Introduction

Cestodes of the genus Soricinia Spassky & Spasskaja, 1954 are among the smallest hymenolepidids with unarmed scoleces, parasitic in shrews. The original diagnosis of Soricinia describes serial development of the strobila and formation of a syncapsule uniting several gravid proglottides. As a result, Spassky (1954) placed the genus within the tribe Ditestolepidini. Spassky (1954) chose Soricinia soricis (Baer, 1925) Spassky, 1954 (syn. Hymenolepis minuta Baer, 1925) as the type-species of Soricinia. The original description of the type-species based on a single specimen collected from an Alpine shrew Sorex alpinus Schinz in Salève Mountain (France) was brief and superficial (Baer, 1925). Gulyaev (1991) stated that the original description of Hymenolepis soricis Baer, 1925 lacks clear morphological differentiating characters and proposed to consider it a species inquirenda thus questioning the validity of the genus Soricinia. Vaucher (in Czaplinski & Vaucher, 1994) retained Soricinia as a separate genus. Moreover, he considered Insectivorolepis Zarnowski, 1955 a synonym of Soricinia. Žarnowski (1955) chose Hymenolepis globosa Baer, 1931 from the Eurasian water shrew (Neomys fodiens Pennant) in Switzerland (Baer, 1931) as the type-species of the genus Insectivorolepis and provided a detailed generic diagnosis of Insectivorolepis that differed substantially from the generic diagnosis of Soricinia (see Vaucher in Czaplinski & Vaucher, 1994). As a result, Irzhavsky et al. (2005) considered Insectivorolepis as a valid genus while suggesting that Soricinia should be a genus inquirenda.

Upon re-examination of the type-specimens of H. soricis and H. globosa, Zubova et al. (2010) concurred with the opinion of Vaucher (in Czaplinski & Vaucher 1994) who considered Insectivorolepis a junior synonym of Soricinia. However, the paper by Zubova et al. (2010) did not contain a redescription of the type-species and detailed diagnosis of the genus. Recently, Binkienė et al. (2015) provided a detailed redescription of Soricinia globosa, but did not amend the generic diagnosis.

Comparative sequence analysis of the nuclear ribosomal 28S and mitochondrial nad1 genes of Soricinia infirma (Zarnowski, 1955), Soricinia quarta (Karpenko, 1983), Soricinia genovi Binkienė, Kornienko & Tkach, 2015 and Soricinia bargusinica (Eltyschev, 1975) revealed that despite the high morphological similarity among species of Soricinia, their sequences exhibit great interspecific divergence levels in both genes, from 0.9 to 4.2% in the 28S gene and from 9.6 to 17.2% in the nad1 gene (Binkienė et al., 2015). In both phylogenetic trees resulting from analyses of the two genes, sequences of specimens identified as S. infirma formed an independent clade that appeared as a sister group to the clade comprising the remaining Soricinia spp. Overall, the members of the “S. infirma” clade differed most significantly from the remaining species. Pairwise comparisons of partial 28S and nad1 sequences have indicated that the two forms of S. infirma (from Altai and the Carpathians) sequenced by Binkienė et al. (2015) and S. infirma sequenced by Haukisalmi et al. (2010) most likely represent three different species. Additional studies including all current members of Soricinia are necessary in order to verify their congeneric status (Binkienė et al., 2015).

The aim of this study is to revise the content of the genus Soricinia using results of morphological and genetic analyses and provide an amended diagnosis of the genus. We provide redescriptions of the type-species S. soricis and two other insufficiently described species, S. infirma and S. quarta.

Materials and methods

The holotype of S. soricis deposited at the Museum of Natural History of Geneva (MHNG; accession numbers C7/11, MHNG-PLAT-15531) and the holotype of S. quarta deposited at the Museum of Zoology of the Institute of Systematics and Ecology of Animals, Novosibirsk, Russian Federation (ISEA) (accession number 3589) were used for re-descriptions of these species.

