Introduction
Originally described from Europe in the late 1700s as one of the earliest recognized cestodes, Taenia erinacei Gmelin, 1791 was named after the mammalian genus Erinaceus (hedgehogs) (Gmelin, Reference Gmelin1791). Further studies revealed that the morphology of T. erinacei corresponded to cestodes attributed to Hymenolepis and a transfer to this genus was proposed (Janicki, Reference Janicki1906; Baer, Reference Baer1932). However, despite the description of Hymenolepis erinacei corresponding to the genus Hymenolepis, Lopez-Neyra (Reference Lopez-Neyra1942) transferred H. erinacei to the genus Dicranotaenia Railliet, 1892. Later, however, the concept for Hymenolepis became further refined (Skrjabin & Matevosyan, Reference Skrjabin and Matevosyan1948) and this study again confirmed the position of D. erinacei within Hymenolepis.
Based on the morphology of the larvocyst stage and strobili of the adult, Spassky (Reference Spassky1954) relegated H. erinacei to the genus Rodentolepis Spassky, 1954. Genov (Reference Genov1984) noticed that cestodes from hedgehogs possessed an unarmed rostellum in both adults and cysticercoids, and referred R. erinacei again to Hymenolepis. Irzhavsky & Ketenchiev (Reference Irzhavsky and Ketenchiev2011) excluded H. erinacei from Hymenolepis and erected a new genus Erinaceolepis Gulyaev & Irzhavsky, 2011, based on their observations that the uterus of H. erinacei is not an irregular network, although Czaplinski & Vaucher (Reference Czaplinski, Vaucher, Khalil, Jones and Bray1994) recognized it as one of the features of the genus Hymenolepis. In the most recent morphological revision of the genus, the cestode species from hedgehogs was confirmed as a congener within Hymenolepis among a larger assemblage of species (Makarikov & Tkach, Reference Makarikov and Tkach2013).
The present study explores the systematic position of H. erinacei based on molecular sequences and phylogenetic analysis. Further, we provide a comparison of morphological characters, analysing their congruence with the molecular phylogeny of the group, and examine the role of host colonization in diversification in several genera of Hymenolepididae.
Materials and methods
We collected road-killed hedgehogs (Erinaceus roumanicus Barrett-Hamilton) in south-eastern Lithuania (table 1). Twenty-six hedgehogs were examined during the period from March to September, 2013–2016. Hedgehogs were dissected near the time of collection. Cestodes were preserved in 70% ethanol, stained in Ehrlich's haematoxylin, differentiated in 70% ethanol with hydrochloric acid, cleared in clove oil and mounted in Canada balsam. Permanent mounted slides of specimens used for morphological studies were deposited in the Institute of Ecology, Nature Research Centre, Vilnius, Lithuania (accession numbers EKOI HELMI 946–949). Measurements are given in micrometres; they are presented as the range followed by the mean and the number of the measurements (n) in parentheses.
Erinaceus roumanicus: dates of collections, places and coordinates (WGS).
dist., district.
Total genomic DNA for molecular analysis was isolated from cestodes according to the protocol proposed by Stunžėnas et al. (Reference Stunžėnas, Petkevičiūtė and Stanevičiūtė2011), with a slight modification described by Petkevičiūtė et al. (Reference Petkevičiūtė, Stunžėnas and Stanevičiūtė2014). A fragment at the 5′ end of the 28S rRNA gene was amplified using the forward primer ZX-1 (5′-ACCCGCTGAATTTAAGCATAT-3′; Scholz et al., Reference Scholz, De Chambrier, Kuchta, Littlewood and Waeschenbach2013) and reverse primer 1500R (5′-GCTATCCTGAGGGAAACTTCG-3′; Olson et al., Reference Olson, Cribb, Tkach, Bray and Littlewood2003; Tkach et al., Reference Tkach, Littlewood, Olson, Kinsella and Swiderski2003). The amplification protocol was the following: 3 min denaturation at 96°C; 40 cycles of 30 s at 95°C, 38 s at 53°C, 1 min 48 s at 70°C; and 8 min final extension at 70°C. New primers were constructed to amplify a partial sequence (650–750 bp) of mitochondrial 16S rRNA gene: forward primer Cyclo16SF (5′-AATAGATAAGAACCGAACTGG–3′) and reverse primer Cyclo16SR (5′-TGCCTTTTGCATCATGCT-3′). The amplification protocol with new primers was the following: 3 min denaturation at 96°C; 38 cycles of 40 s at 94°C, 40 s at 43°C, 1 min 17 s at 72°C; and 10 min final extension at 72°C. Polymerase chain reaction (PCR) products were purified and sequenced in both directions at BaseClear B.V. (Leiden, The Netherlands) using PCR primers. Contiguous sequences were assembled using Sequencher 4.7 software (Gene Codes Corporation, Ann Arbor, Michigan, USA).
