Bull. Natl. Mus. Nat. Sci., Ser. A, 42(3), pp. 107–122, August 22, 2016

Digeneans Parasitic in Freshwater Fishes (Osteichthyes) of Japan
VIII. Allocreadiidae, Crepidostomum
Takeshi Shimazu
10486–2 Hotaka-Ariake, Azumino, Nagano 399–8301, Japan
E-mail: azygia79@gmail.com(Received 13 May 2016; accepted 22 June 2016)

Abstract This paper reviews three species of Crepidostomum Braun, 1900 (Trematoda, Digenea,
Allocreadioidea, Allocreadiidae) parasitic in freshwater ﬁshes of Japan: Crepidostomum chaenogobii Yamaguti and Matumura, 1942, Crepidostomum farionis (Müller, 1780), and Crepidostomum
metoecus (Braun, 1900). Each species is described and ﬁgured. Crepidostomum uchimii Fujita,
1920 and Crepidostomum salmonis Fujita, 1921 are regarded as junior synonyms of C. farionis
and C. metoecus, respectively. Molecular and life-cycle studies of the three species are brieﬂymentioned. A key to the three species in Japan is presented.
Key words : Digeneans, Allocreadiidae, Crepidostomum, freshwater ﬁshes, Japan, review.

Introduction
This is the eighth paper of a series that reviews
adult digeneans (Trematoda) parasitic in freshwater ﬁshes (Osteichthyes) of Japan (Shimazu,2013). This contribution deals with three speciesof Crepidostomum Braun, 1900 in the family
Allocreadiidae Looss, 1902 sensu Caira andBogéa (2005) of the superfamily Allocreadioidea
Looss, 1902 sensu Cribb (2005). In Japan, twogenera are known in the family Allocreadiidae:
Crepidostomum with three pairs of muscularpapillae of the oral sucker and Allocreadium
Looss, 1900 with no muscular papillae (Shimazu,2016). The Introduction, Materials, and Methods
for the review were given in the ﬁrst paper(Shimazu, 2013).
Abbreviations used in the ﬁgures. cp, cirrus
pouch; cvd, common vitelline duct; dlmp, dorsolateral muscular papilla; dmmp, dorsomedialmuscular papilla; e, esophagus; ed, ejaculatory
duct; egg, egg in uterus and metraterm; ep,
excretory pore; esp, eyespot pigment; ev, excretory vesicle; ga, genital atrium; gp, genital pore;i, intestine; Lc, Laurerʼs canal; m, metraterm;
Mg, Mehlisʼ gland; o, ovary; od, oviduct; os, oral

sucker; ot, ootype; p, pharynx; pc, prostatic cells;
pp, pars prostatica; pr, prepharynx; sd, sperm
duct; sr, seminal receptacle; sv, seminal vesicle;
t, testis; tnc, transverse nerve commissure; u,uterus; vd, vitelline duct; vf, vitelline follicles;
vlmp, ventrolateral muscular papilla; vs, ventral
sucker.
Superfamily Allocreadioidea Looss, 1902
Family Allocreadiidae Looss, 1902
Genus Crepidostomum Braun, 1900
Crepidostomum chaenogobii
Yamaguti and Matumura, 1942
(Figs. 1–5)
Crepidostomum chaenogobii Yamaguti and Matumura,
1942: 117–119, ﬁgs. 1–2; Shimazu, 1981: 21–22, ﬁgs.
17–20; Shimazu, 1990: 2–3, ﬁgs. 1–4.

