Journal of Helminthology
cambridge.org/jhl
Research Paper
Cite this article: Binkienė R, Miliūtė A,
Stunžėnas V. Molecular data confirm the
taxonomic position of Hymenolepis erinacei
(Cyclophyllidea: Hymenolepididae) and host
switching, with notes on cestodes of
Palaearctic hedgehogs (Erinaceidae). Journal
of Helminthology https://doi.org/10.1017/
S0022149X18000056
Received: 19 October 2017
Accepted: 2 January 2018
Author for correspondence:
R. Binkienė, Fax: +370 5 2729352, E-mail:
zrasa@ekoi.lt
© Cambridge University Press 2018
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Molecular data confirm the taxonomic position
of Hymenolepis erinacei (Cyclophyllidea:
Hymenolepididae) and host switching, with
notes on cestodes of Palaearctic hedgehogs
(Erinaceidae)
R. Binkienė1, A. Miliūtė2 and V. Stunžėnas1
1
Nature Research Centre, Akademijos 2, LT-08412 Vilnius, Lithuania and 2Vilnius University, Saulėtekio al. 7,
LT-10257 Vilnius, Lithuania
Abstract
The cestode Hymenolepis erinacei is regarded as a widely distributed parasite in European
hedgehogs of the genus Erinaceus, although the taxonomic position of this hymenolepidid
has been debated for a considerable period of time. We present the first molecular data for
this cestode, including partial DNA sequences of mitochondrial 16S and nuclear 28S riboso-
mal genes. Molecular phylogenetic analysis clusters H. erinacei in one clade together with
representatives of the genus Hymenolepis from rodents. Characteristic morphological features,
including the oval embryophore without filaments and shape of the embryonic hooks of H.
erinacei are described. Features of these cestode eggs are proposed as a basis for non-invasive
detection of parasitic infections in small mammal populations. The present study explores
phylogenetic relationships within the genus Hymenolepis and the host switching related to
H. erinacei. Cases of host switching in other genera of the family Hymenolepididae are
reviewed. A short critical review of cestodes parasitizing hedgehogs in the Palaearctic is
presented.
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, 1791). Further studies revealed that the morphology of T. erinacei corresponded to
cestodes attributed to Hymenolepis and a transfer to this genus was proposed (Janicki, 1906;
Baer, 1932). However, despite the description of Hymenolepis erinacei corresponding to the
genus Hymenolepis, Lopez-Neyra (1942) transferred H. erinacei to the genus Dicranotaenia
Railliet, 1892. Later, however, the concept for Hymenolepis became further refined (Skrjabin
& Matevosyan, 1948) 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 (1954)
relegated H. erinacei to the genus Rodentolepis Spassky, 1954. Genov (1984) noticed that ces-
todes from hedgehogs possessed an unarmed rostellum in both adults and cysticercoids, and
referred R. erinacei again to Hymenolepis. Irzhavsky & Ketenchiev (2011) 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 (1994) 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, 2013).
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 exam-
ine 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.
 2 R. Binkienė et al.

Table 1. Erinaceus roumanicus: dates of collections, places and coordinates The amplification protocol with new primers was the following:
(WGS). 3 min denaturation at 96°C; 38 cycles of 40 s at 94°C, 40 s at
No. Date Place Coordinates 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
1 08.03.2013 Šalčininkai dist. 54.310813, 24.966447 sequenced in both directions at BaseClear B.V. (Leiden, The
2 03.07.2014 Vilnius 54.724381, 25.269527
Netherlands) using PCR primers. Contiguous sequences were
assembled using Sequencher 4.7 software (Gene Codes
3 23.04.2015 Alytus 54.400621, 24.049204 Corporation, Ann Arbor, Michigan, USA).
