgehogs and rabbits between 1998 and 2002. Deutsch. Tierärztl. Wochenschr. 2004, 111, 243–247. [Google Scholar]
  123. Raue, K.; Heuer, L.; Bohm, C.; Wolken, S.; Epe, C.; Strube, C. 10-year parasitological examination results (2003 to 2012) of faecal samples from horses, ruminants, pigs, dogs, cats, rabbits and hedgehogs. Parasitol. Res. 2017, 116, 3315–3330. [Google Scholar] [CrossRef] [PubMed]
  124. Hofmannova, L.; Hauptman, K.; Huclova, K.; Kvetonova, D.; Sak, B.; Kvac, M. Cryptosporidium erinacei and C. parvum in a group of overwintering hedgehogs. Eur. J. Protistol. 2016, 56, 15–20. [Google Scholar] [CrossRef]
  125. Takeuchi, M.; Hideaki, K.; Asakawa, M. Parasites obtained from the Amur hedgehogs (Erinaceus amurensis) in Shizuoka prefecture, Japan. Jpn. J. Zoo Wildl. Med. 2017, 22, 47–50. [Google Scholar] [CrossRef] [Green Version]
  126. Brander, P.; Denzler, T.; Henzi, M. Capillaria hepatica in a dog and a hedgehog. Schweiz. Arch. Tierheilk. 1990, 132, 365–370. [Google Scholar]
  127. Sharpilo, L.D. On the current state of knowledge of the helminth fauna of insectivores, lagomorphs and rodents in the Ukrainian SSR. In Parasites, Intermediate Hosts and Vectors; Mazurmovich, B.N., Ed.; Naukova Dumka: Kiev, Ukraine, 1966; pp. 232–242. [Google Scholar]
  128. Hofmannova, L.; Jurankova, J. Survey of Toxoplasma gondii and Trichinella spp. in hedgehogs living in proximity to urban areas in the Czech Republic. Parasitol. Res. 2019, 118, 711–714. [Google Scholar] [CrossRef]
  129. Vagin, N.A.; Malysheva, N.S.; Vlasov, E.A.; Samofalova, N.A.; Uspensky, A.V.; Odoevskaya, I.M.; Vagin, Y.A. Finding of Trichinella in northern white-breasted hedgehogs (Erinaceus roumanicus) in the Kursk oblast. Theor. Pract. Paras. Dis. Contr. 2016, 17, 100–102. [Google Scholar]
  130. Majeed, S.; Morris, P.; Cooper, J. Occurrence of the lungworms Capillaria and Crenosoma spp. in British hedgehogs (Erinaceus europaeus). J. Comp. Pathol. 1989, 100, 27–36. [Google Scholar] [CrossRef]
  131. Allen, S.; Greig, C.; Rowson, B.; Gasser, R.B.; Jabbar, A.; Morelli, S.; Morgan, E.R.; Wood, M.; Forman, D. DNA Footprints: Using Parasites to Detect Elusive Animals, Proof of Principle in Hedgehogs. Animals 2020, 10, 1420. [Google Scholar] [CrossRef] [PubMed]
  132. Barradas, P.F.; Flores, A.R.; Mateus, T.L.; Carvalho, F.; Gartner, F.; Amorim, I.; Mesquita, J.R. Crenosoma striatum in lungs of European hedgehogs (Erinaceus europeus) from Portugal. Helminthologia 2020, 57, 179–184. [Google Scholar] [CrossRef]
  133. Alvarez, F.; Iglesias, R.; Bos, J.; Rey, J.; Sanmartin Duran, M.L. Lung and hearth nematodes in some Spanish mammals. Wiad. Parazytol. 1991, 37, 481–490. [Google Scholar]
  134. Barus, V.; Procopic, J. The systematic position and the distribution of nematodes of genus Crenosoma Molin, 1861 parasitic in the hedghog (Erinaceus europeus). Vest. Ceskosl. Spol. Zool. 1972, 36, 6–11. [Google Scholar]
  135. Fedoseev, S.D. To the nematode fauna of mammals in the Gorky Oblast. Proceed. Gorky State Ped. Inst. 1937, 1, 121–133. [Google Scholar]