Hosts in Japan. “Chaenogobius annularisurotaenia Hilgendorf” (Gobiidae) (type host)(Yamaguti and Matumura, 1942), Cottus amblystomopsis Schmidt, 1904 (Cottidae) (Shimazu,
1990), Cottus hangiongensis Mori, 1930
(Shimazu, 1990), Cottus nozawae Snyder, 1911
(Shimazu, 1981), and Gymnogobius opperiens

108

Takeshi Shimazu

Figs. 1–5. Crepidostomum chaenogobii, adult specimens. — 1, holotype (MPM Coll. No. 22289) found in intestine of “Chaenogobius annularis urotaenia Hilgendorf,” entire body, ventral view; 2, specimen (NSMT-Pl
3076) found in intestine of Cottus hangiongensis, entire body, ventral view; 3, specimen (NSMT-Pl 1850)
found in intestine of Co. nozawae, muscular papillae of oral sucker, dorsal view; 4, specimen (NSMT-Pl
3076), terminal genitalia, ventral view; 5, specimen (NSMT-Pl 3078) found in intestine of Co. hangiongensis,
ovarian complex, dorsal view. Scale bras: 0.5 mm in Figs. 1–2; 0.2 mm in Figs. 3–5.

Stevenson, 2002 (Gobiidae) (Shimazu, 1990; thispaper).
Sites of infection. Intestine and pyloric ceca.
Geographical distribution. Hokkaido: Sapporo (type locality) (Yamaguti and Matumura,1942); Ashibetsu River in Tsurui Village(Shimazu, 1981); Oono River at Chiyoda,
Hokuto City (Shimazu, 1990; this paper); andTobetsu River at Tobetsu, Hokuto City (Shimazu,

1990; this paper).
In Russian Far East: Sakhalin Island (Shedko,
2003; Sokolov et al., 2012).
Material examined. (1) 2 specimens (Yamagutiʼs Collection, MPM Coll. No. 22289, holotype and 1 paratype) of Crepidostomum chaenogobii, adult, ex intestine of “Chaenogobius
annularis urotaenia Hilgendorf” (Chaenogobius
urotaenia of Shimazu (1990), Chaenogobius

Digeneans Parasitic in Freshwater Fishes of Japanurotaenia? of Shimazu (1994)), Sapporo (otherdata not given) (Yamaguti and Matumura, 1942;
Shimazu, 1990, 1994). (2) 8 (NSMT-Pl 3073–
3074) of C. chaenogobii, immature, adult, ex
intestine of Cottus amblystomopsis, Oono Rivernear Hakodate, or at Chiyoda, Hokuto City, 20
August 1984 (Shimazu, 1990, 1994). (3) 79(NSMT-Pl 3076–3085) of C. chaenogobii, adult,
ex intestine and pyloric ceca of Co. hangiongensis, Tobestu River, Kamiiso, or at Tobetsu,
Hokuto City, 26 August 1984 (Shimazu, 1990,
1994). (Eleven adult specimens (NSMT-Pl 3075,
ex intestine and pyloric ceca of Co. amblystomopsis, Tobetsu River, 26 August 1984) of
Shimazu (1990) were not reexamined. Probably,
they had been lost on loan.) (4) 79 (NSMT-Pl
1846–1852) of C. chaenogobii, immature, adult,
ex intestine of Co. nozawae, Ashibetsu Rivernear Kushiro, or in Tsurui Village, 10 May 1977
(Shimazu, 1981, 1990, 1994). (5) 1 (NSMT-Pl
3072) of C. chaenogobii, adult, ex intestine of
Gymnogobius opperiens (Chaenogobius urotaenia (＝Chaenogobius annularis, the middlereaches type) of Shimazu (1990)), Tobetsu River,
26 August 1984 (Shimazu, 1990, 1994).
Description. 1) For the original description
for Creptostomum chaenogobii, see Yamaguti
and Matumura (1942). Holotype 1.59 by 0.32
(Fig. 1).
2) Based on specimens (NSMT-Pl 3072–
3085), after Shimazu (1990), modiﬁed from thepresent study (Figs. 2–5). Body elongate-ovate,
more tapering posteriorly, small, 0.94–1.70 by
0.30–0.52; forebody 0.30–0.52 long, occupying
29–32% of body length. Tegument smooth. Eyespot pigment not seen even in small immature
specimens. Small gland cells present in forebody.
Oral sucker globular, 0.13–0.20 by 0.14–0.21,
ventrally subterminal, with one pair each of ventrolateral, dorsolateral, and dorsomedial muscularpapillae; ventrolateral papillae conical, small, 25
by 55 μm in Fig. 3; dorsolateral and ventromedial
papillae bluntly rounded, equal in size, large,
79 μm in diameter in Fig. 3. Prepharynx short.
Pharynx globular, 0.05–0.07 in diameter; ratio oforal sucker width to pharynx width [not pharynx

