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Discovery of Natural Infection by Metagonimus Hakubaensis Shimazu, 1999 (Trematoda: Heterophyidae) in Japanese Water Shrews (Chimarrogale Platycephala) in Japan

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Discovery of Natural Infection by Metagonimus Hakubaensis Shimazu, 1999 (Trematoda: Heterophyidae) in Japanese Water Shrews (Chimarrogale Platycephala) in Japan NOTE Wildlife Science Discovery of Natural Infection by Metagonimus hakubaensis Shimazu, 1999 (Trematoda: Heterophyidae) in Japanese Water Shrews (Chimarrogale platycephala) in Japan Noboru KUDO1)*, Kai SHIGETA1), Koji MATSUMOTO1) and Takashi OYAMADA1) 1)Department of Veterinary Parasitology, School of Veterinary Medicine, Kitasato University, Towada, Aomori 034–8628, Japan (Received 30 May 2014/Accepted 23 July 2014/Published online in J-STAGE 12 August 2014) ABSTRACT. A total of 611 preserved adult Metagonimus spp. specimens recovered from 32 of 53 Japanese water shrews (Chimarrogale platycephala) that had previously been collected in Aomori Prefecture between June 1994 and August 1996, were examined in this study. Morphological examination revealed that 603 of these flukes were identical toM. hakubaensis Shimazu, 1999, and that the others were M. takahashii Suzuki, 1930 (n=4), M. otsurui Saito et Shimizu, 1968 (n=2), and M. miyatai Saito et al., 1997 (n=2). Each of the 32 Japanese water shrews infected with M. hakubaensis contained between 1 and 83 flukes. This is the first record of the natural final host for M. hakubaensis, since this fluke species was described. KEY WORDS: first record, Japanese water shrew, Metagonimus hakubaensis, natural final host doi: 10.1292/jvms.14-0281; J. Vet. Med. Sci. 76(11): 1531–1533, 2014 Metagonimus hakubaensis Shimazu, 1999 was originally from the intestines of 32 water shrews. Of these flukes, 603 described from laboratory rats that had been orally adminis- were identical to M. hakubaensis, and the others were identi- tered metacercariae recovered from sand lampreys (Lethen- fied asM. takahashii (n=4), M. otsurui (n=2) and M. miyatai teron reissneri (Dybowski)) from Nagano Prefecture, Japan (n=2). Metagonimus hakubaensis was found in all of the [6]. Trematodes in the genus Metagonimus occur naturally infected animals, and the number of flukes recovered from in the small intestines of a variety of mammals and birds. each animal ranged from 1 to 83. Representative specimens In Japan, natural infections of M. yokogawai (Katsurada, of M. hakubaensis were deposited in the collection of the 1912), M. takahashii Suzuki, 1930 and M. miyatai Saito et Meguro Parasitological Museum (MPM Coll. No. 20948). al., 1997, have been reported in dogs, cats, pigs, raccoon In addition, Plagiorchis fuji and Echinostoma hortense were dogs, weasels, martens, red foxes, Japanese water shrews, detected in 38 and 2 water shrews, respectively. Although 3 thrushes, kites, gulls and humans [2, 3]. Although M. otsurui intestinal trematode species belonging to genus Macroorchis Saito et Shimizu, 1968 and M. katsuradai Izumi, 1935 have (Ma. chimarrogalus, Ma. elongatus and Ma. spinulosus) been recovered from Japanese water shrews and stray dogs, have been reported from Japanese water shrews in eastern respectively [5, 7], the natural final host of M. hakubaensis Japan, these flukes were not found in this study [4]. The mor- has remained unknown. We therefore conducted morpholog- phology of the M. hakubaensis specimens recovered from ical examinations of preserved Metagonimus spp. specimens the water shrews is described below. that had been recovered from Japanese water shrews (Chi- Body elongated oval or elliptical, flattened dorsoventrally, marrogale platycephala (Temminck)) collected in Aomori 600–760 µm long, maximum width of posterior half measur- Prefecture approximately 20 years previously. ing 248–320 µm (Fig. 1A and 1B). Body surface covered Between June 1994 and August 1996, a total of 53 water with minute scale-like spines, which are conspicuous on shrews were collected from three sites (Temmabayashi, anterior half of body. Oral sucker subterminal, transversely Kamikita and Sitinohe) in eastern Aomori Prefecture, Japan. elliptical, measuring 60–74 by 56–72 µm. Prepharynx short. The water shrews were examined for intestinal flukes, which Pharynx subglobular, 24–36 µm long, 26–38 µm wide. were fixed in 70% alcohol between a glass slide and a cover Esophagus 50–92 µm long, bifurcating at approximately slip, stained with alum carmine and mounted in Canada bal- anterior one-fifth of body. Two ceca extend laterally, termi- sam. The stained specimens were preserved in our laboratory nating at anterior margin of right testis and posterior margin until morphological examination. of left testis; ceca do not extend over testes to the posterior A total of 611 adult Metagonimus spp. were recovered end of body (Fig. 1C and 1D). Ventral sucker, with adjoined genital atrium, situated at middle of anterior half of body, *CORRESPONDENCE TO: KUDO, N., Department of Veterinary Parasi- deflecting to right of median line with the long axis inclined