  136. Naem, S.; Tavakoli, M.; Javanbakht, J.; Alimohammadi, S.; Farshid, A.A.; Mohammad Hassan, M.A. Macroscopic and microscopic examination of pulmonary Crenosoma striatum in hedgehog. J. Parasit. Dis. 2014, 38, 185–189. [Google Scholar] [CrossRef] [Green Version]
  137. Rodonaya, T.E. Helminth fauna of wild mammals in Lagodekhi Nature Reserve. Proceed. Inst. Zool. Acad. Sci. Georgian SSR 1956, 14, 147–187. [Google Scholar]
  138. Gerichter, C.B. Two new lung nematodes from Near-East mammals. Parasitology 1951, 41, 184–188. [Google Scholar] [CrossRef]
  139. Gorgani, T.; Naem, S.; Farshid, A.A.; Otranto, D. Scanning electron microscopy observations of the hedgehog stomach worm, Physaloptera clausa (Spirurida: Physalopteridae. Parasites Vectors 2013, 6, 87. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  140. Nematollahi, A.; Helan, J.A.; Golezardy, H.; Zaboli, N.; Nouruzi, M.; Azari, M. Parasitic fauna of east European hedgehog (Erinaceus concolor) and their pathological aspects in Iran. Adv. Zool. Botan. 2014, 2, 1–5. [Google Scholar] [CrossRef]
  141. Chen, H.-X.; Ju, H.-D.; Li, Y.; Li, L. Further study on Physaloptera clausa (Spirurida: Physalopteridae) from the Amur hedgehog Erinaceus amurensis Schrenk (Eulipotyphla: Erinaceidae). Acta Parasitol. 2017, 62, 846–852. [Google Scholar] [CrossRef] [PubMed]
  142. Oldham, J.N. Studies on parasites of the grey squirrel (Sciurus carolinensis Gmelin) from South Eastern England. I.—Helminth parasites. J. Helminthol. 1961, 35 (Suppl. S1), 127–130. [Google Scholar] [CrossRef] [PubMed]
  143. Miquel, J.; Blasco, S.; Marchand, B.; Torres, J.; Feliu, C. A scanning electron microscope study of the female of Pterygodermatites (Pterygodermatites) plagiostoma (Nematoda, Rictulariidae) in a new host. Vie Milieu/Life Environ. 1997, 47, 213–220. [Google Scholar]
  144. Heckmann, R.A.; Amin, O.M.; Halajian, A.; El-Naggar, A.M. The morphology and histopathology of Nephridiacanthus major (Acanthocephala: Oligacanthorhynchidae) from hedgehogs in Iran. Parasitol. Res. 2013, 112, 543–548. [Google Scholar] [CrossRef] [PubMed]
  145. James, P.M. On some helminths from British small mammals, with a re-description of Echinorhynchus rosai Porta, 1910. J. Helminthol. 1954, 28, 183–188. [Google Scholar] [CrossRef]
  146. Skuballa, J.; Taraschewski, H.; Petney, T.N.; Pfäffle, M.; Smales, L.R. The avian acanthocephalan Plagiorhynchus cylindraceus (Palaeacanthocephala) parasitizing the European hedgehog (Erinaceus europaeus) in Europe and New Zealand. Parasitol. Res. 2010, 106, 431–437. [Google Scholar] [CrossRef]
  147. Lisitsyna, O.I.; Miroshnichenko, A.I. Acanthocephala and Monogenea. Catalogue of Helminths of Vertebrates of Ukraine; I.I. Schmalhausen Institute of Zoology of National Academy of Sciences of Ukraine: Kiev, Ukraine, 2008; pp. 3–138. [Google Scholar]
  148. Laubmeier, E. Untersuchungen uber die Endoparasiten des Igels (Erinaceus europaeus) bei Freilebenden und in Menschlicher Obhut Uberwinterten Tieren Sowie Entwurmungsversuche mit Ivermectin. Ph.D. Thesis, Ludwig-Maximilians-Universitat, Munchen, Germany, 1985. [Google Scholar]