Additional 28S rDNA sequences representing genera and species among the Hymenolepididae were downloaded from GenBank and included in pairwise sequence comparisons and phylogenetic analyses: HM138521 Hymenolepis weldensis Greiman & Schmidt, 1988; HM138523 and HM138525 Hymenolepis spp.; AF286917, AY157181, HM138522 and LC064143 Hymenolepis diminuta (Rudolphi, 1819); KT148845 and HM138527 Hymenolepis hibernia Montgomery, Montgomery & Dunn, 1987; GU166233 Rodentolepis asymmetrica (Janicki, 1904); GU166254 Vigisolepis spinulosa (Cholodkowsky, 1906); GU166248 and GU166249 Neoskrjabinolepis schaldybini Spassky, 1947; GU166250 Lineolepis scutigera (Dujardin, 1845); KC789835 Staphylocystoides gulyaevi Greiman, Tkach & Cook, 2013; KC789836 Staphylocystoides parvissima (Voge, 1953); GU166225 and GU166226 Arostrilepis sp.; GU166259 and GU166260 Soricinia infirma (Zarnowski, 1955); GU166269 and GU166271 Pseudobotrialepis globosoides (Soltys, 1954); LC064145 and LM405059 Rodentolepis nana (von Siebold, 1852); GU166268 Rodentolepis fraterna (Stiles, 1906); GU166244 Rodentolepis sp.; AF286918, GU166267, GU166278 and LC064144 Rodentolepis microstoma (Dujardin, 1854); GU969051 Vampirolepis sp.; GU166277 Hymenolepididae sp.; GU166236 and GU166265 Rodentolepis straminea (Goeze, 1782); JQ260805 Staphylocystis brusatae (Vaucher, 1971); GU166274 and GU969049 Staphylocystis furcata (Stieda, 1862); KF257896 Staphylocystis schilleri (Rausch & Kuns, 1950); AF286919 Wardoides nyrocae (Yamaguti, 1935); and as outgroup taxa – AF286914 Raillietina australis (Krabbe, 1869). In the GenBank database, the H. diminuta sequence (accession no. AP017664) was a single 16S rDNA gene sequence representing the genus. Also, available 16S rDNA sequences of Hymenolepididae species were downloaded from GenBank and included in the phylogenetic analyses: AP017664 H. diminuta, AP017665 R. microstoma, KT951722 R. nana, KF257885–KF257887 Staphylocystis sp., KF257888 S. schilleri, KF257889 S. furcata and EU665473 Raillietina australis as outgroup taxa. For the phylogenetic analyses, the sequences were aligned using ClustalW (Thompson et al., Reference Thompson, Higgins and Gibson1994) with an open gap penalty of 15 and gap extension penalty of 6.66. The best-fit model of sequence evolution for phylogenetic analysis was estimated using jModeltest v. 0.1.1 software (Posada, Reference Posada2008). Ambiguously aligned positions were excluded from phylogenetic analysis. Maximum likelihood (ML) phylogenetic trees were obtained and analysed using MEGA v6 (Tamura et al., Reference Tamura, Stecher, Peterson, Filipski and Kumar2013). Branch support was estimated by bootstrap analyses with 1000 replicates. The ML trees were obtained using the general time reversible model with a gamma distribution of rates and a proportion of invariant sites (GTR + G + I) for both the internal transcribed spacer-2 (ITS2) and the 28S gene datasets. Gamma shape and number of invariant sites were estimated from the data. Parsimony analysis based on subtree pruning and regrafting (SPR) was used with default parsimony settings. Estimates of mean evolutionary divergence over sequence pairs within and between groups were calculated using the program MEGA v6.
Results
During the parasitological examination of hedgehogs, H. erinacei was detected for the first time in Lithuania. Specimens of H. erinacei were collected from the intestines of 13 (host numbers 1–3, 10–12, 14, 16, 18–20, 24, 25) of the 26 hedgehogs (50%). The number of cestodes per individual varied from 1 to 328; only two hedgehogs had more than 200 cestodes. The mean intensity was 67 cestodes per host.