Live cestodes were rinsed in saline, killed with hot water and fixed in 70% ethanol. For morphological study, four complete specimens were stained with Ehrlich’s haematoxylin, dehydrated in a graded ethanol series, cleared in clove oil and mounted in Canada balsam; two specimens were mounted in Berlese’s medium to facilitate examination of the copulatory apparatus. The specimens were deposited in the Natural History Museum, Geneva, Switzerland (MHNG) and the Museum of Zoology of the Institute of Systematic and Ecology of Animals, Novosibirsk, Russian Federation (ISEA).

Measurements are given in micrometres unless otherwise stated and are presented as the range followed by the mean and the number of measurements taken (n) in parentheses. The terminology used in the description of different stages of proglottis development follows Mas-Coma & Puchades (1991).

Soricinia soricis (Baer, 1925) Spassky & Spasskaja, 1954

Syn. Hymenolepis minuta Baer, 1925

Type-host: Sorex alpinus Schinz (Soricomorpha: Soricidae).

Type-locality: Region of Salève, France (see Baer, 1925).

Site in host: Intestine.

Type-material: Deposited in MHNG. Holotype: slide C7/11, Sorex alpinus, MHNG-PLAT-15531, coll. Dr. E. Andre.

Redescription (Fig. 1)

[Based on the holotype.] Small cestode with total length 360 (Fig. 1A). Strobilation gradual. Strobila consisting of 9 proglottides: 2 juvenile, 3 hermaphroditic (1 mature), 3 pregravid and 1 gravid, latter containing fully-formed eggs. Mature proglottis acraspedote, transversely elongate, 20 × 90 (Fig. 1B). Single gravid proglottis 48 × 70. Male and female gonads appearing simultaneously, subsequent maturation following functional protandry pattern. Osmoregulatory canals without transverse anastomoses. Genital pore unilateral, dextral. Genital atrium cylindrical, immediately pre-equatorial.

Fig. 1
figure 1

Soricinia soricis (Baer, 1925) ex Sorex alpinus Schinz. Holotype. A, Total view; B, Mature proglottides; C, Evaginated cirrus. Scale-bars: A, 100 µm; B, 50 µm; C, 30 µm

Full size image

Scolex relatively large, slightly compressed dorso-ventrally, 90 wide. Suckers 75–76 × 60–61 (n = 2), with well-developed muscular rim. Rhynchus and rostellar apparatus absent. Neck distinct, 68 wide.

Testes 3, oval, 15–18 × 18–22 (16 × 20; n = 3), arranged in triangle, 1 poral and 2 antiporal, in median field of proglottis (Fig. 1B). Diminishing testes visible in first pregravid proglottis. Cirrus-sac cigar-shaped, elongate, thin-walled, 30–33 × 10, crossing poral osmoregulatory canals, not reaching midline of proglottis (Fig. 1B). Internal seminal vesicle small, 15 × 9, ovoid; external seminal vesicle elongate, 19 × 10, median, ventral. Cirrus conical, 30–32 × 7, covered with heteromorphic spines: basal part unarmed, parabasal part covered with long, thin, needle-shaped spines decreasing in size towards end of cirrus (Fig. 1C).

Copulatory part of vagina pear-shaped, opening ventral to cirrus-sac. Ovary large, entire or slightly lobed, 48 × 22, ventral to testes, occupying large part of middle field. Vitellarium compact, oval, 18 × 15, aporal, ventral to testes, postovarian (Fig. 2B). Uterus sac-like, ventral to testes, occupying almost entire median field, containing 8–9 large eggs. Eggs oval, 38–44 × 16–18 (41 × 17; n = 3); oncospheres 13–15 (14; n = 3) in diameter; embryophore fusiform, with straight polar projections, 25–27 × 13–14 (26 × 14; n = 3); embryonic hooks small, 8–10 (9; n = 2).

Fig. 2
figure 2

Soricinia infirma (Zarnowski, 1955) ex Sorex araneus L. Neotype and voucher specimens from the same host individual. A, Total view (neotype); B, Scolex (voucher specimen); C, Mature proglottides (neotype); D, Invaginated cirrus (voucher specimen); E, Evaginated cirrus (voucher specimen). Scale-bars: A, B, 100 µm; C, 50 µm; D, E, 40 µm

Full size image

Remarks

The original description of S. soricis by Baer (1925) was incomplete and did not provide information on the number and/or size of the proglottides, eggs, ovary and vitellarium. Besides, it contained erroneous information on the cirrus-sac and cirrus length. The cirrus-sac length reported in the original description was 240–300 µm with the cirrus being only 8 µm long. Our re-examination showed that the cirrus-sac of the holotype is 30–33 µm long and the cirrus is 30–32 µm long. It is obvious that Baer (1925) measured only the evaginated part of the cirrus. The poor original description hindered the proper systematic placement of this cestode for a long time.