  149. Janicki, C. Zur Kenntnis einiger Säugetiercestoden. Zool. Anst. Univ. Bas. 1904, 27, 770–782. [Google Scholar]
  150. Yalden, D.W. The food of the hedgehog in England. Acta Theriol. 1976, 21, 401–424. [Google Scholar] [CrossRef]
  151. Wroot, A.J. Foraging in the European hedgehog, Erinaceus europaeus. Mammal. Rev. 1985, 15, 1–2. [Google Scholar]
  152. Faltynkova, A.; Nasinkova, V.; Kablaskova, L. Larval trematodes (Digenea) of the great pond snail, Lymnaea stagnalis (L.), (Gastropoda, Pulmonata) in Central Europe: A survey of species and key to their identification. Parasite 2007, 14, 39–51. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  153. Radev, V.; Kanev, I.; Khrusanov, D.; Fried, B. Reexamination of the life cycle of Isthmiophora melis (Trematoda: Echinostomatidae) on material from southeast Europe. Parazitologiia 2009, 43, 445–453. [Google Scholar] [PubMed]
  154. Kirillova, N.Y.; Kirillov, A.A. Trematodes (Trematoda) of small mammals in the Middle Volga region. Parasitologiia 2009, 43, 225–239. [Google Scholar]
  155. Joyeux, C. Recherches sur le cycle evolutif d’Hymenolepis erinacei (Gmelin, 1789). Aniils Parasif. Hum Comp. 1927, 5, 20–26. [Google Scholar] [CrossRef]
  156. Procopic, J. The life cycle of the cestode Rodentolepis erinacei (Gmelin, 1789). Fol. Parasitol. 1971, 18, 27–32. [Google Scholar]
  157. Sudarikov, V.E.; Shigin, A.A.; Kurochkin, Y.V.; Lomakin, V.V.; Sten’ko, R.P.; Yurlova, N.I. Metacercariae of Trematodes—Parasites of Freshwater Aquatic Organisms in Central Russia; Nauka: Moscow, Russia, 2002; pp. 3–298. [Google Scholar]
  158. Ryzhikov, K.M.; Gvozdev, E.V.; Tokobaev, M.M.; Shaldybin, L.C.; Matsaberidze, G.V.; Merkusheva, I.V.; Nadtochiy, E.V.; Khokhlova, I.G.; Sharpilo, L.D. Keys to the Helminths of Rodents in the USSR Fauna, Cestodes and Trematodes; Nauka: Moscow, Russia, 1978; pp. 3–232. [Google Scholar]
  159. Stocker, L. The Complete Hedgehog; Chatto & Windus: London, UK, 1987; pp. 3–175. [Google Scholar]
  160. Young, R.P.; Davison, J.; Trewby, I.D.; Wilson, G.J.; Delahay, R.J.; Doncaster, C.P. Abundance of hedgehogs (Erinaceus europaeus) in relation to the density and distribution of badgers (Meles meles). J. Zool. 2006, 269, 349–356. [Google Scholar] [CrossRef]
  161. Hof, A.R. A Study of the Current Status of the Hedgehog (Erinaceus europaeus), and Its Decline in Great Britain since 1960. Ph.D. Thesis, University of London, London, UK, 2009. [Google Scholar]
  162. Kirillov, A.A.; Ruchin, A.B.; Fayzulin, A.I.; Chihlyaev, I.V. Helminths of reptiles of Mordovia: Advance information. Proceed. Mord. State Nat. Res. 2015, 14, 243–255. [Google Scholar]
  163. Kirillov, A.A.; Kirillova, N.Y. Overview of helminths in reptiles of the National park “Samarskaya Luka” (Russia). Nat. Conserv. Res. 2018, 3, 73–82. [Google Scholar] [CrossRef] [Green Version]
  164. Kirillov, A.A.; Kirillova, N.Y. Helminth fauna of reptiles in the National park “Smolny”, Russia. Nat. Conserv. Res. 2021, 6, 9–22. [Google Scholar] [CrossRef]
