Anoplocephalidae Cholodkovsky, 1902

Sasaki, Mizuki, Anders, Jason Lee & Nakao, Minoru, 2021, Cestode fauna of murid and cricetid rodents in Hokkaido, Japan, with assignment of DNA barcodes, Species Diversity 26, pp. 255-272 : 263-264

Family Anoplocephalidae Cholodkovsky, 1902 Genus Paranoplocephala Lühe, 1910

5. Paranoplocephala kalelai ( Tenora, Haukisalmi, and Henttonen, 1985)

The adult tapeworms of Paranoplocephala kalelai (nos. 19AK378, 19AK412, 19AK419, 19AK436, 19AK454-2, and 19AK454-3) were found from My. rufocanus in Asahikawa. This is the first record from Japan. The following description was made based on one specimen ( Fig. 6A–C ): Scolex distinctly wider than neck, 0.59 in maximum width. Rostellum absent. Suckers protruding, crateriform, four in number, 0.28–0.29 in diameter. Mature proglottids shorter in length than width, 0.40–0.45 long by 0.74–0.78 wide. Genital pore located on posterior half of lateral margin. Testes spherical, 26–30 in number, forming compact group, 0.04–0.06 in diameter. Cirrus sac 0.13–0.15 long by 0.07–0.08 wide. Seminal receptacle pyriform or ovoid, 0.13–0.15 long by 0.17–0.19 wide. Ovary irregularly lobed, 0.40–0.48 in width. Vitellarium asymmetrically bilobed, 0.19–0.22 long by 0.07– 0.10 wide. Gravid proglottids longer in length than width, 1.09–1.29 long by 0.82–0.93 wide. Uterus labyrinthine, occupying entire field of proglottid.

A phylogenetic tree of cox 1 showed that P. kalelai , Paranoplocephala omphalodes (Hermann, 1783) sensu stricto, Paranoplocephala macrocephala (Douthitt, 1915) , and Paranoplocephala jarrelli (Haukisalmi, Henttonen, and Hardman, 2006) are distinguishable from one another, and that our isolates from Hokkaido should be classified as P. kalelai ( Fig. 7 ). The tree reconfirmed that the Fennoscandian isolates of P. kalelai could be divided into two clades named as Narvik and Kilpisjärvi ( Haukisalmi et al. 2004). The Hokkaido isolates of P. kalelai showed a sister relationship to the Narvik clade. The values of pairwise divergence between the Narvik and Kilpisjärvi clades and between the Hokkaido and Narvik clades were 0.034 and 0.015, respectively. The sequencing of 28S rDNA supports the species identification (see the isolate 19AK 378 in Fig. 2 ).

Members of the genus Paranoplocephala Lühe, 1910 are widely distributed in the Holarctic region ( Haukisalmi et al. 2014). Currently, the species complex of P. omphalodes sensu lato has been divided into several species ( Haukisalmi and Henttonen 2003; Haukisalmi et al. 2004, 2007; Vlasenko et al. 2019). Most species of Paranoplocephala parasitize Microtus voles, whereas P. kalelai is specific to Myodes voles in Fennoscandia ( Tenora et al. 1985; Haukisalmi et al. 2004, 2007). Our data suggest that P. kalelai is distributed widely from Fennoscandia to the Far East, along with the geographic expansion of Myodes voles.

Apodemus mice in Hokkaido also serve as definitive hosts for several species of anoplocephalid tapeworms ( Ishimoto 1974; Rausch 1976; Asakawa and Ohbayashi 1986; Iwaki et al. 1994b). Those were identified as P. omphalodes , Paranoplocephala blanchardi (Moniez, 1891) , Anoplocephaloides baeri Rausch, 1976 , and Andrya apodemi Iwaki, Tenora, Abe, Oku, and Kamiya, 1994 . Tenora et al. (1999) erected the genus Hokkaidocephala for anoplocephalid tapeworms from Apodemus mice in Hokkaido. Haukisalmi et al. (2008) examined the generic status and regarded Hokkaidocephala apodemi (= And. apodemi ) and Hokkaidocephala baeri (= Ano. baeri ) as valid species due to their unique uterine structure and development.

Moreover, unidentified species of Anoplocephalidae were recorded from Eo. smithii and Microtus montebelli (Milne- Edwards, 1872) in Honshu and Shikoku islands ( Asakawa et al. 1992c).

Figures

Fig. 6. Adult tapeworms of Paranoplocephala kalelai, Catenotaenia sp., and Raillietina sp. A, Scolex of P. kalelai; B, mature proglottid of P. kalelai; C, gravid proglottid of P. kalelai; D, scolex of Catenotaenia sp.; E, mature proglottid Catenotaenia sp.; F, gravid proglottids of Catenotaenia sp.; G, scolex of Raillietina sp.; H, mature proglottids of Raillietina sp. Scale bars: A–C, E, H, 500µm; D, G, 200µm; F, 1mm.

Fig. 7. A maximum-likelihood phylogenetic tree of the genus Paranoplocephala. The tree was made with mitochondrial cox1 sequences (546 nucleotide sites) under the substitutional model GTR+G+I. The isolates of this study (19AK378, 19AK412, 19AK419, 19AK436, 19AK454-2, and 19AK454-3) are shown in bold face. The DNA accession number of each taxon is shown in parenthesis. Hymenolepis diminuta (accession no. AF314223) was used as an outgroup taxon.

Fig. 2. A maximum likelihood phylogenetic tree of the families Hymenolepididae, Anoplocephalidae, Catenotaeniidae, and Davaineidae. The tree was made with sequences of 28S rDNA (1137 nucleotide sites) under the substitutional model GTR+G. The isolates of this study (19AK270, JA175, 19AK170, JA313, 19AK378, AMU, and Para33SI) are shown in bold face. The DNA accession number of each taxon is shown in parenthesis. Bootstrap percentages are shown on each node. Scale bar indicates the number of substitutions per nucleotide site. Dibothriocephalus nihonkaiensis (accession no. LC474508) was used as an outgroup taxon.