Morphological analysis
Four cestodes were used for detailed morphological description. There were no significant differences among our specimens of H. erinacei and those recently re-described by Irzhavsky & Ketenchiev (Reference Irzhavsky and Ketenchiev2011) from E. roumanicus from the Caucasus. Specimens of H. erinacei found in Lithuania were characterized by a slightly smaller scolex and proglottids (table 2) but the position and shape of the genital organs were similar to prior morphological descriptions. The differences could reflect the methods used for preservation during the respective studies. We detected proglottids with atypical numbers or positions of testes in one cestode specimen. Typically, H. erinacei has three testes per proglottid, one poral and two antiporal, but a few proglottids had four testes. The positions of these testes in atypical proglottids were one poral and three antiporal, or two poral and two antiporal. In some proglottids, the positions of testes were two poral and one antiporal. Eggs were typically subspherical, 50–61 × 37–50 (54 × 39, n = 10), numerous, with a thin outer coat. Embryophores were thin, oval 30–38 × 16–20 (30 × 17, n = 10), without filaments, close to the surface of the oncosphere; oncospheres were 27–36 × 14–18 (27 × 15, n = 10) (fig. 1). Embryonic hooks (fig. 1c), typical for Hymenolepis, were different in shape and length, with antero-lateral hooks more robust than the slender postero-lateral, both measuring 10–11 (11, n = 10) in length, guard with a ‘v’-shaped ring surrounding the base of the blade (fig. 1); median hooks 12–13 (12, n = 10) in length.
Hymenolepis erinacei eggs: (a) embryophores with embryonic hooks; (b) egg; (c) embryonic hooks.
The morphological measurements of Hymenolepis erinacei in the present study and in the description of Irzhavsky & Ketenchiev (Reference Irzhavsky and Ketenchiev2011). Measurements are given in micrometres except where otherwise stated.
Differential diagnosis of the eggs
The dimensions of eggs of H. erinacei overlap with those in specimens of Hymenolepis tualatinensis Gardner, 1985; Hymenolepis pseudodiminuta Tenora, Asakawa & Kamiya, 1994; Hymenolepis robertrauschi Gardner, Luedders & Duszynski, 2014; Hymenolepis rymzhanovi Makarikov & Tkach, 2013; Hymenolepis bicaudata Makarikov, Tkach & Bush, 2013; Hymenolepis sulcata (von Linstow, 1879); Hymenolepis folkertsi Makarikov, Nims, Galbreath & Hoberg, 2015; Hymenolepis alterna Makarikov, Tkach, Villa & Bush, 2013 and H. hibernia. In contrast, the embryonic hooks of most of the mentioned species are larger (17–20 in H. tualatinensis, 31–37 in H. pseudodiminuta, 13.1–20.5 in H. robertrauschi, 15–16.5 in H. rymzhanovi, 17.5–19 in H. bicaudata and 16–18 in H. folkertsi). Based on the length of embryonic hooks of those species of the genus Hymenolepis for which the eggs have been described, only two species are similar to H. erinacei. Specimens of H. erinacei differ from those of Hymenolepis haukisalmii Makarikov, Tkach & Bush, 2013 and H. alterna in possessing an ovoid rather than subspherical embryophore. Moreover, compared to H. erinacei, the eggs and oncospheres are smaller in H. haukisalmii (37–46 × 29–34 and 18–20 × 15–17, respectively). The outer coat of H. alterna is relatively thick (Makarikov et al., Reference Makarikov, Tkach and Bush2013, Reference Makarikov, Tkach, Villa and Bush2015c), while it is thin in H. erinacei. There are no detailed descriptions and images of the eggs of H. sulcata or H. hibernia. The eggs of H. hibernia are spherical while those of H. sulcata are oval and have a larger oncosphere (36–43 × 27–39) than H. erinacei (27–36 × 14–18).
Eggs without filaments and with differently shaped embryonic hooks possessing a guard with a ‘v’-shaped ring surrounding the base of the blade also occur in some other hymenolepidid genera from small mammals, i.e. Potorolepis, Staphylocystis and Talpolepis.
