LAGUNA（汽水域研究）15，19〜23 頁（2008 年 12 月）
LAGUNA 15，p.19–23（2008）

Some leeches (Annelida: Hirudinida: Piscicolidae,
Glossiphoniidae) in the Hii River system,
Shimane Prefecture, Japan
Takeo Yamauchi1, Tetsuya Itoh2, Katsuhide Yamaguchi3 and Kazuya Nagasawa4
Abstract: During a parasitological survey in the Hii River system including two brackishwater lakes, Shinjiko and Nakaumi, three species of leeches (an unidentified piscicolid,
Limnotrachelobdella okae, and Batracobdella kasmiana) were recorded. The unidentified
species was collected from the body surface of Japanese icefish Salangichthys microdon
captured in Shinjiko and the Ôhashi River. Limnotrachelobdella okae was found unattachedin both Shinjiko and Nakaumi. Batracobdella kasmiana was collected from the mussel Unio
douglasiae nipponensis from the Hii River. Color photographs of live specimens of these leeches
are given.
Key words: Batracobdella kasmiana, Limnotrachelobdella okae, Unio douglasiae nipponensis,
Salangichthys microdon, brackish-water lake, coloration.

Introduction

acranulata (Whitman, 1886), Whitmania pigra (Whitman,
1884), Dina lineate (O. F. Müller, 1774) (as Erpobdellalineata), Erpobdella octoculata japonica Pawlowski, 1962(as Erpobdella octoculata), Erpobdella testacea (Savigny,1822), and Mimobdella japonica Branchard, 1897 because
many ecological and faunal studies of benthic animals
have been conducted in the river system including two
brackish-water lakes, Shinjiko and Nakaumi.
During a parasitological survey in the Hii River system,
three species of leeches were collected. The present paper
provides distributional and ecological data of these leeches
in the river system.

Leeches (Annelida: Hirudinida) are distributed worldwide and can be found living in marine, estuarine, moist
terrestrial and freshwater ecosystems (Sawyer, 1986). Although about 60 species of leeches are recorded in Japan(Itoh, 2003), only fragmentary information is available.
For most species of Japan, little is known about their host
preference and geographical distribution.
To date, the leech fauna of Chugoku District has beenpoorly understood. However, 12 leech species (five in
the Glossiphoniidae; one in the Piscicolidae; two in the
Hirudinidae; four in the Erpobdellidae) are known in
the Hii River system (Uéno, 1943; Anonymous, 2000):
Alboglossiphonia lata (Oka, 1910) (as Glossiphonia
weberi lata), Glossiphonia complanata (Linnaeus, 1758),
Helobdella stagnalis (Linnaeus, 1758), Hemiclepis
japonica (Oka, 1932) (as Placobdella japonica),
Placobdelloides okadai (Oka, 1925) (as Hemiclepis
okadai), “Ichthyobdella uobir Oka, 1910”, Whitmania
12
3
4

Materials and Methods
The Hii River system (Fig. 1) consists of the riveritself, Shinjiko, the Ôhashi River, Nakaumi, and the Sakai
Channel. Both Shinjiko and Nakaumi form an estuarine
system which opens to the Sea of Japan. These lakes andthe Ôhashi River, a short connecting river between the

Toyama Institute of Health, Imizu 939-0363, JAPANMarine Biological Research Institute of Japan Co., Ltd. (Sapporo Branch), Sapporo 007-0862, JAPANShinjiko Nature Museum, Izumo 691-0076, JAPANGraduate School of Biosphere Science, Hiroshima University, Higashi-Hiroshima 739-8528, JAPAN

19

20

Takeo Yamauchi, Tetsuya Itoh, Katsuhide Yamaguchi and Kazuya Nagasawa

Sea of Japan
NakaumiShinjikoÔhashi River

Sakai Channel

Hii River

䂥
0

400km

䂦
䃂

䃂

䂦

Fig. 1. Map of the Hii River system, Shimane and Tottori Prefectures, Japan. Two closed
circles, two open triangles, and a closed triangle represent collection localities of Piscicolidae
gen. sp., Limnotrachelobdella okae, and Batracobdella kasmiana, respectively.