109

width to oral sucker width in Shimazu (1981,1990)] 1 : 0.3–0.5. Esophagus fairly long, 0.08–
0.16 long, surrounded by small gland cells, bifurcating anterior to ventral sucker. Intestines (orceca) terminating blindly at about midlevel ofpost-testicular region. Ventral sucker subglobular, usually smaller than oral sucker, 0.12–0.17
by 0.14–0.20, situated at about junction of anterior and middle thirds of body; sucker width ratio
1 : 0.8–1.2. Testes two, spherical, large, anterior
one always smaller than posterior one, 0.13–0.30
in diameter, median, tandem, in middle third of
hindbody, slightly separated by vitelline follicles[not contiguous]. Cirrus pouch (or cirrus-sac)club-shaped, thickened posteriorly, thick-walled,
muscular, long, 0.30–0.55 by 0.16–0.19, extending usually to ovarian level but sometimes toanterior testis, including seminal vesicle, prostatic complex, and ejaculatory duct (or cirrus).
Seminal vesicle tubular, thick-walled, muscular,
short, straight (Figs. 1, 2, and 4) to S-shaped(Shimazu, 1981, ﬁg. 19), occupying posterior
third to half of cirrus pouch. Pars prostatica elliptical, 0.05–0.09 by 0.03–0.05; prostatic cells welldeveloped. Ejaculatory duct straight or slightly
undulating, thick-walled, 0.16–0.28 by 0.02, surrounded by small gland cells, sometimes slightly
everted. Genital atrium small, cup-shaped. Genital pore median, bifurcal or slightly anterior to it.
Ovary globular to elliptical, smaller than testes,
0.09–0.17 in diameter, between ventral sucker
and anterior testis, dextrally or sinistrally submedian or almost lateral. Ovarian complex postovarian. Seminal receptacle canalicular, clubshaped, 0.04–0.10 by 0.04–0.07. Laurerʼs canalfairly long. Ootype vesicular, large; Mehlisʼ
gland well developed. Uterus coiled a few times,
usually pretesticular, rarely extending slightly
into testicular region; metraterm well developed,
very thick-walled, much shorter than cirrus
pouch, 0.05–0.16 long. Eggs fewer than 20,
broad-ovate, operculate, light brown, 60–72 by
40–48 μm, unembryonated; eggshells smooth.
Vitellaria follicular; follicles large, slightly entering prebifurcal region, extending to posterior
extremity of body, separate anteriorly, conﬂuent

110

Takeshi Shimazu

between two testes and in post-testicular region,
sometimes interrupted laterally to ventral sucker,
ovary, and testes. Excretory vesicle I-shaped,
extending anteriorly to seminal receptacle
beyond anterior testis; excretory pore posteroterminal or -dorsal.
Remarks. Yamaguti and Matumura (1942)
fully described and ﬁgured Crepidostomum
chaenogobii as a new species on the basis of theholotype and paratype. The type host “Chaenogobius annularis urotaenia Hilgendorf” is currently assigned to Gymnogobius. However, its
current scientiﬁc name is unknown, because they
identiﬁed the type host ﬁsh from the then classiﬁcation of Chaenogobius. The present specimens
agree well with the type specimens in morphology
and measurements.
Life cycle. Not known in Japan.
Crepidostomum farionis (Müller, 1780)(Figs. 6–11)
Fasciola farionis Müller, 1780: 4, pl. 72.
Crepidostomum farionis: Lühe, 1909: 63, ﬁg. 54;
Shimazu, 1990, in part: 4, ﬁgs. 5–8.
Crepidostomum uchimii Fujita, 1920: 105–107, pl. 2, ﬁgs.
1–5.
Crepidostomum uchimii Fujita, 1920, sp. inq.: Shimazu,
1990: 10, ﬁg. 21.
For other synonyms, see Hopkins (1934) and Caira(1989).