4 25.04.2015 Alytus 54.379081, 24.064271 Additional 28S rDNA sequences representing genera and
5 25.04.2015 Vilnius dist. 54.774325, 25.193879
species among the Hymenolepididae were downloaded from
GenBank and included in pairwise sequence comparisons and
6 28.04.2015 Vilnius 54.72431, 25.269566 phylogenetic analyses: HM138521 Hymenolepis weldensis Grei-
7 10.07.2015 Alytus 54.39124, 24.056278 man & Schmidt, 1988; HM138523 and HM138525 Hymenolepis
8 10.07.2015 Vilnius 54.69918, 25.241608
spp.; AF286917, AY157181, HM138522 and LC064143 Hymeno-
lepis diminuta (Rudolphi, 1819); KT148845 and HM138527
9 01.08.2015 Varėna dist. 54.243217, 24.555375 Hymenolepis hibernia Montgomery, Montgomery & Dunn,
10 13.09.2015 Vilnius dist. 54.575642, 25.053232 1987; GU166233 Rodentolepis asymmetrica (Janicki, 1904);
11 09.04.2016 Vilnius 54.702848, 25.265055
GU166254 Vigisolepis spinulosa (Cholodkowsky, 1906);
GU166248 and GU166249 Neoskrjabinolepis schaldybini Spassky,
12 09.04.2016 Alytus dist. 54.546599, 24.160185 1947; GU166250 Lineolepis scutigera (Dujardin, 1845); KC789835
13 09.04.2016 Vilnius dist. 54.581456, 25.061031 Staphylocystoides gulyaevi Greiman, Tkach & Cook, 2013;
KC789836 Staphylocystoides parvissima (Voge, 1953);
14 09.04.2016 Daugai 54.367135, 24.341742
GU166225 and GU166226 Arostrilepis sp.; GU166259 and
15 17.04.2016 Alytus dist. 54.532953, 24.151305 GU166260 Soricinia infirma (Zarnowski, 1955); GU166269 and
16 18.04.2016 Trakai dist. 54.595316, 25.074764 GU166271 Pseudobotrialepis globosoides (Soltys, 1954);
LC064145 and LM405059 Rodentolepis nana (von Siebold,
17 23.04.2016 Varėna dist. 54.350869, 24.558878
1852); GU166268 Rodentolepis fraterna (Stiles, 1906);
18 25.04.2016 Vilnius 54.577673, 25.055694 GU166244 Rodentolepis sp.; AF286918, GU166267, GU166278
19 25.04.2016 Vilnius dist. 54.577673, 25.055694 and LC064144 Rodentolepis microstoma (Dujardin, 1854);
GU969051 Vampirolepis sp.; GU166277 Hymenolepididae sp.;
20 25.04.2016 Prienai dist. 54.57527, 24.169177
GU166236 and GU166265 Rodentolepis straminea (Goeze,
21 30.04.2016 Alytus 54.399738, 24.054602 1782); JQ260805 Staphylocystis brusatae (Vaucher, 1971);
22 02.05.2016 Varėna dist. 54.260164, 24.54009 GU166274 and GU969049 Staphylocystis furcata (Stieda, 1862);
KF257896 Staphylocystis schilleri (Rausch & Kuns, 1950);
23 03.05.2016 Alytus dist. 54.50026, 24.134315
AF286919 Wardoides nyrocae (Yamaguti, 1935); and as outgroup
24 03.05.2016 Alytus dist. 54.536972, 24.153847 taxa – AF286914 Raillietina australis (Krabbe, 1869). In the
25 03.05.2016 Alytus dist. 54.530748, 24.150541 GenBank database, the H. diminuta sequence (accession no.
