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Helminths of Erinaceus roumanicus (Eulipotyphla, Erinaceidae): History
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Subjects: Parasitology
Contributor:
Alexander Kirillov

Among Eulipotyphla, the Erinaceinae subfamily containing the well-known hedgehogs of Eurasia and Africa deserves special attention. The helminth fauna of the Northern white-breasted hedgehog Erinaceus roumanicus was studied in the Republic of Mordovia (Russia) for the first time. A total of 54 parasite species were recorded across Erinaceus europaeus, E. roumanicus, E. concolor and E. amurensis. 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.

  • Erinaceus spp.
  • parasitic worms
  • Western European hedgehog
  • Northern white-breasted hedgehog
  • Southern white-breasted hedgehog
  • Amur hedgehog
  • Palaearctic

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].
Hedgehogs are nocturnal and spend most of their active time foraging [15],[16]. 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 [17]. Hedgehogs are often found in urban and suburban environments [16].
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 [18]. 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.

2. Helminths of Erinaceus roumanicus in Mordovia (Russia)

Nine helminth species in twenty-three hedgehogs from the Republic of Mordovia were found, including two trematodes, one cestode, five nematodes, and one acanthocephalan (Table 1). The total infestation of hedghogs by helminths was 100%, the index of helminth mean abundance was 118.5. The intensity range of hedgehog invasion by helminths was from 17 to 514 specimens. Most of 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 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.
Table 1. Helminth fauna of Erinaceus roumanicus in Mordovia (Russia).
Helminth Species Location in Host P, % IR, Spec. MA
Trematoda
Isthmiophora melis (Schrank, 1788)		 small intestine 13.0 2–86 4.0
Strigea strigis (Schrank, 1788), metacercaria mesentery around oesophagus and trachea 4.3 2 0.1
Cestoda
Hymenolepis erinacei (Gmelin, 1789)		 small intestine 52.2 1–97 7.8
Nematoda
Aonchotheca erinacei (Rudolphi, 1819)		 stomach, small intestine 56.5 1–149 19.5
Physaloptera clausa Rudolphi, 1819 stomach 100 9–420 77.4
Crenosoma striatum Zeder, 1800 bronchi 8.7 3–18 0.9
Physocephalus sexalatus (Molin, 1860), juv. walls of stomach and small intestine 13.0 8–177 8.6
Agamospirura minuta Sharpilo, 1963 gastric mucosa and first third of small intestine 4.3 3 0.1

Acanthocephala

Nephridiorhynchus major (Bremser, 1811)

 small intestine 4.3 2 0.1

 

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

The helminth fauna of Erinaceus spp. in 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. A significantly smaller number of parasite species was found in E. concolor (12) and E. amurensis (4). The greatest richness of the helminth fauna in hedgehogs was in Russia and Belarus, where 17 species of parasites were found in each country (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 (Figure 1).

Diversity 14 00165 g001 550
Figure 1. Species richness of helminths in hedgehogs of Erinaceus genus in Palaearctic region.
The helminth communities in hedgehogs is 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 (in each country); five helminth species – in Denmark, Slovakia and Georgia. Four species of parasites were found in E. concolor from Armenia. Three helminth species of were noted in hedgehogs in France, Serbia and Japan (in each country).  In other seven countries, data on hedgehog parasites include only 1–2 species (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).

Comparative analysis of the helminth species composition in Erinaceus spp. from different countries showed, on the one hand, the originality of the parasite faunas of each hedgehog species, on the other, the similarity of the helminth communities of Erinaceus spp. from different 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 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 1). As a result, the average and low degree of similarity of the helminth faunas of different species of Erinaceus hedgehogs index 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 different 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), 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 different species of hedgehogs from distant countries has 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) 
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 [34],[35],[36]. In addition, the diet of hedgehogs includes amphibians; small reptiles; small mammals; birds, their young, and their eggs; and carrion [34].
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.

4. 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, nine species of helminths in hedgehogs were found. 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.
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.

This entry is adapted from the peer-reviewed paper 10.3390/d14030165

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