Hosts in Japan. Oncorhynchus masou masou(Brevoort, 1856) (Salmonidae) (Fujita, 1920;
Shimazu, 1990; this paper), Oncorhynchus
mykiss (Walbaum, 1792) (Seki, 1975a, b;
Shimazu, 1981, 1990; this paper), Salvelinus
fontinalis (Mitchill, 1814) (Salmonidae) (thispaper), Salvelinus leucomaenis leucomaenis(Pallas, 1814) (Seki, 1975a, b; this paper), andSalvelinus malma malma (Walbaum, 1792)(Shimazu, 1981, 1990; this paper).
Sites of infection. Intestine and pyloric ceca,
and also rectum (accidental (?)) and gall bladder(normal (?)).
Geographical distribution. Hokkaido: Lake
Panketo at Akan-cho, Kushiro City (Seki, 1975a,b; Shimazu, 1981, 1990, 1994; this paper); Lake
Shikaribetsu at Shikaoi Town (Seki, 1975a, b;
Shimazu, 1981, 1990, 1994; this paper); Mamachi River at Aoba, Chitose City (this paper);Nishibestu River at Nijibetsu, Shibecha Town
(this paper); Nishibetsu River in Shibecha Town
(Fujita, 1920; this paper); Nobusha and Shokanbetsu rivers in Mashike Town (Shimazu, 1990,
1994); Onishibetsu River in Sarufutsu Village(Shimazu, 1990, 1994); and Tawaramappu Riverin Nakashibetsu Town (this paper).
In the Holarctic region (e.g., Caira, 1989).
Material examined. (1) 3 specimens (FujitaʼsCollection, III-10, HUNHM 48659, labeled“Crepidostomum uchimii Fujita [Host: Oncorhynchus masou] [Intestine] [Nijibestu River] [Hokkaido][September 1918],” syntypes) of C. uchimii,
adult, 2 balsam-mounted, 1 in glycerin-alcohol,
ex intestine of O. masou masou (syn. O. masou),Nijibetsu River, Kushiro, or now Nishibestu
River in Shibecha Town, eastern Hokkaido, September, 1918 (Fujita, 1920). (2) 11 (NSMT-Pl
3086) of C. farionis, adult, ex intestine of O.
masou masou, Onishibetsu River, 15 July 1984
(Shimazu, 1990). (3) 2 (NSMT-Pl 3087–3088) of
C. farionis, immature, adult, ex intestine andrectum (accidental (?)) of O. masou masou, Shokanbetsu River, 1 August 1984 (Shimazu, 1990).
(4) 2 (NSMT-Pl 3089–3090) of C. farionis,
immature, adult, ex intestine of O. masou masou,
Nobusha River, 2 August 1984 (Shimazu, 1990).
(Seven adult specimens (NSMT-Pl 3091) of
Shimazu (1990) were not reexamined. Probably,
they had been lost on loan.) (5) 13 (NSMT-Pl
5822–5823), adult, ex intestine of O. masou
masou, Mamachi River, 18 April 2011, 9 August
2011. (6) 1 (NSMT-Pl 5824), adult, ex gall bladder of O. masou masou, Mamachi River, 9August 2011. (7) 1 (HUNHM 61343), adult, ex
intestine of O. masou masou, Tawaramappu
River, 1 August 2011. (8) 1 (NSMT-Pl 5803),
adult, ex intestine of O. mykiss, Nishibetsu Riverat Nijibetsu, 18 April 2011. (9) 3 (NSMT-Pl
5799, HUNHM 61342), immature, adult, ex
intestine of Salvelinus fontinalis (formalin-ﬁxed
and fresh), Nishibetsu River at Nijibetsu, 2Digeneans Parasitic in Freshwater Fishes of Japan111