Karpenko (1999) identified as S. soricis a small cestode found in Sorex caecutiens Laxmann in the Russian Far East (Khabarovsk Kray), revised the genus Soricinia and amended its diagnosis. He placed Insectivorolepis infirma, Insectivorolepis globosa (syn. Hymenolepis globosa), Ditestolepis secunda Schaldybin, 1964 and Sinuterilepis spasskyi Sadowskaja, 1965 among the synonyms of S. soricis. However, the cestode from the Far East collected by Karpenko (1999) differs from the holotype of S. soricis in the length of the cirrus sac (40–45 vs 30–33 µm) and the cirrus armature. According to Karpenko the cirrus is evenly covered with small spines, whereas the spines of the type-specimen of S. soricis are heteromorphic. Additionally, the study by Binkienė et al. (2015) demonstrated substantial morphological differences between S. infirma and S. globosa. Therefore, the taxonomic status of the species from Khabarovsk Kray identified by Karpenko (1999) as S. soricis remains unclear.

Soricinia infirma (Zarnowski, 1955) Czaplinski & Vaucher, 1994

Type-host: Sorex araneus L. (Soricomorpha: Soricidae).

Type-locality: Near village Vishnyaki, Khorolsky District, Poltavska Oblast, Ukraine (54°07′59″N, 24°01′05″E).

Site in host: Intestine.

Type-material: Neotype, Sorex araneus, MNHG-PLAT-91139. Voucher specimens from the same individual of S. araneus are deposited in the ISEA (No. 18.6.2.2-18.6.2.5).

Description (Fig. 2)

[Based on five specimens; measurements of the holotype are followed by the range, mean and number of measurements in parentheses.] Small cestodes, 600 (300–600; 420; n = 5) long. Strobila consisting of 13 (10–13; 12; n = 5) proglottides: 2–3 juvenile, 2–3 hermaphroditic (1 mature), 3–4 postmature and 2–3 gravid. Strobilation gradual. Proglottides acraspedote, transversely elongate (Fig. 2C). Mature proglottis 29 × 120 (28–36 × 110–120; 31 × 117; n = 5), pregravid proglottides 55 × 160 (55–73 × 150–170; 66 × 162; n = 5). Primordia of male and female gonads appearing simultaneously, subsequent maturation following functional protandry pattern. Scolex relatively large, slightly compressed dorso-ventrally, 120 (110–120; 113; n = 5) wide. Neck 86 (79–91; 86; n = 5) wide, clearly differentiated from scolex. Suckers subspherical, cup-shaped, 74 × 70 (68–85 × 58–80; 76 × 70; n = 5), with well-developed muscular rim (Fig. 2B). Rhynchus and rostellar apparatus absent.

Osmoregulatory canals without transverse anastomoses. Ventral osmoregulatory canals 2 (2–3; 2.4; n = 5) in diameter, dorsal canals 1 (1–2; 1.3; n = 5) in diameter. Genital pores unilateral, dextral, opening in middle of proglottis margin. Genital atrium simple, cylindrical 12 (11–15; 14; n = 7) deep.

Testes 3, oval, 33–36 × 22–23 (28–36 × 19–29; 32 × 25; n = 10), 1 poral and 2 antiporal, arranged in almost right-angled triangle in median field of proglottis (Fig. 2C). Cirrus-sac cigar-shaped, elongate, thin-walled, 60–62 × 9–10 (57–65 × 8–10; 61 × 8; n = 6), crossing poral osmoregulatory canals, reaching midline of proglottis. Cirrus cylindrical, large, 30 (30–38; 33; n = 5), armed. Parabasal portion of cirrus covered with numerous, long, needle-shaped spines, 2–3 (2–3; 2.5; n = 10) long, decreasing in size towards end of cirrus (Fig. 2D, E). Internal seminal vesicle oval, 18 × 6 (14–21 × 6–10; 19 × 8; n = 6); external seminal vesicle elongated, 30 × 15 (30–36 × 14–19; 31 × 16; n = 6), positioned along anterior margin of proglottis.