  165. Kirillov, A.A.; Kirillova, N.Y. First finding of spirurid larva (Chromadorea, Spirurida) in the common European viper Vipera berus (Linnaeus, 1758) of the Russian fauna. IOP Conf. Ser. Earth Envir. Sci. 2021, 818, 012017. [Google Scholar] [CrossRef]
  166. Grewal, P.S.; Grewal, S.K.; Tan, L.; Adams, B.J. Parasitism of molluscs by nematodes: Types of associations and evolutionary trends. J. Nematol. 2003, 35, 146–156. [Google Scholar] [PubMed]
  167. Barus, V.K.; Blazek, K. The life cycle and the pathogenicity of the nematode Crenosoma striatum (Zeder, 1800). Folia Parasitol. 1971, 18, 215–226. [Google Scholar]
  168. Romashov, B.V. Life cycle of nematoda Capillaria erinacei (Capillariidae). Helminthologia 1981, 17, 181–189. [Google Scholar]
  169. Lisitsyna, O.I. Taxonomic and ecology diversity of acanthocephalans of the fauna of Ukraine. In Parasitology in Changing World, Proceedings of the V Congress of Russian Society of Parasitologists of the Russian Academy of Sciences, 23–26 September 2013, Novosibirsk, Russia; Galaktionov, K.V., Ed.; Institute of Systematics and Ecology of Animals of Siberian Branch of RAS: Novosibirsk, Russia, 2013; p. 107. [Google Scholar]
  170. Drabick, J.J.; Egan, J.E.; Brown, S.L.; Vick, R.G.; Sandman, B.M.; Neafie, R.C. Dicroceliasis (lancet fluke disease) in an HIV seropositive man. JAMA 1988, 259, 567–568. [Google Scholar] [CrossRef] [PubMed]
  171. Akbaev, M.S.; Vodyanov, A.A.; Kosminkov, N.E.; Yatusevich, A.I.; Pashkin, P.I.; Vasilevich, F.I. Parasitology and Invasive Animal Diseases; Kolos: Moscow, Russia, 1998; pp. 3–743. [Google Scholar]
  172. Taylor, M.A.; Coop, R.L.; Wall, R.L. Veterinary Parasitology, 3rd ed.; Blackwell Publishing: Oxford, UK, 2007; pp. 3–874. [Google Scholar]
  173. Lalosevic, D.; Lalosevic, V.; Klem, I.; Stanojev-Jovanovic, D.; Pozio, E. Pulmonary Capillariasis Miming Bronchial Carcinoma. Am. J. Trop. Med. Hyg. 2008, 78, 14–16. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  174. Kuchta, R.; Scholz, T.; Brabec, J.; Narduzzi-Wicht, B. Diphyllobothrium, Diplogonoporus and Spirometra. In Biology of Foodborne Parasites; Xiao, L., Ryan, U., Feng, Y., Eds.; CRC Press: Boca Raton, FL, USA, 2015; pp. 299–326. [Google Scholar]
  175. Gaevskaya, A.V. The World of Human Parasites. 2. Nematodes and Foodborne Nematodoses; ECOSI-Hydrophysics: Sevastopol, Russia, 2016; pp. 3–442. [Google Scholar]
  176. Gaevskaya, A.V. The World of Human Parasites. 3. Cestodes and Foodborne Cestodoses; Institute of Biology of the Southern Seas RAS: Sevastopol, Russia, 2017; pp. 3–357. [Google Scholar]
  177. Kuchta, R.; Kołodziej-Sobocińska, M.; Brabec, J.; Młocicki, D.; Sałamatin, R.; Scholz, T. Sparganosis (Spirometra) in Europe in the molecular era. Clin. Infect. Dis. 2021, 72, 882–890. [Google Scholar] [CrossRef]
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Figure 1. Species richness of helminths in hedgehogs of Erinaceus genus in Palaearctic region.
Figure 1. Species richness of helminths in hedgehogs of Erinaceus genus in Palaearctic region.