Figs. 6–11. Crepidostomum farionis, adult specimens. — 6, specimen (NSMT-Pl 5799) found in intestine ofSalvelinus fontinalis, entire body, ventral view; 7, specimen (NSMT-Pl 5803) found in intestine of Oncorhynchus mykiss, muscular papillae of oral sucker, dorsal view; 8, specimen (NSMT-Pl 5822) found in intestine of
O. masou masou, terminal genitalia, ventral view; 9, specimen (NSMT-Pl 5799), ovarian complex, dorsal
view; 10, egg with warty eggshell; 11, syntype of C. uchimii (HUNHM 48659) found in intestine of O. masou
masou, entire body, ventral view. Scale bars: 0.5 mm in Figs. 6 and 11; 0.2 mm in Figs. 7–9; 0.05 mm in Fig. 10.

October 1986, 18 April 2011. (10) 1 (NSMT-Pl
5798), adult, ex intestine of S. leucomaenis
leucomaenis (formalin-ﬁxed), Nishibetsu Riverat Nijibetsu, 2 October 1986. (11) 2 (NSMT-Pl
5806), adult, ex intestine of S. malma malma,
Tawaramappu River, 1 August 2011.
Description. 1) Based on slightly ﬂattened
adult specimens (NSMT-Pl 3086, 3087, 3090–

3091, 5803, 5806, 5822–5823; HUNHM 61342–
61343) (Figs. 6–10). Body elongate-ovate, widest at level of ventral sucker, fairly small,
1.90–5.36 by 0.57–1.20; forebody 0.52–1.43
long, occupying 24–33% of body length. Eyespot
pigment usually dispersed but rarely solid inforebody. Oral sucker small, 0.19–0.32 by 0.21–
0.35; ventrolateral papillae ear-shaped, fairly

112

Takeshi Shimazu

large, 32–35 by 48–50 μm in Fig. 7; dorsolateralpapillae horn-shaped, small, 31–33 by 17–22 μm
in Fig. 7; dorsomedial papillae narrow elliptical,
small, 13–16 by 40 μm in Fig. 7. Pharynx large,
0.12–0.23 by 0.13–0.23; ratio of oral sucker
width to pharynx width 1 : 0.5–0.8. Esophagus
bifurcating dorsally to anterior border of ventral
sucker or slightly anteriorly to it. Intestines terminating at about midlevel of post-testicularregion. Ventral sucker 0.25–0.47 by 0.28–0.46;
sucker width ratio 1 : 1.2–1.5. Testes globular,
0.23–0.63 by 0.19–0.44, oblique or tandem, in
middle third of hindbody, contiguous or slightly
separated by vitelline follicles. Cirrus pouch clavate, thin-walled, long, 0.25–0.90 by 0.09–0.23,
lateral to ventral sucker, sometimes extending
posteriorly slightly beyond ventral sucker. Seminal vesicle long, thin-walled, thick and convoluted in proximal two-thirds, thin and slender indistal third (Figs. 6 and 8), occupying posterior
two-thirds of cirrus pouch. Pars prostatica elliptical to elongate, 0.03–0.12 by 0.03–0.04; prostatic
cells well developed. Ejaculatory duct straight orslightly undulating, short, 0.11–0.23 by 0.02,
occupying anterior third of cirrus pouch, sometimes slightly everted. Genital atrium large, shallow. Genital pore ventral to pharynx or slightly
posterior to it. Ovary almost globular, smaller
than testes, 0.21–0.39 by 0.19–0.41, dextrally orsinistrally submedian or sometimes median.
Seminal receptacle club-shaped, 0.12–0.32 by
0.06–0.14, between ovary and anterior testis.
Laurerʼs canal short, sometimes making proximal
dilatation to store sperm in it. Ootype large;
Mehlisʼ gland well developed. Uterus coiled
between anterior testis and ventral sucker,
between intestines, slightly overlapping them,rarely extending slightly into testicular region;
metraterm much shorter than [not almost as longas in Shimazu (1990)] cirrus pouch. Eggs numerous, broad-ovate, brown, 59–79 by 32–49 μm[70–82 by 42–50 μm in Shimazu (1990)]; eggshells warty (Fig. 10) or smooth. Vitelline follicles distributed from oral sucker to posterior
extremity of body, separate anteriorly, conﬂuent
in post-testicular region. Excretory vesicle