Ovary compact, 63 × 35 (61–66 × 28–36; 64 × 32; n = 5), in middle of proglottis, anterior and ventral to testes. Vitellarium compact, oval, 30 × 16 (22–30 × 16–19; 26 × 18; n = 5), aporal, ventral to testes, posterior to ovary. Vagina thin-walled, opening ventral to cirrus-sac. Copulatory part of vagina 28 × 9 (27–33 × 7–9; 29 × 9; n = 5), pin-shaped, leading to small oval seminal receptacle, 17 × 8 (15–17× 7–8; 16 × 8; n = 5) in middle of proglottis. Uterus sac-like, occupying almost entire median field, not extending beyond osmoregulatory canals. Uterus in gravid proglottides containing 16–20 (18; n = 7) eggs (Fig 2A). Embryonic hooks small, 6–7 (6.4; n = 8).

Remarks

The holotype of S. infirma, described from S. araneus in the vicinities of Puławy, Lublin District, eastern Poland (Žarnowski, 1955), could not be located in any collection in Poland despite the effort undertaken by Pojmańska et al. (2012). It appears, therefore, that the holotype of this species as well as any other specimens that could be considered as belonging to the type-series, are not extant. The ongoing research on Soricinia spp. throughout the Holarctic and the use of molecular tools for differentiation among morphologically similar species of the genus (Binkienė et al., 2015; our unpublished data) require clarification of the identity of S. infirma to preserve the taxonomic stability of the species and avoid confusion in the future. We have found several specimens of S. infirma from the type-host S. araneus in Poltavska Oblast’, Ukraine, within a reasonable proximity to the type-locality. These specimens corresponded very closely to the original description of the species by Žarnowski (1955) and possessed the main features differentiating S. infirma from the morphologically closest species S. soricis (see below). Therefore, a complete specimen collected from S. araneus in the Ukraine, was designated as the neotype and deposited in the collection of the Natural History Museum, Geneva, Switzerland.

Soricinia infirma is morphologically most similar to S. soricis. The two species are similar in scolex morphology and the number of proglottides (10–13 vs 9). Nevertheless, S. infirma can be distinguished from S. soricis by having a longer cirrus-sac (57–65 µm, reaching midline of proglottis vs 30–33 µm, not reaching midline of proglottis), a larger ovary (61–66 × 28–36 vs 48 × 22 µm) and a larger number of eggs in gravid proglottides (16–20 vs 8–9). In addition, the cirrus of S. infirma is cylindrical, while in S. soricis it is conical.

Soricinia quarta (Karpenko, 1983) Karpenko, 1999

Syn. Ditestolepis quarta Karpenko, 1983

Type-host: Sorex isodon Turov (Soricomorpha: Soricidae).

Type-locality: Solnechny District of Khabarovsk Kray, Russian Federation (see Karpenko, 1983).

Site in host: Intestine.

Type-material: Holotype (ISEA 3589, S. isodon, village Beryosovka, Solnechny District of Khabarovsk Kray, Russian Federation, coll. 16.viii.1979; host field number 3589). The holotype and five paratypes of the same species are on the same slide. The holotype is clearly indicated.

Redescription (Fig. 3)

[Based on the holotype and four paratypes; measurements of the holotype are followed by the range, mean and number of measurements in parentheses.] Small tapeworms, 500 (400–500; 450; n = 5) long. Strobilation gradual. Strobila consisting of 17 (15–20; 17; n = 5) proglottides: 3–4 juvenile, 3–4 hermaphroditic (1 mature), 7–8 postmature and 1–4 gravid. Proglottides acraspedote, transversely elongate (Fig. 3B). Mature proglottis 35 × 87 (29–35 × 85–87; 31 × 86; n = 5), pregravid proglottides 59–62 × 101–102 (54–62 × 101–105; 57 × 103; n = 5). Primordia of male and female gonads appearing simultaneously subsequent maturation following functional protandry pattern.