Scolices of Potorolepis and Staphylocystis each have a rostellum with hooks. Unfortunately, not all species descriptions contain detailed egg descriptions. It is known that some species of Staphylocystis have an embryophore with poral filaments, while in some these structures have not been observed (Velikanov, Reference Velikanov1997). The eggs of Staphylocystis clydesengeri Tkach, Makarikov & Kinsella, 2013 from Sorex vagrans (Baird, 1857) are similar to those of cestodes of the genus Hymenolepis: they have a thin outer coat, an embryophore without poral filaments and antero-lateral embryonic hooks that are more robust than the postero-lateral and median hooks (Tkach et al., Reference Tkach, Makarikov and Kinsella2013). These eggs differ from those of H. erinacei in size (40–44 × 32–39 in S. clydesengeri and 50–61 × 37–50 in H. erinacei), embryophore shape (subspherical in S. clydesengeri and oval in H. erinacei) and size of embryonic hooks (14.5–16 in S. clydesengeri and 10–13 in H. erinacei).
Gulyaev & Melnikova (Reference Gulyaev, Melnikova and Alimov2005) transferred four species from moles from the genus Hymenolepis to the genus Talpolepis. The eggs of Talpolepis peipingensis (Hsü, 1935), parasitizing moles Mogera robusta Nehring, 1891 from Primorskii Kray (Russia), Talpolepis dymecodontis Sawada & Harada, 1990, parasitizing Dymecodon pilirostris True, 1886 from Japan and Scaptochirus moschatus Milne-Edwards, 1867 from China, as well as Potorolepis gulyaevi Makarikova & Makarikov, 2012, from the bat Rhinolophus sinicus Andersen, 1905 from China, have thick outer coats and the length of the embryonic hooks are 12–16, 14–18 and 13–15, respectively (Sawada & Harada, Reference Sawada and Harada1990; Sawada et al., Reference Sawada, Harada, Oda and Koyasu1992; Gulyaev & Melnikova, Reference Gulyaev, Melnikova and Alimov2005; Makarikova & Makarikov, Reference Makarikova and Makarikov2012); in contrast, the outer coat in H. erinacei is thin and the length of hooks varied from 10 to 13. The outer coat of Talpolepis mogerae Sawada & Koyasu, 1991 is also thin and the oncosphere is oval, but the embryonic hooks are small (7) and the antero-lateral hooks are relatively thin (Sawada & Koyasu, Reference Sawada and Koyasu1991).
The egg shape and hook lengths of H. erinacei are similar to those of Relictolepis feodorovi, another species of hymenolepidid (Gulyaev & Makarikov, Reference Gulyaev and Makarikov2007), but they differ in egg dimensions (37–44 × 27–30 in the latter) and in the shape of the guards (ring-shaped) on the antero-lateral embryonic hooks.
Phylogenetic analysis
Among these specimens of H. erinacei, the partial mitochondrial 16S rRNA gene (855 bp) and partial sequence of nuclear 28S rRNA gene (up to 1517 bp) were amplified and sequenced. The new 16S and 28S sequences for H. erinacei were deposited in GenBank under accession numbers KX928755, KX928756, KX928758 and KX928757. BLAST searches (http://www.ncbi.nlm.nih.gov/blast/Blast.cgi) and comparisons of 28S sequences demonstrated that H. erinacei was most similar to Hymenolepis species obtained from rodents. Maximum likelihood, with the 28S gene dataset consisting of 1230 characters and phylogenetic analysis, placed H. erinacei in a consistently supported clade with other Hymenolepis species, including the type species of the genus, H. diminuta (fig. 2). The sequence of H. erinacei differed from 28S rDNA sequences of H. diminuta in 41 out of 1377 bp (2.98%) and the range of differences from other Hymenolepis spp. varied from 24 to 34 bp (1.74–2.47%). Although only a few mitochondrial 16S gene sequences of hymenolepidid cestodes were available in GenBank, phylogenetic analyses demonstrated the same relationships of H. erinacei in the genus Hymenolepis (fig. 3).