AP017664) was a single 16S rDNA gene sequence representing
26 06.05.2016 Vilnius 54.738491, 25.344302
the genus. Also, available 16S rDNA sequences of
dist., district. Hymenolepididae species were downloaded from GenBank and
included in the phylogenetic analyses: AP017664 H. diminuta,
AP017665 R. microstoma, KT951722 R. nana, KF257885–
Permanent mounted slides of specimens used for morphological KF257887 Staphylocystis sp., KF257888 S. schilleri, KF257889 S.
studies were deposited in the Institute of Ecology, Nature furcata and EU665473 Raillietina australis as outgroup taxa. For
Research Centre, Vilnius, Lithuania (accession numbers EKOI the phylogenetic analyses, the sequences were aligned using
HELMI 946–949). Measurements are given in micrometres; they ClustalW (Thompson et al., 1994) with an open gap penalty of
are presented as the range followed by the mean and the number 15 and gap extension penalty of 6.66. The best-fit model of
of the measurements (n) in parentheses. sequence evolution for phylogenetic analysis was estimated
Total genomic DNA for molecular analysis was isolated from using jModeltest v. 0.1.1 software (Posada, 2008). Ambiguously
cestodes according to the protocol proposed by Stunžėnas et al. aligned positions were excluded from phylogenetic analysis.
(2011), with a slight modification described by Petkevičiūtė Maximum likelihood (ML) phylogenetic trees were obtained
et al. (2014). A fragment at the 5′ end of the 28S rRNA gene and analysed using MEGA v6 (Tamura et al., 2013). Branch sup-
was amplified using the forward primer ZX-1 (5′ -ACCC port was estimated by bootstrap analyses with 1000 replicates. The
GCTGAATTTAAGCATAT-3′ ; Scholz et al., 2013) and reverse ML trees were obtained using the general time reversible model
primer 1500R (5′ -GCTATCCTGAGGGAAACTTCG-3′ ; Olson with a gamma distribution of rates and a proportion of invariant
et al., 2003; Tkach et al., 2003). The amplification protocol was sites (GTR + G + I) for both the internal transcribed spacer-2
the following: 3 min denaturation at 96°C; 40 cycles of 30 s at (ITS2) and the 28S gene datasets. Gamma shape and number of
95°C, 38 s at 53°C, 1 min 48 s at 70°C; and 8 min final extension invariant sites were estimated from the data. Parsimony analysis
at 70°C. New primers were constructed to amplify a partial based on subtree pruning and regrafting (SPR) was used with
sequence (650–750 bp) of mitochondrial 16S rRNA gene: forward default parsimony settings. Estimates of mean evolutionary
primer Cyclo16SF (5′ -AATAGATAAGAACCGAACTGG–3′ ) and divergence over sequence pairs within and between groups were
reverse primer Cyclo16SR (5′ -TGCCTTTTGCATCAT GCT-3′ ). calculated using the program MEGA v6.

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 Journal of Helminthology
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 (2011) 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 pos-
ition and shape of the genital organs were similar to prior mor-
phological 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.
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 spe-
cies are larger (17–20 in H. tualatinensis, 31–37 in H. pseudodimi-
nuta, 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 sub-
spherical 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., 2013, 2015c),
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3
Table 2. The morphological measurements of Hymenolepis erinacei in the
present study and in the description of Irzhavsky & Ketenchiev (2011).
Measurements are given in micrometres except where otherwise stated.
Irzhavsky &
Present study Ketenchiev (2011)
Body length, cm 5.3–9.2 8–11
Mature proglottids 962–1852 × 203–360 1370–2300 × 500–650
Scolex 284–338 × 354–397 390–480 × 420–500
Suckers 190–243 × 139–184 260–340 × 200–250
Neck, width 232–278 280–330
Rostellum 168–216 × 110–122 290–300 × 158–160
Cirrus-sac, length 235–294 345–380
Cirrus, length 41–50 60–65
Testes 162–200 × 106–135 180–200 × 140–170
Ovary, width 157–286 317–330
Vitellarium 54–126 × 34–79 84–100 × 80–84
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,
1997). 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., 2013). 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 (subsphe-
rical in S. clydesengeri and oval in H. erinacei) and size of embry-
onic hooks (14.5–16 in S. clydesengeri and 10–13 in H. erinacei).