Fig. 3
figure 3

Soricinia quarta Karpenko, 1983 ex Sorex isodon Turov. Holotype. A, Total view; B, Mature proglottides; C, Cirrus-sac; D, Invaginated cirrus. Scale-bars: A, 100 µm; B, 50 µm; C, 40 µm; D, 20 µm

Full size image

Osmoregulatory canals without transverse anastomoses. Ventral osmoregulatory canals 2–3 (2–3; 2.4; n = 5) in diameter, dorsal canals 1–2 (1–2; 1.6; n = 5) in diameter. Genital pores unilateral, dextral, opening in middle of proglottis margin. Genital atrium cylindrical, simple, 3–4 (3–4; 3.6; n = 5) deep.

Scolex relatively large, slightly compressed dorso-ventrally, 155 (155–160; 157; n = 5) wide. Neck 52 (52–62; 57; n = 5) wide, clearly differentiated from scolex. Suckers elongate, bothrium-like, 97–98 × 81–83 (89–98 × 81–87; 93 × 85; n = 5), with muscular thickening along edges. Rhynchus and rostellar apparatus absent.

Testes 3, oval, 14–21 × 11–13 (13–21 × 10–14; 16 × 12; n = 10), 1 poral and 2 antiporal, arranged in almost right-angled triangle in median field of proglottis (Fig. 2B). Cirrus-sac cigar-shaped, elongated, thin-walled, 35 × 7 (35–40 × 7–9; 37 × 8; n = 5), crossing poral osmoregulatory canals, not reaching midline of proglottis (Fig. 2B, C). Cirrus cylindrical, large, 15–17 (15–18; 17; n = 5), armed. Parabasal portion of cirrus covered with numerous small spines; longest spines in apical part of cirrus (Fig. D). Internal seminal vesicle oval, 11 × 6 (10–13 × 6–7; 11 × 6; n = 5); external seminal vesicle elongated, 23 × 8 (22–24 × 8–11; 23 × 9; n = 6), positioned along anterior margin of proglottis, may be bent toward centre of proglottis.

Ovary tri-lobed, 54 × 23 (45–60 × 23–30; 50 × 24; n = 5), in middle of proglottis, anterior and ventral to testes. Vitellarium compact, oval, 20 × 13 (15–22 × 12–16; 19 × 14; n = 5), antiporal, ventral to testes, posterior to ovary. Vagina thin-walled, opening ventral to cirrus-sac. Copulatory part of vagina 21 × 7 (19–21 × 6–7; 20 × 7; n = 5). Uterus sac-like, occupying almost entire median field, not extending laterally beyond osmoregulatory canals. Uterus in pregravid proglottides containing 32–35 (30–35; 33; n = 7) eggs. No gravid proglottides were observed.

Remarks

This species has been described as Ditestolepis quarta Karpenko, 1983 from S. isodon collected in the Khabarovsk Kray (Russian Federation) (Karpenko, 1983). Later, he (Karpenko, 1999) re-described the species from S. unguiculatus Dobson collected on Kunashir Island (Kuril Archipelago, Russian Federation), transferred it to Soricinia and proposed an amended generic diagnosis of Soricinia. However, Karpenko’s generic diagnosis contained several inaccuracies. Among other characters, he listed the cirrus-sac as not extending to the midline of the proglottis, a slightly lobate ovary and the possibility of gravid proglottides detaching from the strobila in groups. However, according to Korneva & Kornienko (2014), eggs of Soricinia possess sclerotised outer envelope and are dispersed in the environment individually through ruptures in the uterine and proglottis walls.