Phylogenetic tree based on analysis of partial sequences of the 28S rRNA gene. Bootstrap support given for maximum likelihood analysis. Bootstrap support values lower than 70% are not shown. GenBank numbers: KX928758, KX928757 Hymenolepis erinacei; HM138521 Hymenolepis weldensis; HM138523, HM138525 Hymenolepis spp.; AF286917, AY157181, HM138522, LC064143 Hymenolepis diminuta; KT148845, HM138527 Hymenolepis hibernia; GU166233 Rodentolepis asymmetrica; GU166254 Vigisolepis spinulosa; GU166248, GU166249 Neoskrjabinolepis schaldybini; GU166250 Lineolepis scutigera; KC789835 Staphylocystoides gulyaevi; KC789836 Staphylocystoides parvissima; GU166225, GU166226 Arostrilepis sp.; GU166259, GU166260 Soricinia infirma; GU166269, GU166271 Pseudobotrialepis globosoides; LC064145, LM405059 Rodentolepis nana; GU166268 Rodentolepis fraternal; GU166244 Rodentolepis sp.; AF286918, GU166267, GU166278, LC064144 Rodentolepis microstoma; GU969051 Vampirolepis sp.; GU166277 Hymenolepididae sp.; GU166236, GU166265 Rodentolepis straminea; JQ260805 Staphylocystis brusatae; GU166274, GU969049 Staphylocystis furcata; KF257896 Staphylocystis schilleri; AF286919 Wardoides nyrocae and AF286914 Raillietina australis.
Phylogenetic tree based on analysis of partial sequences of the mitochondrial 16S rRNA gene. Bootstrap support given for maximum likelihood analysis. Bootstrap support values lower than 70% are not shown. GenBank numbers: KX928755, KX928756 Hymenolepis erinacei; AP017664 Hymenolepis diminuta; AP017665 R. microstoma; KT951722 R. nana; KF257885-KF257887 Staphylocystis sp.; KF257888 S. schilleri; KF257889 S. furcata and EU665473 Raillietina australis.
Discussion
Morphological features observed in specimens of H. erinacei are broadly consistent with characters described in other species of Hymenolepis (Makarikov & Tkach, Reference Makarikov and Tkach2013; Makarikov et al., Reference Makarikov, Tkach and Bush2013, Reference Makarikov, Nims, Galbreath and Hoberg2015b, Reference Makarikov, Tkach, Villa and Bushc). The eggs have only been described in a few species of the genus Hymenolepis: H. diminuta, H. tualatinensis, H. robertrauschi, Hymenolepis apodemi Makarikov & Tkach, 2013, H. rymzhanovi, H. haukisalmii, H. bicaudata, Hymenolepis bilaterala Makarikov, Tkach, Villa & Bush, 2013, H. alterna and H. folkertsi. The embryophores are subspherical in all of them, thus differing from H. erinacei. Other morphological features of the eggs common to this genus are: embryophores without filaments, antero-lateral embryonic hooks of different shape and length (compared to postero-lateral), i.e. antero-lateral embryonic hooks are more robust than lateral and have a ‘v’-form guard surrounding the base of the blade. It seems that these morphological features of the eggs are characteristic for the genus Hymenolepis. Egg morphology is an important morphological feature, which can be used in the identification of species that are morphologically similar as adults (Velikanov, Reference Velikanov1997). Additionally, egg morphology, especially shape, and the shape of the embryonic hooks could serve as reliable features for non-invasive detection and monitoring of cestode species of different genera. However, for this task, it is necessary to have descriptions of the eggs of all species, or as many as possible.
Considering strobila of H. erinacei, we offer several additional new observations. An atypical number or position of testes is not very common in cestodes of small mammals – apparently there are only a few descriptions of atypical variability in testes number and distribution. Such abnormalities have been noted in H. diminuta, H. hibernia, Hymenolepis vogeae Singh, 1956, T. mogerae and T. peipingensis (Montgomery et al., Reference Montgomery, Montgomery and Dunn1987; Sawada & Koyasu, Reference Sawada and Koyasu1991; Mas-Coma & Tenora, Reference Mas-Coma and Tenora1997; Gulyaev & Melnikova, Reference Gulyaev, Melnikova and Alimov2005). The shape of the fully developed uterus was one of the primary features leading to the placement of H. erinacei in the genus Erinaceolepis (Irzhavsky & Ketenchiev, Reference Irzhavsky and Ketenchiev2011), but later, taking into account other morphological features, it was again relegated to Hymenolepis (Makarikov & Tkach, Reference Makarikov and Tkach2013). The morphology of the scolex and proglottids, however, and the presence of transverse anastomoses between the ventral osmoregulatory canals, and the common attributes of the eggs described herein, confirm the allocation of this species to the genus Hymenolepis.