Gulyaev & Melnikova (2005) 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, 1990; Sawada
et al., 1992; Gulyaev & Melnikova, 2005; Makarikova &
Makarikov, 2012); in contrast, the outer coat in H. erinacei is
thin and the length of hooks varied from 10 to 13. The outer
 4 R. Binkienė et al.
Fig. 1. Hymenolepis erinacei eggs: (a) embryophores
with embryonic hooks; (b) egg; (c) embryonic hooks.
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, 1991).
The egg shape and hook lengths of H. erinacei are similar to
those of Relictolepis feodorovi, another species of hymenolepidid
(Gulyaev & Makarikov, 2007), 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
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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 dif-
fered 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 hyme-
nolepidid cestodes were available in GenBank, phylogenetic ana-
lyses demonstrated the same relationships of H. erinacei in the
genus Hymenolepis (fig. 3).
Discussion
Morphological features observed in specimens of H. erinacei are
broadly consistent with characters described in other species of
Hymenolepis (Makarikov & Tkach, 2013; Makarikov et al., 2013,
2015b, c). The eggs have only been described in a few species of
the genus Hymenolepis: H. diminuta, H. tualatinensis, H. rober-
trauschi, Hymenolepis apodemi Makarikov & Tkach, 2013, H.
rymzhanovi, H. haukisalmii, H. bicaudata, Hymenolepis bilaterala
 Journal of Helminthology
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 com-
mon 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 morph-
ology is an important morphological feature, which can be used
in the identification of species that are morphologically similar
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5
Fig. 2. 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. Gen-
Bank numbers: KX928758, KX928757 Hymenolepis eri-
nacei; HM138521 Hymenolepis weldensis; HM138523,
HM138525 Hymenolepis spp.; AF286917, AY157181,
HM138522, LC064143 Hymenolepis diminuta;
KT148845, HM138527 Hymenolepis hibernia;
GU166233 Rodentolepis asymmetrica; GU166254 Vigi-
solepis spinulosa; GU166248, GU166249 Neoskrjabino-
lepis schaldybini; GU166250 Lineolepis scutigera;
KC789835 Staphylocystoides gulyaevi; KC789836 Sta-
phylocystoides parvissima; GU166225, GU166226 Aros-
trilepis sp.; GU166259, GU166260 Soricinia infirma;
GU166269, GU166271 Pseudobotrialepis globosoides;
LC064145, LM405059 Rodentolepis nana; GU166268
Rodentolepis fraternal; GU166244 Rodentolepis sp.;
AF286918, GU166267, GU166278, LC064144 Rodento-
lepis microstoma; GU969051 Vampirolepis sp.;
GU166277 Hymenolepididae sp.; GU166236,
GU166265 Rodentolepis straminea; JQ260805 Staphy-
locystis brusatae; GU166274, GU969049 Staphylocystis
furcata; KF257896 Staphylocystis schilleri; AF286919
Wardoides nyrocae and AF286914 Raillietina australis.
as adults (Velikanov, 1997). Additionally, egg morphology, espe-
cially shape, and the shape of the embryonic hooks could serve as
reliable features for non-invasive detection and monitoring of ces-
tode species of different genera. However, for this task, it is neces-
sary 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.
 6 R. Binkienė et al.
Fig. 3. Phylogenetic tree based on analysis of partial
sequences of the mitochondrial 16S rRNA gene.
Bootstrap support given for maximum likelihood ana-
lysis. Bootstrap support values lower than 70% are not
shown. GenBank numbers: KX928755, KX928756
Hymenolepis erinacei; AP017664 Hymenolepis dimin-
uta; AP017665 R. microstoma; KT951722 R. nana;
KF257885-KF257887 Staphylocystis sp.; KF257888 S.
schilleri; KF257889 S. furcata and EU665473 Raillietina
australis.
diminuta, H. hibernia, Hymenolepis vogeae Singh, 1956, T.
mogerae and T. peipingensis (Montgomery et al., 1987; Sawada
& Koyasu, 1991; Mas-Coma & Tenora, 1997; Gulyaev &
Melnikova, 2005). The shape of the fully developed uterus was
one of the primary features leading to the placement of H. erina-
cei in the genus Erinaceolepis (Irzhavsky & Ketenchiev, 2011), but
later, taking into account other morphological features, it was
again relegated to Hymenolepis (Makarikov & Tkach, 2013).