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Figure 2. Similarity dendrogram of the helminth faunas in Erinaceus spp. from various countries, obtained by the Morisita index (UPGMA). Cophen. corr.: r = 0.875.
Figure 2. Similarity dendrogram of the helminth faunas in Erinaceus spp. from various countries, obtained by the Morisita index (UPGMA). Cophen. corr.: r = 0.875.
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Table
Table 1. Helminth fauna of Erinaceus roumanicus in Mordovia (Russia).
Table 1. Helminth fauna of Erinaceus roumanicus in Mordovia (Russia).
Helminth SpeciesLocation in HostP, %IR, Spec.MA
Trematoda
    Isthmiophora melis (Schrank, 1788)		small intestine13.02–864.0
Strigea strigis (Schrank, 1788), metacercariamesentery around oesophagus and trachea4.320.1
Cestoda
    Hymenolepis erinacei (Gmelin, 1789)		small intestine52.21–977.8
Nematoda
    Aonchotheca erinacei (Rudolphi, 1819)		stomach, small intestine56.51–14919.5
Physaloptera clausa Rudolphi, 1819stomach1009–42077.4
Crenosoma striatum Zeder, 1800bronchi8.73–180.9
Physocephalus sexalatus (Molin, 1860), juv.walls of stomach and small intestine13.08–1778.6
Agamospirura minuta Sharpilo, 1963gastric mucosa and first third of small intestine4.330.1
Acanthocephala
    Nephridiorhynchus major (Bremser, 1811)		small intestine4.320.1
Table
Table 2. List of helminths of Erinaceus hedgehogs in the Palaearctic region.
Table 2. List of helminths of Erinaceus hedgehogs in the Palaearctic region.
Helminth SpeciesDHostCountryReferences
Trematoda
Brachylaima recurva (Dujardin, 1845)1 EE. concolorGeorgia[55]
2Brachylaima erinacei Blanchard, 1847 (Syn.: Brachylaima helicis (Meckel, 1846))3 PE. europaeusUK[28,56,57,58,59,60,61]
E. europaeusFrance[62]
E. europaeusGermany[59,63,64,65,66,67,68,69,70,71,72]
E. europaeusItaly[73,74,75,76]
E. europaeusSpain[77]
E. europaeusSwitzerland[29,78,79,80]
E. europaeus, E. roumanicusCzech Republic[34,81]
E. europaeus, E. roumanicusPoland[82,83]
E. europaeusRussia[84]
E. concolorIran[85]
Brachylaima sp.-E. europaeusPortugal[86]
E. europaeusDenmark[35]
E. roumanicusGreece[87]
2,4Isthmiophora melis (Schrank, 1788)
Syn.: Euparyphium melis (Schrank, 1788)		5 HE. europaeusCzech Republic[81,88]
E. roumanicusMoldova[30,45]
E. roumanicusBelarus[33,89,90]
E. roumanicusUkraine[91,92]
E. roumanicusRussiathis study
Nephrotrema truncatum (Leuckart, 1842)EE. europaeusAustria[93]
Dicrocoelium dendriticum (Rudolphi, 1819)6 CE. europaeusItaly[73,75]
Dicrocoelium sp.-E. europaeusGermany[69]
Brachylecithum aetechini Dollfus, 1951EE. europaeusItaly[73,75]