Our reexamination of the type-material of S. quarta revealed inaccuracies in the original description by Karpenko (1983) who described the suckers in this species as cup-shaped (bothrium-like according to our observations) and the strobilation as serial (in reality it is gradual). These errors were later incorporated by Karpenko (1999) in the generic diagnosis of Soricinia. Moreover, the holotype appears to be morphologically different from the remaining specimens in the type-series. In addition, some features provided in the re-description by Karpenko (1999) from Kunashir Island differed significantly from those in the original description (see Karpenko, 1983; Table 1). In part, the cirrus-sac and cirrus in the specimens from Kunashir Island are almost twice as long as the cirrus-sac and cirrus in S. quarta from the Khabarovsk Kray (60–72 and 45–52 vs 37–42 and 21–22 µm). In the original description, the ovary is tri-lobed while in the text of the redescription it is referred to as slightly lobed, but illustrated as entire (figure 2 in Karpenko, 1999). The number of proglottides in the two forms is also different (22–23 in specimens from Kunashir vs 11–21 in the original description). Karpenko (1999) explained these differences by the poor condition of his specimens from Kunashir Island (i.e. upon which the redescription was based). Our morphological examination of both the type-specimen and the specimens from Kunashir Island collected by Karpenko (1999) has confirmed that Karpenko’s (1999) description of specimens from Kunashir was accurate. However, his identification was erroneous because the specimens from Kunashir certainly belong to a different, yet undescribed species.

Table 1 Morphological variation in different descriptions of Soricinia quarta
Full size table

Soricinia quarta is morphologically most similar to S. aurita Irzhavsky, Gulyaev & Kornienko, 2005 from the Caucasian shrew S. satunini Ognev and S. sawadai Zubova, Gulyaev & Kornienko, 2010 from S. unguiculatus from Sakhalin Island (Far East of Russian Federation). In these three species, the suckers are located in dorsal and ventral bothrium-like depressions. Soricinia quarta can be distinguished from the other two species by the shape of the ovary, the length of the cirrus-sac and cirrus, and the number of eggs per proglottis (Irzhavsky et al., 2005; Zubova et al., 2010). The cirrus-sac of S. quarta is more than 2–3 times shorter than in S. aurita and S. sawadai and not reaching the midline of proglottis whereas it crosses the midline in the latter two species. The ovary of S. quarta is tri-lobed, whereas the ovary in S. aurita and S. sawadai is compact. The number of eggs in the gravid proglottides of S. quarta is much greater than in S. sawadai (30–45 vs 15–22). Although the cirrus armature is overall similar in the three species, S. quarta has long needle-shaped spines on the apical part of the cirrus whereas in S. aurita and S. sawadai spines are located on the parabasal part of the cirrus.

Genus Soricinia Spassky & Spasskaja, 1954

Amended diagnosis (modified after Vaucher in Czaplinski & Vaucher, 1994)

Small Hymenolepididae. Strobila consisting of few proglottides. Development of proglottides gradual. Proglottides transversely elongate, acraspedote. Scolex relatively large, unarmed, without rostellar apparatus; suckers cup-shaped. Osmoregulatory canals without transverse anastomoses. Testes three, one poral and two antiporal, situated in a triangle or in a row. Cirrus-sac crossing poral osmoregulatory canals, sometimes extending beyond midline of proglottis. Cirrus armed. Internal and external seminal vesicle both present; internal seminal vesicle small. Ovary entire or tri-lobed. Vitellarium subspherical, postovarian, compact. Uterus median, sac-like. Eggs relatively few. Parasites of shrews of the genera Sorex L. and Neomys Kaup in the Holarctic.

Type-species: Soricinia soricis (Baer, 1925) Spassky & Spasskaja, 1954 (syn. Hymenolepis minuta Baer, 1925) ex S. alpinus from France.

Other species:

  • Soricinia aurita (Irzhavsky, Gulyaev & Kornienko, 2005) Zubova, Gulyaev & Kornienko, 2010 (syn. Insectivorolepis aurita Irzhavsky, Gulyaev & Kornienko, 2005) ex S. raddei Satunin and S. volnuchini Ognev from Central Caucasus (the Kabardino-Balkar Republic, Russian Federation) (Irzhavsky et al., 2005; Zubova et al., 2010);

  • Soricinia bargusinica Eltyschev, 1975 [syn. Insectivorolepis bargusinica (Eltyschev, 1975) Afanasjeva, 1993)] ex S. araneus and S. caecutiens from East Siberia (Russian Federation) (Eltyschev, 1975; Afanasjeva, 1993);