Our phylogenetic analyses, based on the 16S and 28S gene datasets, unequivocally establish the taxonomic position of H. erinacei and confirm the inclusion of the species in the genus Hymenolepis (figs 2, 3). The genus Hymenolepis forms a monophyletic group of cestodes occurring in one species of hedgehog and several species of rodents. The phylogenetic analyses highlight that the genus Hymenolepis is a strongly supported group among cestodes of mammals in the family Hymenolepididae.
The species of the family Hymenolepididae are characterized by a high degree of host specificity (stenoxenous). The host specificity of most hymenolepidid genera of mammals is at the level of host genera, less often to subfamily or family (Vaucher, Reference Vaucher1982; Vasileva et al., Reference Vasileva, Vaucher, Tkach and Genov2004). Despite this apparent specificity, events of host colonization are evident in the history of diversification of this group (Binkienė et al., Reference Binkienė, Kontrimavichus and Hoberg2011). The genus Hymenolepis is unique among Hymenolepididae as its representatives parasitize hosts of the different orders, Rodentia and Eulipotyphla. Additionally, some species of Hymenolepis have been described from Chiroptera, but this ‘requires significant revision to verify the superficial description of these species’ (Makarikov & Tkach, Reference Makarikov and Tkach2013); there are no molecular data to support the allocation of these species in the genus.
Phylogenetic analyses by Haukisalmi et al. (Reference Haukisalmi, Hardman, Foronda, Feliu, Laakkonen, Niemimaa and Henttonen2010), Greiman & Tkach (Reference Greiman and Tkach2012) and Makarikov et al. (Reference Makarikov, Mel'nikova and Tkach2015a) have revealed that three hymenolepidid genera, Rodentolepis, Staphylocystis and Vampirolepis, form the Rodentolepis clade, which displays frequent events of host switching among various rodents, shrews and bats. Based on phylogenetic analyses, Haukisalmi et al. (Reference Haukisalmi, Hardman, Foronda, Feliu, Laakkonen, Niemimaa and Henttonen2010) suggested the colonization of rodents by the ancestor of Arostrilepis spp. from shrews. Nowadays, species of the genus Arostrilepis are not found in shrews or other Eulipotyphla and appear largely restricted in distribution to arvicoline rodents as hosts. In contrast to the origins of Arostrilepis, the history of host association and the possible direction of colonization events related to H. erinacei suggest rodents as ancestral hosts. Our phylogenetic analysis indicates that, in the genus Hymenolepis, host colonization from rodents to hedgehogs appears consistent with the relationships demonstrated for H. erinacei arising in hedgehogs. Spassky (Reference Spassky1954), in establishing the genus Rodentolepis where H. erinacei was relegated to the genus Rodentolepis, wrote about this possible pathway of colonization of hedgehogs by H. erinacei. Such a colonization event is postulated to have occurred deep in the past due to historical interaction between ecological fitting, oscillation and taxon pulses (Hoberg & Brooks, Reference Hoberg and Brooks2008, Reference Hoberg, Brooks and Rohde2013).
A mechanism for host switching remains unclear, although always represents the interaction of ecological opportunity and capacity of particular parasites to utilize common resources found in different spectra of hosts (essentially ecological fitting as discussed by Agosta et al. (Reference Agosta, Janz and Brooks2010) and Araujo et al. (Reference Araujo, Braga, Brooks, Agosta, Hoberg, von Hartenthal and Boeger2015)). One example among the hymenolepidids does provide a possible mechanism for host colonization – water shrews of the genus Neomys have a distinct tapeworm species compared to those occurring in other shrews (Binkienė et al., Reference Binkienė, Kontrimavichus and Hoberg2011). In northern Europe, only atypical cestodes appear to parasitize Neomys fodiens (Pennant, 1771): Vigisolepis spinulosa (Cholodkowsky, 1906) from Finland (Haukisalmi, Reference Haukisalmi2015) and Neoskrjabinolepis schaldybini Spassky, 1947, from Karelia Republic (Russia) (Anikanova et al., Reference Anikanova, Bugmyrin, Yeshko, Alimov, Galkin and Dubinina2002). The specific identity of V. spinulosa from the water shrew has been confirmed by DNA sequences (Haukisalmi et al., Reference Haukisalmi, Hardman, Foronda, Feliu, Laakkonen, Niemimaa and Henttonen2010). In southern and central Europe, these two cestodes parasitize only Sorex shrews, not N. fodiens. Haukisalmi (Reference Haukisalmi2015) concluded that the absence of typical parasites of N. fodiens in northern Europe could be due to the ‘restricted/patchy distribution of amphipods as the intermediate hosts and their low numbers in the diet of water shrews’. This may be the primary circumstance for host switching from Sorex to Neomys shrews and the formation of new species in the future.