tology, School of Veterinary Medicine, Kitasato University, Towa- obliquely or directed transversely; ventral sucker is elliptical da, Aomori 034–8628, Japan. e-mail: [email protected] in shape, measuring 56–72 by 40–52 µm, slightly smaller ©2014 The Japanese Society of Veterinary Science than or equal to oral sucker in size (size ratio of ventral This is an open-access article distributed under the terms of the Creative sucker to oral sucker 0.85–1.16: 1). Testes round to elliptical, Commons Attribution Non-Commercial No Derivatives (by-nc-nd) lying obliquely at posterior end of body; right testis close to License <http://creativecommons.org/licenses/by-nc-nd/3.0/>. posterior extremity, measuring 104–150 by 70–110 µm; left 1532 N. KUDO, K. SHIGETA, K. MATSUMOTO AND T. OYAMADA Table 1. Comparison of measurements of Metagonimus hakubaensis from 2 different hosts (in µm) Present authors Shimazu (1999) Host Water shrew Rata) No. of specimens 20 20b) Body length 600–760 490–640 width 248–320 280–420 Oral sucker 60–74 × 56–72 58–78 × 43–58 Ventral sucker 56–72 × 40–52 51–70 × 39–51 Pharynx 24–36 × 26–38 27–35 × 19–31 Esophagus 50–92 20–94 Left testis 100–144 × 68–114 100–150 × 70–120 Right testis 104–150 × 70–110 100–160 × 80–120 Ovary 66–90 × 62–70 60–90 × 70–100 Seminal vesicle 70–150 × 30–60 80–136 × 40–64 Seminal receptacle 60–112 × 40–100 60–160 × 40–100 Eggs 28–32 × 16–20 28–34 × 16–20 a) Rats were experimentally infected with the metacercariae of M. hakubaensis collected from sand lampreys. b) Flukes from day 22 post- infection. similar to those recovered from experimentally infected rats (Table 1). The Japanese water shrew lives in rapidly flowing streams, small rivers and ponds, where it swims actively to capture prey, such as crabs, shrimps, tadpoles, small fishes and aquatic insects [1]. In previous surveys of metacercarial infections in fresh water fishes (unpublished data), we found an M. hakubaensis-like species in sand lampreys collected at Temmabayashi (one of the sites where M. hakubaensis was Fig. 1. Metagonimus hakubaensis recovered from a Japanese water detected in water shrews) in Aomori Prefecture. It is thus shrew. Bar=100 µm. (A, B) ventral view of entire body and (C, D) possible that the water shrews may have become infected ventral view of posterior region. with M. hakubaensis by preying on sand lampreys. Since trematodes in the genus Metagonimus infect a wide range of mammals and birds, further studies are necessary in order testis 100–144 by 68–114 µm. Ovary round or oval, 66–90 to clarify the final hosts of M. hakubaensis. This is the first by 62–70 µm in size, situated at middle of body. Seminal known record of a natural final host for M. hakubaensis, vesicle transversely elliptical, located in front of ovary, vary- since this fluke species was described. ing in size, 70–150 by 30–60 µm. Seminal receptacle oval or kidney-shaped, 60–112 by 40–100 µm, located slightly REFERENCES behind right side of ovary. Uterus occupying almost all available space in midbody from ventral sucker to testes, not 1. Imaizumi, Y. 1970. Chimarrogale platycephala. pp. 191–195. extending to posterior extremity between both testes. Vitel- In: The Handbook of Japanese Land Mammals, vol.1, Shin- laria extending in lateral and median fields from ovary to Shicho-sha, Tokyo (in Japanese). 2. Ito, J. 1964. Metagonimus and other human heterophyid trema- midlevel of left testis. Eggs yellowish-brown, oval to ellipti- todes. pp. 317–393. In: Progress of Medical Parasitology in cal in shape, with a distinct operculum, embryonated; eggs Japan, vol. 1, Meguro Parasitological Museum, Tokyo. in uterus measuring 28–32 by 16–20 µm. 3. Saito, S., Chai, J. Y., Kim, K. H., Lee, S. H. and Rim, H. J. According to Shimazu [6], M. hakubaensis is closely 1997. Metagonimus miyatai sp. nov. (Digenea: Heterophyidae), similar to M. otsurui and M. katsuradai in that the oral a new intestinal trematode transmitted by freshwater fishes in sucker is larger than the ventral sucker, but differs from these Japan and Korea. Korean J. Parasitol. 35: 223–232. [Medline] 2 species in that neither the ceca nor the vitellaria extend [CrossRef] posteriorly beyond the right testis, and the uterus hardly 4. Saito, Y., Watanabe, T. and Yamashita, T. 1982. Two new intesti- enters the post-testicular region. The morphological findings nal trematodes, Macroorchis chimarrogalus n. sp. and Macroor- of the specimens recovered from water shrews in this study chis elongatus n. sp. from Japanese water shrew and others, with a description of the metacercaria of Macroorchis chimarrogalus agree very well with previously published characteristics of n. sp. (Trematoda: Nanophyetidae). Acta Med. Biol. (Niigata) M. hakubaensis [6]. In addition, the morphometric measure- 30: 47–56. ments of the flukes recovered from the water shrews were M. HAKUBAENSIS INFECTION IN WATER SHREWS 1533 5. Saito, Y., Yamashita, T., Watanabe, T. and Saito, S. 1982. Study Bull. Nat. Sci. Mus. Ser. A 25: 87–99. on trematodes from Japanese water shrew VI. Jpn. J. Parasitol. 7. Yoshikawa, M., Miyata, I.
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