lakes, are the largest brackish-water ecosystem remaining
in Japan at present.
In March to July 2002 and February 2004, fishes were
captured by a pound stationary net (Japanese name:Masu-ami) in Shinjiko, the Ôhashi River, and Nakaumi
and were macroscopically examined. On September 16,
2002, we collected a leech from a mussel Unio douglasiae
nipponensis Martens, 1877, that had been sampled from theHii River (between two bridges, Nada-bashi and Mizuhoô-hashi) and reared in an aquarium of the Shinjiko Nature
Museum (SNM). The mussel examined had no experience
to cohabit with populations from other localities.
The leeches collected were photographed alive for
their coloration. Then, they were fixed in 10% formalin,preserved in 70% ethanol, then examined and measured
under a stereoscopic microscope. Specimens examined inthis paper are deposited in the National Science Museum,
Tokyo (NSMT-An 388, 389, 390, 391). The common andscientific names of fishes follow those recommended
by Froese and Pauly (2007) and the scientific names ofmussels follow Masuda and Uchiyama (2004).

Results
Two leeches were found attached to the body surface ofJapanese icefish Salangichthys microdon (Bleeker, 1860):
one (Figs. 2-4) was found in Shinjiko (off Aika, Matsue)
on March 24, 2002, and another was in the Ôhashi Riveron February 15, 2004. The icefish (79.5 mm SL [standard
length]) attached by latter was dead when the leech wascollected. Two leeches were identified as Piscicolidae

gen. sp. on the basis of the following characters: bodycolor light yellow with pale-green pigmentation (in fresh);radial color pattern on the surface of caudal sucker; 18.8mm in total length [TL]; 2.4 mm in maximum body width[MBW]; cylindrical body; neck region indistinct fromabdomen; pulsatile vesicles on both lateral sides of bodyunclear; male and female gonopores on the segment XII;
annulation of body unclear; and one pair of eyes on thedorsal surface of anterior sucker. A few days after theleech was collected in Shinjiko, it was retained in a petri
dish containing water of Shinjiko and deposited lightbrown cocoons (Fig. 5). Unfortunately, the leech collectedin Shinjiko was not preserved.
Two unattached leeches were found among fishes
consisting of various species: one (Figs. 6-7) was foundin Shinjiko (off Aika, Matsue) on April 26, 2002, andanother was in Nakaumi (off Ronden, Yasugi) on April 29,
2002. They were identified as Limnotrachelobdella okae
(Moore, 1924) based on the following characters: color
black (in fresh) or pale black (in 70% ethanol); 75-87
mm TL; 17.0-17.5 mm MBW; body flattened, markedly
subdivided into neck and abdomen region; caudal sucker
considerably less than maximum body width. Althoughthese specimens almost agree to the descriptions of Sawyer(1986), Epshtein (1987) and Nagasawa et al. (2008),
lateral margins of their body have indistinct vesicles. We
donʼt think that this difference is important enough for
specific segregation.
A leech (Figs. 8-11) was collected from U. douglasiae
nipponensis (infection site unrecorded, see Materials
and Methods) on September 16, 2002. The leech wasSome leeches (Annelida: Hirudinida: Piscicolidae, Glossiphoniidae) in the Hii River system, Shimane Prefecture, Japan

21

4

2

3

5

6

10

7

8

9

11

Figs. 2-11. Live leeches collected in the Hii River system. 2: Piscicolidae gen. sp., lateral view. 3: Ditto,
dorsal view. 4: Ditto, caudal sucker, lateral view. 5: Ditto, cocoon. 6: Limnotrachelobdella okae, ventral view.
7: Ditto, oral sucker and trachelosome, ventral view. 8: Batracobdella kasmiana, dorsal view. 9: Ditto, ventral
view. 10: Ditto, oral sucker, dorsal view. 11: Ditto, caudal sucker, dorsal view. Scale bars: 20 mm in Fig. 6; 10
mm in Figs. 7-9; 1 mm in Fig. 10; 2 mm in Fig. 11. Scale bars are not given in Figs. 2-5 for Piscicolidae gen.
sp. because its live specimen was not measured.

identified as Batracobdella kasmiana (Oka, 1910), whichshow the following characters: color translucent yellowish
brown dorsally with five yellow longitudinal stripes (Fig.
8); 11.1 mm TL; 3.8 mm MBW; body elongated, headslightly broadened; eyes one pair (Fig. 10).