Besides H. erinacei, three other species of cestodes from the genus Mathevotaenia (Anoplocephalidae: Linstowiinae) were also detected in hedgehogs that were originally described as a species of the genus Erinaceus (in Beveridge, Reference Beveridge2008). Mathevotaenia parva (Janicki, 1904) (syn. Davainia parva Janicki, 1904) was described in Erinaceus sp. from Cyprus (Janicki, Reference Janicki1904), but only Hemiechinus auritus (Gmelin, 1770) occurs on this island, which was originally described as Erinaceus auritus Gmelin, 1770. The same situation occurs with the species Mathevotaenia skrjabini Spassky 1949. Originally it was described and illustrated from the gut of Erinaceus (Hemiechinus) auritus from middle Asia (Spassky, Reference Spassky1949). Mathevotaenia erinacei Meggitt, 1920 was found in northern Africa in hedgehogs of the family Atelerix and Erinaceus sp. (Beveridge, Reference Beveridge2008) – doubtless the latter is Hemiechinus sp. as the habitat appropriate for Erinaceus is absent in Africa. In other localities, M. erinacei has only been found in hedgehogs of the genera Hemiechinus, Paraechinus and Atelerix (Al-Zihiry, Reference Al-Zihiry2009; Khaldi et al., Reference Khaldi, Torres, Samsó, Miquel, Biche, Benyettou, Barech, Benelkadi and Ribas2012; Amin & Heckmann, Reference Amin and Heckmann2016; Zolfaghari & Nabavi, Reference Zolfaghari and Nabavi2016). Consequently, H. erinacei is the only known species of cestode parasitizing hedgehogs of the genus Erinaceus, while cestodes from the genus Mathevotaenia can be detected in Hemiechinus, Paraechinus and Atelerix hedgehogs only.
The genus Erinaceus contains four species of hedgehogs (E. europaeus Linnaeus, 1758; E. concolor Martin, 1837; E. roumanicus Barrett-Hamilton, 1900 and E. amurensis Schrenk, 1859), but in the Palaearctic ecozone only one cestode species, H. erinacei, is found parasitizing Erinaceus hedgehogs (Baer, Reference Baer1932; Spassky, Reference Spassky1954; Prokopič, Reference Prokopič1959; Furmaga, Reference Furmaga1961; Arzamasov et al., Reference Arzamasov, Merkusheva, Myhalop and Chikilevskaja1969; Genov, Reference Genov1984; Bunnell, Reference Bunnell2001; Cirak et al., Reference Cirak, Senlik, Aydogdu, Selver and Akyol2010; Irzhavsky & Ketenchiev, Reference Irzhavsky and Ketenchiev2011; Pfäffle et al., Reference Pfäffle, Bolfikova, Hulva and Petney2014). Hymenolepis erinacei has not been reported in E. amurensis, which inhabits south-eastern Eurasia (lowlands of China, north to the Amur Basin and Korea) (Cassola, Reference Cassola2016), as there are no data on the helminth fauna of this mammal. Therefore it remains possible that this hedgehog can possess the same, or other, species of cestodes.
Knowledge about the helminths of hedgehogs in different regions and effective methods for the monitoring of parasites are necessary because hedgehogs have become exotic pets, leading to an increase in their importance in small animal veterinary practice (Brooks et al., Reference Brooks, Hoberg, Boeger, Gardner, Galbreath, Herczeg, Mejía-Madrid, Rácz and Tsogtsaikhan Dursahinhan2014). This requires adequate observation of parasitic infections of hedgehogs and also identifies a possible pathway for parasites to be introduced to new geographic localities.
Acknowledgements
The authors would like to thank Rimvydas Milius, Danutė Tocionienė, Kasparas Bublys and Saulius Skuja for their assistance in the collection of hedgehogs killed by motor vehicles on roads. We are also grateful to Dr Eric Hoberg, Dr Tim Littlewood and an anonymous reviewer for making very useful suggestions and improving the English.
Financial support
This work was supported by the Research Council of Lithuania (grant no. MIP-43/2015).
Conflict of interest
None.