extending anteriorly slightly beyond anterior testis; excretory pore postero-terminal or -dorsal.
2) Based on 3 adult syntypes of C. uchimii(HUNHM 48659, 1 lacking posterior part ofbody) (Fig. 11). Body much contracted, 0.79–(about 1.10) by 0.44–0.54. Eyespot pigment notseen. Oral sucker 0.13–0.15 by 0.17–0.21; ventrolateral papillae bending internally, 20–25 by
28–39 μm; dorsolateral papillae horn-shaped,
24–27 by 9–19 μm; dorsomedial papillae narrow
elliptical, 9–14 by 25–37 μm. Pharynx large,
0.09–0.12 by 0.08–0.13; ratio of oral sucker
width to pharynx width 1 : 0.5–0.6. Esophagus
bifurcating dorsally to ventral sucker. Intestines
terminating at about midlevel of post-testicularregion. Ventral sucker 0.16–0.26 by 0.20–0.30;
sucker width ratio 1 : 1.2–1.4. Testes 0.10–0.17
by 0.12–0.22. Cirrus pouch 0.22–0.34 by 0.07,
dorsal to ventral sucker. Seminal vesicle loopingin proximal two-thirds, slender in distal third,
occupying posterior two-thirds of cirrus pouch.
Pars prostatica elliptical, in anterior third of cirrus pouch. Ejaculatory duct short, occupying
anterior third of cirrus pouch. Genital pore atposterior half of pharynx. Ovary 0.12 by 0.11,
dextrally submedian. Ovarian complex not
clearly observed. Uterus extending to dorsal sideof anterior testis. Eggs rather numerous, 51–64
by 35–46 μm (collapsed); eggshells warty orsmooth. Vitelline follicles distributed between
oral sucker and posterior extremity of body.
Excretory vesicle not clearly observed.
Remarks. The present specimens, except for
Fujitaʼs three specimens, closely resemble Crepidostomum farionis as described by Brown(1927), Hopkins (1934), Ślusarski (1958), andCaira (1989). Furthermore, they agreed well inmorphology with the following whole-mounted
adult specimens of C. farionis borrowed from theInstitute of Parasitology, Czech Republic: 3 (No.
Coll. D-42/3 and D-43/3), ex intestine of Thymallus thymallus (Salmonidae), Kamenice River,
13 and 15 November 1978; and 4 (No. Coll.
D-43/1), ex intestine of Salmo trutta fario,Černovický Brook (Elve River basin), 7 September 1977, 10 October 1977; Osoblaha River