The morphology of the scolex and proglottids, however, and the
presence of transverse anastomoses between the ventral osmo-
regulatory 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. eri-
nacei and confirm the inclusion of the species in the genus
Hymenolepis (figs 2, 3). The genus Hymenolepis forms a mono-
phyletic group of cestodes occurring in one species of hedgehog
and several species of rodents. The phylogenetic analyses high-
light 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 spe-
cificity of most hymenolepidid genera of mammals is at the
level of host genera, less often to subfamily or family (Vaucher,
1982; Vasileva et al., 2004). Despite this apparent specificity,
events of host colonization are evident in the history of diversifi-
cation of this group (Binkienė et al., 2011). The genus
Hymenolepis is unique among Hymenolepididae as its representa-
tives parasitize hosts of the different orders, Rodentia and
Eulipotyphla. Additionally, some species of Hymenolepis have
been described from Chiroptera, but this ‘requires significant revi-
sion to verify the superficial description of these species’
(Makarikov & Tkach, 2013); there are no molecular data to sup-
port the allocation of these species in the genus.
Phylogenetic analyses by Haukisalmi et al. (2010), Greiman &
Tkach (2012) and Makarikov et al. (2015a) 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. (2010)
suggested the colonization of rodents by the ancestor of
Arostrilepis spp. from shrews. Nowadays, species of the genus
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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 (1954), 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 postu-
lated to have occurred deep in the past due to historical inter-
action between ecological fitting, oscillation and taxon pulses
(Hoberg & Brooks, 2008, 2013).
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. (2010) and Araujo et al. (2015)).
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., 2011). In northern
Europe, only atypical cestodes appear to parasitize Neomys fodiens
(Pennant, 1771): Vigisolepis spinulosa (Cholodkowsky, 1906)
from Finland (Haukisalmi, 2015) and Neoskrjabinolepis schaldy-
bini Spassky, 1947, from Karelia Republic (Russia) (Anikanova
et al., 2002). The specific identity of V. spinulosa from the water
shrew has been confirmed by DNA sequences (Haukisalmi
et al., 2010). In southern and central Europe, these two cestodes
parasitize only Sorex shrews, not N. fodiens. Haukisalmi (2015)
concluded that the absence of typical parasites of N. fodiens in
northern Europe could be due to the ‘restricted/patchy distribu-
tion of amphipods as the intermediate hosts and their low num-
bers 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 spe-
cies of the genus Erinaceus (in Beveridge, 2008). Mathevotaenia
parva (Janicki, 1904) (syn. Davainia parva Janicki, 1904) was
 Journal of Helminthology
described in Erinaceus sp. from Cyprus (Janicki, 1904), 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, 1949). Mathevotaenia erinacei Meggitt, 1920 was
found in northern Africa in hedgehogs of the family Atelerix
and Erinaceus sp. (Beveridge, 2008) – 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, 2009; Khaldi et al., 2012; Amin & Heckmann, 2016;
Zolfaghari & Nabavi, 2016). 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. rouma-
nicus Barrett-Hamilton, 1900 and E. amurensis Schrenk, 1859),
but in the Palaearctic ecozone only one cestode species, H. erina-
cei, is found parasitizing Erinaceus hedgehogs (Baer, 1932;
Spassky, 1954; Prokopič, 1959; Furmaga, 1961; Arzamasov et al.,
1969; Genov, 1984; Bunnell, 2001; Cirak et al., 2010; Irzhavsky
& Ketenchiev, 2011; Pfäffle et al., 2014). 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, 2016), 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., 2014). 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.
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