Brachylecithum mackoi Casanova et Ribas, 2004EE. europaeusItaly[94]
Rubenstrema exasperatum (Rudolphi, 1819)PE. roumanicusUkraine[92]
2Alaria alata (Goeze, 1782), msc.CE. roumanicusMoldova[30,45]
E. roumanicusBelarus[33,89,90,95]
E. europaeusRussia[84]
E. roumanicusUkraine[91,92]
Strigea falconis Szidat, 1928, mtc.CE. roumanicusBelarus[33,95]
Strigea sphaerula (Rudolphi, 1803), mtc.PE. roumanicusBelarus[33,95]
2,4Strigea strigis (Schrank, 1788), mtc.PE. roumanicusBelarus[89]
E. europaeus, E. roumanicusRussia[84], this study
E. roumanicusUkraine[92]
Cestoda
2,4Hymenolepis erinacei (Gmelin, 1789)
Syn.: Rodentolepis erinacei (Gmelin, 1789), Rodentolepis steudeneri (Janicki, 1904)		PE. europaeusUK[28,57,61,96,97]
E. europaeusGermany[63,64,65,67,69,70,71,72,98]
E. europaeusSwitzerland[80]
E. europaeus, E. roumanicusCzech Republic[34,81,99]
E. europaeus, E. roumanicusSlovakia[99]
E. roumanicusSerbia[100]
E. roumanicusPoland[101]
E. roumanicusBulgaria[32]
E. roumanicusGreece[87]
E. europaeusLithuania[102]
E. roumanicusBelarus[33,89,90,95,103]
E. roumanicusRussia[49,104,105,106,107,108], this study
E. roumanicusUkraine[91,109]
E. concolorArmenia[47]
E. concolorGeorgia[55]
E. concolorTurkey[110]
E. concolorIran[85,111]
Spirometra erinacei (Rudolphi, 1819), plc. (Syn.: Diphyllobothrium erinacei (Rudolphi, 1819))CE. roumanicusBulgaria[32]
E. roumanicusMoldova[30,45]
E. roumanicusBelarus[33,89,90]
Taenia hydatigena Pallas, 1766, larvae (Syn.: Taenia tenuicollis Rudolphi, 1819)CE. roumanicusBelarus[90]
Versteria mustelae (Gmelin, 1790), larvae (Syn.: Taenia mustelae Gmelin, 1790)HE. roumanicusBelarus[33]
Cladotaenia globifera (Batsch, 1786), larvaeHE. europaeusPortugal[112]
Mesocestoides sp., larvae-E. europaeusItaly[73,75,113]
E. roumanicusBulgaria[32] as M. lineatus (Goeze, 1782)
Nematoda
2,4Aonchotheca erinacei (Rudolphi, 1819)
Syn.: Capillaria erinacei (Rudolphi, 1819), Capillaria ovoreticulata Laubmeier, 1985		PE. europaeusUK[56,57,58,61,96]
E. europaeusIreland[114]
E. europaeusItaly[73,74,75,76]
E. europaeusGermany[67,70,71,72]
E. europaeusSwitzerland[29]
E. europaeusPortugal[112]
E. europaeusSpain[77]
E. europaeus, E. roumanicusCzech Republic[41,81,99] as Capillaria sp 2 and 3
E. europaeus, E. roumanicusSlovakia[99,115]
E. roumanicusSerbia[100]
E. europaeus, E. roumanicusPoland[82,83]
E. roumanicusBulgaria[32]
E. roumanicusMoldova[30,45,116]
E. roumanicusBelarus[33,89,90,95,103]
E. europaeus, E. roumanicusRussia[49,107,108,117,118,119], this study
E. roumanicusUkraine[91]
E. concolorArmenia[50,120,121]
E. concolorTurkey[110]
Aonchotheca sp. + Eucoleus sp.