Discussion
The unidentified piscicolids found this study resemble
members of the genus Piscicola in the body shape andradial coloration of the caudal sucker. However, we
could not accurately observe their annulation and sexual
reproductive organs. Uéno (1943) recorded marine

piscicolid leeches (as “Uobiru” in Japanese = Ichthyobdellauobir) heavily parasitizing common carp Cyprinus carpio
carpio Linnaeus, 1758 in Shinjiko. Our specimen is
obviously different from I. uobir, which is presently as a
junior synonym of Beringobdella rectangulata (Levinsen,
1881), in the body shape and marking. Japanese icefish isan economically important fish in the two brackish-waterlakes surveyed. Further study on the leech infection of fish
should be made in the river system.
Limnotrachelobdella okae is distributed in Japan, China,
and Russia (Epshtein, 1962, 1987; Yang, 1987; Furinesset al., 2007; Nagasawa et al., 2008a, 2008b, 2009). On
the Japanese coast of the Sea of Japan, L. okae has so far

22

Takeo Yamauchi, Tetsuya Itoh, Katsuhide Yamaguchi and Kazuya Nagasawa

been reported only from Ishikawa (as Kaga) (Oka, 1910)
and Yamagata (Nagasawa et al., 2009). Accordingly, thepresent finding represents the third distributional recordof L. okae from the Japanese coastal Sea of Japan. The
species has hitherto been reported from a variety of hostfishes from Japan (Mizuno, 1989, 2006; Furiness et al.,2007; Nagasawa and Fukuda, 2008; Nagasawa et al.,2008a, 2008b, 2009). However, it is uncertain whether,when we collected our specimens, they were attached tofish hosts or were free in the water because the specimens
were found unattached among the fishes captured by thenet. Further, although the species is known to inhabit on
marine, brackish and fresh waters (Oka, 1927b, 1947b;
Oka and Nagao, 1965b), there is no reliable record inbrackish and fresh waters in Japan. This is the first recordof L. okae from brackish-water lakes. Especially, thefinding in Shinjiko, a low saline, brackish-water lake, issignificant in relation to its distribution. Nagasawa et al.
(2008a) have recently suggested that L. okae is a coastal
marine or brackish-water species.
Batracobdella kasmiana is known as a parasite ofmussels, including Cristaria plicata (Leach, 1815) andAnodonta spp. (Oka, 1927a, 1947a; Oka and Nagao,
1965a; Sawyer, 1986; Yang, 1996). In China, this leech
also parasitizes Unio douglasiae (Gray in Griffith andPidgeon, 1834) (Yang, 1996). Our finding of B. kasmiana
from U. douglasiae nipponensis is the new host record inJapan.

Acknowledgements
We thank Mr. Norihisa Aoyama (SNM) for collecting
the B. kasmiana specimens and Mr. Kô Sasaki (SNM) forcollecting an unidentified piscicolid. Part of the present
study was supported by a Grant-in-Aid for Scientific
Research (B) (No. 18380116) from the Japan Society for
the Promotion of Science.

References
Anonymous (2000) Benthic animals in the Hii Riversystem. 170 pp. Izumo Work Office, Chugoku Regional
Construction Bureau, Ministry of Construction, Izumo(in Japanese).
Epshtein, V. M. (1962) A survey of fish leeches (Hirudinea,
Piscicolidae) from the Bering and Okhotsk Seas andfrom the Sea of Japan. Dokl. Acad. Nauk SSSR, 144:
1181-1184 (in Russian). [English translation].
Epshtein, V. M. (1987) Annelida. In: Identification key toparasites of the freshwater fishes of the USSR. Vol. 3,
Metazoan parasites, Part 2. (ed.) Bauer, O. N. pp. 340372. Nauka, Leningrad (in Russian).
Froese, R. and Pauly, D. (eds.) (2007) FishBase. World
Wide Web electronic publication. www.fishbase.org,

