Helminths of Erinaceus roumanicus (Eulipotyphla, Erinaceidae): Comparison
View Latest Version
Please note this is a comparison between Version 2 by Yvaine Wei and Version 1 by Alexander Alexandrovich 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 [16][17]. Hedgehogs are often found in urban and suburban environments [1617].
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 [1815]. Three hedgehog species inhabit Western Palaearctic: E. europaeus, E. roumanicus, and E. concolor [1918]. 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 [19][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 [21][22],[2324],[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  [2524]. 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 [21][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 [1825]. 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

Diversity 14 00165 g001 550
Figure 1. Species richness of helminths in hedgehogs of Erinaceus genus in Palaearctic region.
Figure 1. SpThe helminth cies richness of helminthsommunities 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 of Erinaceus gin Moldova, Turkey and Poland (in each country); five helminus 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 th 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.

References

  1. Otso Huitu; Kai Norrdahl; Erkki Korpimäki; Competition, predation and interspecific synchrony in cyclic small mammal communities. Ecography 2004, 27, 197-206, 10.1111/j.0906-7590.2003.03684.x.Hiutu, O.; Norrdahl, K.; Koprimäki, E. Competition, predation and interspecific synchrony in cyclic small mammal communities. Ecography 2004, 27, 197–206.
  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). Nature Conservation Research 2020, 5, 36-46, 10.24189/ncr.2020.011.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.
  3. Bashinskiy, I.V.; Beaver impact on water coverage of forest-steppe territories (Penza Region, European Russia). Nature Conservation Research 2021, 6, 88-97, 10.24189/ncr.2021.016.Bashinskiy, I.V. Beaver impact on water coverage of forest-steppe territories (Penza region, European Russia). Nat. Conserv. Res. 2021, 6, 88–97.
  4. Lazutkin, A.N.; Long-term monitoring of red-backed voles number in Magadan Nature Reserve in 1980–2021. Proceedings of Mordovia State Nature Reserve 2021, 29, 319-325.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.
  5. Yakimova, A.E.; Irina S. Gaidysh; The species composition and abundance of terrestrial small mammals in the Finnish-Russian Friendship Nature Reserve. Nature Conservation Research 2021, 6, 127-136, 10.24189/ncr.2021.028.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.
  6. V. A. Gremyachikh; D. A. Kvasov; E. S. Ivanova; Patterns of mercury accumulation in the organs of bank vole Myodes glareolus (Rodentia, Cricetidae). Biosystems Diversity 2019, 27, 329-333, 10.15421/011943.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.
  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, 10.24189/ncr.2019.049.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.
  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. Nature Conservation Research 2020, 5, 1-20, 10.24189/ncr.2020.001.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.
  9. Robert Poulin; Serge Morand; The Diversity of Parasites. The Quarterly Review of Biology 2000, 75, 277-293, 10.1086/393500.Poulin, R.; Morand, S. The diversity of parasites. Quart. Rev. Biol. 2000, 75, 277–293.
  10. Alessandro Balestrieri; Andrea Gazzola; Giulio Formenton; Luca Canova; Long-term impact of agricultural practices on the diversity of small mammal communities: a case study based on owl pellets. Environmental Monitoring and Assessment 2019, 191, 725, 10.1007/s10661-019-7910-5.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.
  11. Laurent Ahissa; Bertin K. Akpatou; Hilaire K. Bohoussou; Blaise Kadjo; Inza Koné; University of Man; Swiss Centre for Scientific Research in Côte d’Ivoire; Species composition and community structure of terrestrial small mammals in Tanoé-Ehy Swamp Forest (South-East Ivory Coast): implication for conservation. Nature Conservation Research 2020, 5, 53-63, 10.24189/ncr.2020.005.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.
  12. Margarita I. Kononova; Yuri A. Prisniy; Helminthes of mouse-like rodents in the Belogorye State Nature Reserve (Russia). Nature Conservation Research 2020, 5, 11-18, 10.24189/ncr.2020.036.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.
  13. Nadezhda Kirillova; Alexander Ruchin; Alexander Kirillov; Helminths in Myomorph Rodents (Rodentia, Myomorpha) from the National Park “Smolny” and Its Surroundings (European Russia). Forests 2021, 12, 1510, 10.3390/f12111510.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.
  14. Boris V. Romashov; Irina M. Odoevskaya; Natalya B. Romashova; Nona A. Golubova; Ecology of trichinellosis transmission in the Voronezh State Nature Reserve and adjacent areas, Russia. Nature Conservation Research 2021, 6, 1-15, 10.24189/ncr.2021.023.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.