(=Capillaria spp.)		-E. europaeusUK[28,58,59,60]
E. europaeusFinland[16]
E. europaeusDenmark[35]
E. europaeusGermany[59,64,65,66,67,68,69,98,122,123]
E. europaeusSwitzerland[79,80]
E. europaeus, E. roumanicusCzech Republic[34,124]
E. roumanicusGreece[87]
E. concolorIran[85]
Capillariidae sp.-E. europaeusFrance[62]
E. amurensisJapan[125]
2Eucoleus aerophilus (Creplin, 1839) (Syn.: Capillaria aerophila (Creplin, 1839); Thominx aerophilus (Creplin, 1839))CE. europaeusUK[57,58,59,61,97]
E. europaeusGermany[59,63,64,65,66,67,69,70,71,72]
E. europaeusDenmark[35]
E. europaeusSwitzerland[29]
E. europaeus, E. roumanicusCzech Republic[34]
E. europaeus, E. roumanicusPoland[82,83]
E. roumanicusBelarus[33,95,103]
E. europaeus, E. roumanicusRussia[49,84,107,108,117,118,119]
E. roumanicusUkraine[91]
E. concolorTurkey[110]
E. concolorIran[85]
2Eucoleus tenuis Dujardin, 1845EE. europaeusUK[96]
E. europaeus, E. roumanicusCzech Republic[99]
E. europaeusSpain[77]
E. roumanicusBulgaria[32]
E. roumanicusRussia[106]
Pterothominx erinacei (Andrejko, 1969) (Syn.: Thominx erinacei Andrejko, 1969)EE. roumanicusMoldova[30,45,116]
Calodium hepaticum (Bancroft, 1893) (Syn.: Hepaticola hepatica (Bancroft, 1893))CE. europaeusDenmark[35]
E. europaeusSpain[77]
E. europaeusSwitzerland[79,126]
E. roumanicusUkraine[127]
2Trichinella spiralis Owen, 1835CE. europaeusBelgium[31]
E. europaeusCzech Republic[128]
E. roumanicusBulgaria[32]
E. roumanicusBelarus[33]
E. europaeusRussia[48,84]
2Trichinella nativa Britov et Boev, 1972, juvenilesHE. roumanicusRussia[129]
Trichuris sp.-E. europaeusGermany[69]
E. europaeusSwitzerland[79,80]
Parastrongyloides winchesi Morgan, 1928HE. roumanicusBelarus[33]
E. roumanicusUkraine[91]
2,4Crenosoma striatum Zeder, 1800PE. europaeusUK[28,56,58,59,60,61,96,97,130,131]
E. europaeusIreland[114]
E. europaeusFrance[62]
E. europaeusDenmark[35]
E. europaeusGermany[59,63,64,65,66,67,68,69,70,71,72,98,122,123]
E. europaeusSwitzerland[29,79,80]
E. europaeusItaly[73,75,76]
E. roumanicusGreece[87]
E. europaeusFinland[16]
E. roumanicusPortugal[86,112,132]
E. europaeusSpain[77,133]
E. roumanicusSerbia[100]
E. europaeus, E. roumanicusCzech Republic[34,81,99,124,134]
E. europaeus, E. roumanicusPoland[82,83,101]
E. europaeus, E. roumanicusSlovakia[99,115,134]
E. roumanicusBelarus[33,89,90,95,103]
E. europaeus, E. roumanicusRussia[48,49,84,107,108,118,119,135], this study
E. roumanicusUkraine[91,109]
E. concolorTurkey[110]
E. concolorIran[85,111,136]
Crenosoma lofocara Gerichter, 1951PE. roumanicusBulgaria[32]
E. concolorGeorgia[137]
E. concolorSiria[138]
Ancylostoma sp.-E. europaeusSwitzerland[80]
2,4Physaloptera clausa Rudolphi, 1819HE. europaeusGermany[67,70,72]
E. europaeusItaly[75,76]
E. europaeusSpain[77]
E. roumanicusGreece[87]
E. europaeus, E. roumanicusCzech Republic[34,81,99]
E. europaeus, E. roumanicusSlovakia[99,115]
E. roumanicusBulgaria[32]
E. europaeus, E. roumanicusPoland[82,83,101]
E. roumanicusMoldova[30,45,116]
E. roumanicusBelarus[33,89,90,95,103]
E. europaeus, E. roumanicusRussia[49,104,105,107,108,118,119,135], this study
E. roumanicusUkraine[91,109,127]
E. concolorTurkey[110]
E. concolorIran[85,111,139,140]
E. amurensisChina[141]
Haemonchus contortus (Rudolphi, 1803)CE. europaeusItaly[75]