version (11/2007).
Furiness, S., Williams, J. I., Nagasawa, K. and Burreson,
E. M. (2007) A collection of fish leeches (Hirudinida:
Piscicolidae) from Japan and surrounding waters
including redescriptions of three species. J. Parasitol.,
93: 875-883.
Itoh, T. (2003) Annelida, Hirudinea. In: The flora andfauna of inland waters in the Ryukyu Islands. (eds.)
Nishida M., Shikatani, N. and Shokita, S. pp. 197-202.
Tokai University Press, Tokyo (in Japanese).
Masuda, O. and Uchiyama, R. (2004) PISCES Ecologicalfield guide series 2 freshwater mollusks of Japan.
2 freshwater mollusks of Japan. Including brackish
water species. PISCES Publishers Co., Ltd., Tokyo (inJapanese).
Mizuno, Y. (1989) Limnotrachelobdella infection. In:
Atlas of fish diseases. (eds.) Hatai, K., Ogawa, K. andHirose, H. p. 20. Midori Shobo Publishing, Tokyo (inJapanese).
Mizuno, Y. (2006) Limnotrachelobdella infection(Limnotrachelobdellosis). In: New atlas of fish diseases.
(eds.) Hatai, K. and Ogawa, K. p. 163. Midori Shobo
Publishing, Tokyo (in Japanese).
Nagasawa, K. and Fukuda, Y. (2008) A case of infestation
by Limnotrachelobdella okae (Hirudinida: Piscicolidae)
on Japanese amberjack Seriola quinqueradiata cultured
in Kyushu, Japan. J. Grad. Sch. Biosp. Sci., Hiroshima
Univ., 47 (29-34).
Nagasawa, K., Ueno, Y., Ishito, Y. and Yamauchi, T. (2008a)
Limnotrachelobdella okae (Hirudinida, Piscicolidae)
from cherry salmon Oncorhynchus masou masou in
neritic deep waters of the western North Pacific Ocean.
Biogeography, 10: 33-39.
Nagasawa, K., Yamauchi, T. and Umino, T. (2008b)
Synopsis of leeches of the families Piscicolidae andOzobranchidae (Annelida, Rhynchobdellida) in Japan(1895-2008). Bull. Jpn. Soc. Biogeogr., 63 (151-171)(in Japanese with English abstract).
Nagasawa, K., Izumikawa, K., Yamanoi, H. and Umino,
T. (2009) New hosts, including marine fishes cultured
in Japan, of Limnotrachelobdella okae (Hirudinida:
Piscicolidae). Comp. Parasitol., 76 (127-129).
Oka, A. (1910) Synopsis der Japanischen Hirudineen, mit
Diagnosen der Neuen Species. Annotnes. Zool. Jpn., 7:165-183.
Oka, A. (1927a) Hemiclepsis kasmiana Oka. In: Illustrated
encyclopedia of the fauna of Japan. (eds.) Oka, A. et al.
p. 1596. Hokuryukan, Tokyo (in Japanese).
Oka, A. (1927b) Trachelobdella okae Moore. In: Illustrated
encyclopedia of the fauna of Japan. (eds.) Oka, A. et al.
p. 1601. Hokuryukan, Tokyo (in Japanese).
Oka, A. (1947a) Hemiclepsis kasmiana Oka. In: Revisedand enlarged illustrated encyclopedia of the fauna ofJapan. (ed.) Uchida, S. p. 1385. Hokuryukan. Tokyo (inSome leeches (Annelida: Hirudinida: Piscicolidae, Glossiphoniidae) in the Hii River system, Shimane Prefecture, Japan

Japanese).
Oka, A. (1947b) Trachelobdella okae Moore. In: Revisedand enlarged illustrated encyclopedia of the fauna ofJapan. (ed.) Uchida, S. p. 1389. Hokuryukan. Tokyo (inJapanese).
Oka, A. and Nagao, Z. (1965a) Hemiclepsis kasmianaOka. In: New illustrated encyclopedia of the fauna ofJapan, Part I. (eds.) Okada, Y., Uchida, S. and Uchida,T. p. 568. Hokuryukan. Tokyo (in Japanese).
Oka, A. and Nagao, Z. (1965b) Trachelobdella okae
Moore. In: New illustrated encyclopedia of the fauna ofJapan, Part I. (eds.) Okada, Y., Uchida, S. and Uchida,T. p. 569. Hokuryukan. Tokyo (in Japanese).
Sawyer, R. T. (1986) Leech biology and behaviour. Vol.

23

II, Feeding biology, ecology, and systematics. 375 pp.
Clarendon Press, Oxford.
Uéno, M. (1943) Ecological studies on Japanese brackish
waters, with special reference to brackish lakes. I.
Benthic fauna of brackish lakes along the Japan Sea
coast. Sci. Rep. Hattori Hôkôkai, (10): 409-425 (inJapanese).
Yang, T. (1987) On the genus Limnotrachelobdella
Epshtein, 1968 and a new species from South China
Sea. Acta Hydrobiol. Sin., 11: 268-273 (in Chinese withEnglish abstract).
Yang, T. (ed.) (1996) Annelida, Hirudinea. Fauna Sinica.
259 pp. Science Press, Beijing (in Chinese with English
abstract).