  • Soricinia genovi Binkiene, Kornienko & Tkach, 2015 ex Neomys fodiens from the Rhodope Mountains (Bulgaria) (Binkienė et al., 2015);

  • Soricinia globosa (Baer, 1931) Vaucher in Czaplinski & Vaucher, 1994 [syns Hymenolepis globosa Baer, 1931; Insectivorolepis globosa (Baer, 1931) Zarnowski, 1955; Dicranotaenia globosa (Baer, 1931) López-Neyra, 1942)] ex Neomys anomalus Cabrera and N. fodiens from Switzerland (Baer, 1931; López-Neyra, 1942; Žarnowski, 1955; Vaucher in Czaplinski & Vaucher, 1994);

  • Soricinia infirma (Zarnowski, 1955) Vaucher in Czaplinski & Vaucher, 1994 [syns Insectivorolepis infirma Zarnowski, 1955; Ditestolepis secunda Schaldybin, 1964] ex S. araneus and S. minutus L. from Białowieża Forest (Poland) (Žarnowski, 1955; Schaldybin, 1964);

  • Soricinia kenki (Locker & Rausch, 1952) Vaucher in Czaplinski & Vaucher, 1994 [syns Hymenolepis kenki Locker & Rausch, 1952; Insectivorolepis kenki (Locker & Rausch, 1952) Zarnowski, 1955] ex S. vagrans vagrans Baird from North America (Oregon, USA) (Locker & Rausch, 1952; Žarnowski, 1955; Vaucher in Czaplinski & Vaucher, 1994; Locker & Rausch, 1952);

  • Soricinia quarta (Karpenko, 1983) Karpenko, 1999 [syns Ditestolepis quarta Karpenko, 1983; Insectivorolepis macracetabulosa Sawada & Koyasu, 1991)] ex S. isodon, S. unguiculatus and S. caecutiens from Khabarovsk Kray (Russian Federation) (Karpenko, 1983; Karpenko, 1999; Sawada & Koyasu, 1991);

  • Soricinia sawadai Zubova, Gulyaev & Kornienko, 2010 ex S. unguiculatus from Sakhalin Island (Russian Federation) (Zubova et al., 2010).

Key to the species of Soricinia

  1. 1a

    Number of proglottides < 15 ……… 2

  2. 1b

    Number of proglottides > 15 ……… 3

  3. 2a

    Number of proglottides 10–13; cirrus-sac 57–65 µm long, reaching midline of proglottis; cirrus cylindrical; number of eggs 16–20 ……… S. infirma (Zarnowski, 1955)

  4. 2b

    Number of proglottides 9; cirrus-sac 30 µm long, not reaching midline of proglottis; cirrus conical; number of eggs 8–9 ……… S. soricis (Baer, 1925)

  5. 3a

    Cirrus-sac reaching midline of proglottis; ovary entire ……… 4

  6. 3b

    Cirrus-sac not reaching midline of proglottis; ovary tri-lobed ……… 7

  7. 4a

    Number of proglottides 55–60; cirrus-sac 108–115 µm long; number of eggs 100–110, parasite of Nearctic shrews ……… S. kenki (Locker & Rausch, 1952)

  8. 4b

    Number of proglottides 19–30, parasites of Palaearctic shrews ……… 5

  9. 5a

    Copulatory part of vagina with well-developed vaginal sphincter; number of proglottides 30; number of eggs 10–16 ……… S. globosa (Baer, 1931)

  10. 5b

    Copulatory part of vagina without distinct vaginal sphincter; number of proglottides 19–26; number of eggs 15–30 ……… 6

  11. 6a

    Entire cirrus covered with needle-shaped spines decreasing towards the apical part of cirrus; cirrus 52–55 µm long; number of proglottides 19–22; number of eggs c.30 ……… S. aurita (Irzhavskii, Gulyaev & Kornienko, 2005)

  12. 6b

    Parabasal portion of cirrus covered with long needle-shaped spines, apical part of cirrus unarmed; cirrus 65–70 µm long; number of proglottides 23–26; number of eggs 15–22 ……… S. sawadai Zubova, Gulyaev & Kornienko, 2010