Trichostrongylus retortaeformis (Zeder, 1800)CE. europaeusUK[142]
2Porrocaecum sp., juveniles-E. europaeusPortugal[112]
E. europaeusSpain[77]
E. roumanicusBelarus[95]
E. roumanicusRussia[49,107,108,118,119] as P. depressum Zeder, 1800
E. amurensisJapan[125]
2,4Physocephalus sexalatus (Molin, 1860), juvenilesPE. roumanicusBulgaria[32]
E. roumanicusBelarus[33,90]
E. roumanicusRussiathis study
Ascarops strongylina (Rudolphi, 1819), juvenilesCE. roumanicusBulgaria[32]
Spirocerca lupi (Rudolphi, 1809), juvenilesCE. roumanicusBulgaria[32]
Gongylonema sp.-E. europaeusGermany[67]
E. europaeusItaly[73]
Spirura rytipleurites Deslongchamps, 1824EE. europaeusItaly[73,75]
E. roumanicusSlovakia[99]
E. europaeusSpain[77]
E. concolorArmenia[50,120]
Spirura sp.-E. europaeusPortugal[112]
Rictularia plagiostoma (Wedl, 1861) (Syn.: Pterygodermatites plagiostoma Wedl, 1861)EE. europaeusSpain[77,143]
E. europaeusPortugal[86]
2,4Agamospirura minuta Sharpilo, 1963, juvenilesPE. roumanicusRussiathis study
Monovaria sp.-E. amurensisJapan[125]
Acanthocephala
2,4Nephridiorhynchus major (Bremser, 1811)PE. europaeusItaly[73,75]
E. europaeus, E. roumanicusCzech Republic[34,81,99]
E. europaeusSpain[77]
E. roumanicusBulgaria[32]
E. roumanicusRussiathis study
E. concolorArmenia[50,120]
E. concolorGeorgia[55,137,141]
E. concolorTurkey[110]
E. concolorIran[111,144]
Oligacanthorhynchus erinacei (Rudolphi, 1793)PE. europaeusUK[58]
2Moniliformis moniliformis (Bremser, 1811)CE. roumanicusRussia[104]
E. concolorGeorgia[55]
Plagiorhynchus cylindraceus (Goeze, 1782) (Syn.: Plagiorhynchus formosus Van Cleave, 1918), Prosthorhynchus rosai (Porta, 1910))H,
7 NZ		E. europaeusUK[59,61,145,146]
E. europaeusGermany[59,146]
E. europaeus, E. roumanicusCzech Republic[34,81,99]
Plagiorhynchus gracilis (Petrotschenko, 1958), juv.PE. roumanicusUkraine[147]
Plagiorhynchus sp. (Syn.: Prosthorhynchus Kostylev, 1915)-E. europaeusUK[28]
E. europaeusSpain[77]
Sphaerirostris picae (Rudolphi, 1819) (Syn.: Sphaerirostris teres (Rudolphi, 1819)), juv.PE. roumanicusUkraine[147]
Note: D—geographical distribution, 1—Europe, 2—helminth species found in Russia, 3—Palaearctic, 4—helminth species found in our study, 5—Holarctic, 6—Cosmopolitan, 7—New Zealand.
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MDPI and ACS Style

Kirillov, A.A.; Kirillova, N.Y.; Ruchin, A.B. Helminths of Erinaceus roumanicus (Eulipotyphla, Erinaceidae) in Mordovia (Russia) with an Overview of Helminth Fauna of Erinaceus spp. Inhabiting the Palaearctic Region. Diversity 2022, 14, 165. https://doi.org/10.3390/d14030165

AMA Style

Kirillov AA, Kirillova NY, Ruchin AB. Helminths of Erinaceus roumanicus (Eulipotyphla, Erinaceidae) in Mordovia (Russia) with an Overview of Helminth Fauna of Erinaceus spp. Inhabiting the Palaearctic Region. Diversity. 2022; 14(3):165. https://doi.org/10.3390/d14030165

Chicago/Turabian Style

Kirillov, Alexander A., Nadezhda Yu. Kirillova, and Alexander B. Ruchin. 2022. "Helminths of Erinaceus roumanicus (Eulipotyphla, Erinaceidae) in Mordovia (Russia) with an Overview of Helminth Fauna of Erinaceus spp. Inhabiting the Palaearctic Region" Diversity 14, no. 3: 165. https://doi.org/10.3390/d14030165

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