  15. Reeve, N.J. . Hedgehogs; T & AD Poyser Natural History: London, UK, 1994; pp. 313.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.
  16. Anni Rautio; Marja Isomursu; Anu Valtonen; Varpu Hirvelä-Koski; Mervi Kunnasranta; Mortality, diseases and diet of European hedgehogs (Erinaceus europaeus) in an urban environment in Finland. Mammal Research 2015, 61, 161-169, 10.1007/s13364-015-0256-7.Reeve, N.J. Hedgehogs; T & AD Poyser Natural History: London, UK, 1994; pp. 3–313.
  17. Jourde, P. . Le hérisson d’Europe; Delachaux et Niestlé: Paris, France, 2013; pp. 207.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.
  18. Hutterer, R. Order Erinaceomorpha; Wilson, D.E., Reeder, D.M., Eds.; Johns Hopkins University Press: Baltimore, USA, 2005; pp. 220-311.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.
  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. 272.Holz, H. Studies on European hedgehogs. Z. Zool. Syst. Evolut. 1978, 16, 148–165.
  20. Holz, H.; Studies on European hedgehogs. Z. Zool. Syst. Evolut.-forsch. 1978, 16, 148-165.Krystufek, B. The distribution of hedgehogs (Erinaceus L., 1758, Insectivora, Mammalia) in Western Yugoslavia. Biosistematika 1983, 9, 71–78.
  21. Krystufek, B.; The distribution of hedgehogs (Erinaceus L., 1758, Insectivora, Mammalia) in Western Yugoslavia. Biosistematika 1983, 9, 71-78.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.
  22. J. M. Seddon; F. Santucci; N. Reeve; G. M. Hewitt; Caucasus Mountains divide postulated postglacial colonization routes in the white-breasted hedgehog, Erinaceus concolor. Journal of Evolutionary Biology 2002, 15, 463-467, 10.1046/j.1420-9101.2002.00408.x.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.
  23. R. S. Sommer; When east met west: the sub‐fossil footprints of the west European hedgehog and the northern white‐breasted hedgehog during the Late Quaternary in Europe. Journal of Zoology 2007, 273, 82-89, 10.1111/j.1469-7998.2007.00302.x.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).
  24. Amori, G. Erinaceus europaeus. The IUCN Red List of Threatened Species 2016: e.T29650A2791303. 2016. Available at https://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T29650A2791303.en. (accessed 13 February 2020)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.
  25. A. S. Bogdanov; A. A. Bannikova; Yu. M. Pirusskii; N. A. Formozov; The first genetic evidence of hybridization between West European and Northern white-breasted hedgehogs (Erinaceus europaeus and E. roumanicus) in Moscow region. Biology Bulletin 2009, 36, 647-651, 10.1134/s106235900906017x.Jourde, P. Le Hérisson d’Europe; Delachaux et Niestlé: Paris, France, 2013; pp. 3–207.
  26. Cassola, F. Erinaceus amurensis. The IUCN Red List of Threatened Species 2016: e.T40604A22325640. 2016. Available at http://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T40604A22325640.en (accessed 20 January 2022)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.Riley, P.Y.; Chomel, B.B. Hedgehog zoonoses. Emerg. Infect. Dis. 2005, 11, 1–5.
  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.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.
  29. Egli, E. Comparison of physical condition and parasite burdens in rural, suburban and urban hedgehogs Erinaceus europaeus: Implications for conservation. M.Sc. Thesis, Bern University, Switzerland, 2004Egli, 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.
  30. Andreyko, O.F. . . Parasites of mammals of Moldova; Stiintsa: Kishinev, Moldova, 1973; pp. 183.Andreyko, O.F. Parasites of Mammals of Moldova; Stiintsa: Kishinev, Moldova, 1973; pp. 3–186.
  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.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.
  32. Genov, T. . Helminths of insectivores and rodents in Bulgaria; Bulgarian Academy of Sciences : Sofia, Bulgaria, 1984; pp. 348.Genov, T. Helminths of Insectivores and Rodents in Bulgaria; Bulgarian Academy of Sciences Publishing House: Sofia, Bulgaria, 1984; pp. 3–348.
  33. Bychkova, E.I.; Akimova, L.N.; Degtyarik, S.M., Yakovich, M.M.. Helminths of vertebrares and man in Belarus; Belarusskaya Nauka : Minsk, Belarus, 2017; pp. 316.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.
  34. Gabriella Gaglio; Simon Allen; Lee Bowden; Mark Bryant; Eric Morgan; Parasites of European hedgehogs (Erinaceus europaeus) in Britain: epidemiological study and coprological test evaluation. European Journal of Wildlife Research 2010, 56, 839-844, 10.1007/s10344-010-0381-1.Robinson, I.; Routh, A. Veterinary care of the hedgehog. Practice 1999, 21, 128–137.
  35. Wroot, A.J.; Foraging in the European hedgehog, Erinaceus europaeus. Mammal. Rev. 1985, 15, 2.Yalden, D.W. The food of the hedgehog in England. Acta Theriol. 1976, 21, 401–424.
  36. A. Faltýnková; V. Našincová; L. Kablásková; 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, 10.1051/parasite/2007141039.Wroot, A.J. Foraging in the European hedgehog, Erinaceus europaeus. Mammal. Rev. 1985, 15, 1–2.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
ScholarVision Creations
Feedback