  13. 7a

    Number of proglottides c.90; cirrus-sac 90 µm long; number of eggs 85–100 ……… S. bargusinica Eltyschev, 1975

  14. 7b

    Number of proglottides < 25; cirrus-sac shorter than 60 µm; number of eggs < 60 ……… 8

  15. 8a

    Number of proglottides 15–20; cirrus-sac 37–40 µm long; number of eggs 32–35 ……… S. quarta Karpenko, 1983

  16. 8b

    Number of proglottides 19–25; cirrus-sac 47–60 µm long; number of eggs 40–52 ……… S. genovi Binkienė, Kornienko & Tkach, 2015

Discussion

Representatives of Soricinia are broadly distributed in the Holarctic and parasitise a number of shrew species belonging to Sorex and Neomys (Table 2). Despite several attempts to revise the genus (Gulyaev, 1991; Vaucher in Czaplinski & Vaucher, 1994; Karpenko, 1999; Irzhavsky et al., 2005; Zubova et al., 2010), the systematic position and species composition of the genus remains controversial. Spassky (1954) erected Soricinia as monotypic. However, due to the incompleteness of the first description of the type-species S. soricis and several inaccuracies in the original generic diagnosis (presence of serial metamerism, fusion of gravid segments into syncapsule), the boundaries of the genus were blurred. This resulted in the inclusion in Soricinia of numerous species that later proved to belong to other genera, e.g. Soricinia collaris Karpenko, 1984, transferred to Ecrinolepis Spassky & Karpenko, 1983 by Gulyaev (1991); Soricinia macrospina Karpenko, 1984, transferred to Ecrinolepis by Gulyaev (1991); Soricinia aporalis Karpenko, 1984, transferred to Ecrinolepis by Gulyaev (1991); Soricinia cirravaginata Eltyshev, 1975, synonymised with Ecrinolepis longibursata (Morozov, 1957) by Gulyaev (1991); Soricinia japonica Sawada & Koyasu, 1991, synonymised with Mathevolepis skrjabini (Sadovskaja, 1965) by Gulyaev & Karpenko (1998); and Soricinia tripartita Zarnowski, 1955, transferred to Gulyaevilepis Kornienko & Binkiene 2014 by Kornienko & Binkiene (2014). In addition, Soricinia longisegmentalis Sawada & Kobayashi, 1994 should be removed from Soricinia due to the presence of serial metamerism in this species (see Sawada & Kobayashi, 1994). Likewise, Soricinia syncapsulata Nanda & Malholtra, 1991 does not belong to Soricinia because of the presence of a rudimentary rostellum and uterine syncapsules (see Nanda & Malholtra, 1991).

Table 2 List of the species of Soricinia Spassky & Spasskaja, 1954, their hosts and geographical distribution
Full size table

Zubova et al. (2010) compared the descriptions of I. macracetabulosa published by Sawada & Harada (1993) and Sawada & Koyasu (1991) and concluded that I. macracetabulosa of Sawada & Koyasu (1991) is a synonym of S. quarta, whereas I. macracetabulosa of Sawada & Harada (1993) is a distinct species, which they named Soricinia haradai Zubova, Gulyaev & Kornienko, 2010. Zubova et al. (2010) mentioned the differences in the number of proglottides, the size of the scolex and the length of the cirrus and cirrus-sac as distinguishing characters. However, our comparison of the two descriptions of I. macracetabulosa did not show any significant differences between the two forms. Therefore, we consider the S. haradai a junior synonym of S. quarta.

In conclusion, the re-examination of type-materials and/or freshly collected specimens of several species of Soricinia (S. soricis, S. infirma, S. quarta, S. globosa, S. genovi, S. bargusinica, S. aurita, S. sawadai) allowed us to confirm their congeneric status and to amend the diagnosis of Soricinia incorporating important morphological characteristics of the genus. Remarkably, in contrast to the high diversity of Soricinia spp. in the Palaearctic species of the genera Sorex and Neomys, only a single species of Soricinia is known from North American shrews, namely S. kenki. Considering the diverse fauna and broad distribution of Sorex spp. in North America, we anticipate that additional species of Soricinia may be discovered from shrews in the Nearctic.