Digeneans Parasitic in Freshwater Fishes of Japan(Oder River basin), 13 May 1961; and Bystřice
River (Danube River basin), 6 June 1989, allfrom former Czechoslovakia. Consequently, I
identify the present specimens as C. farionis.
Crepidostomum farionis differs from C. chaenogobii (see above) mainly in that the oral sucker issmaller, instead of usually larger, than the ventral
sucker; the ventrolateral papillae of the oral
sucker are ear-shaped instead of conical; the dorsolateral papillae are horn-shaped and small insteadof bluntly rounded and large; the dorsomedial
papillae are narrow elliptical and small instead ofbluntly rounded and large; the ratio of the oral
sucker width to the pharynx width is higher,
1 : 0.5–0.8 instead of 1 : 0.3–0.5; the seminal vesicle is long and convoluted instead of short andstraight; the genital pore opens ventral to thepharynx or slightly posterior to it instead of at
the intestinal bifurcation or slightly anterior to it;
and eggshells are sometimes warty instead ofsmooth.
Fujita (1920) described a new species, Crepidostomum uchimii, on the basis of wholemounted and serially sectioned adult specimens,
which had been found in the intestine of
Oncorhynchus masou masou (syn. O. masou)collected in the “Nijibetsu River” [probably the
Nishibetsu River of today] in Kushiro [Kushiro
no Kuni, now Shibecha Town, eastern Hokkaido]. Fujitaʼs Collection included three adultspecimens of C. uchimii in a vial (see Material
examined). Since he did not designate a holotype
for C. uchimii, I consider them syntypes of C.
uchimii. I made two of them into stained balsammounted preparations, but they were poorly prepared. These two whole-mounts and anotherspecimen in new glycerin-alcohol were used forthe present study.
In C. uchimii as described by Fujita, (1) the
muscular papillae of the oral sucker are diagrammatically ﬁgured (ﬁg. 1), lacking morphologicaldetails; (2) no eyespot pigment is seen; (3) theventrolateral papillae of the oral sucker are oneseventh as large as the larger diameter [width] of
the oral sucker; (4) the pharynx is small, with theratio of the oral sucker width to the pharynx

113

width of 1 : 0.4 (my calculation from the description) and 1 : 0.3 (my calculation from ﬁg. 1); but
the pharynx is large in a sagittal section (ﬁg. 2);(5) the seminal vesicle is long and convoluted,
occupying the posterior half of the cirrus pouch;and the ejaculatory duct is short, occupying theanterior half of the cirrus pouch; (6) the genital
pore is located ventral to the pharynx; (7) the egg
size is 0.08 by 0.04 mm in the description and0.08 by 0.04 by 0.03 mm in the English speciﬁc
diagnosis; and (8) the excretory vesicle extends
anteriorly to the anterior border of the anterior
testis. In the three syntypes reexamined (Fig. 11),(1) the body was contracted; (2) the ventrolateralpapillae bent internally, the dorsolateral papillae
were horn-shaped, and the dorsomedial papillae
were narrow elliptical; (3) the pharynx was large,
with the ratio of oral sucker width to pharynx
width of 1 : 0.5–0.6; the convoluted seminal vesicle occupied the posterior two-thirds of the cirrus
pouch, and the ejaculatory duct occupied theanterior one-third of the cirrus pouch; (4) the
genital pore was located ventral to the pharynx;(5) eggs were 51–64 by 35–46 μm (collapsed),and some eggshells were slightly warty; and (6)the excretory vesicle was not clearly observed.
Margolis (1982) said that C. uchimii mightwell be a synonym of C. farionis, but Shimazu(1990, 1994) preferred to retain C. uchimii as a
species inquirenda until reexamination of Fujitaʼs
original material. In the above-mentioned features,
C. uchimii closely resembles the present specimens of C. farionis. In order to obtain some new
specimens of C. uchimii, I examined formalinpreserved ﬁsh (2 individuals of O. masou masou,
3 of O. mykiss, 5 of S. leucomaenis leucomaenis,
and 6 of S. fontinalis) and fresh ﬁsh (13 of O.
masou masou, 3 of O. mykiss, 8 of S. leucomaenis
leucomaenis, and 15 of S. fontinalis) all collectedin the Nishibetsu River at Nijibetsu, Shibecha
Town, on 2 October 1986 and 18 April 2011,
respectively; and fresh ﬁsh (32 of O. masou
masou, 2 of S. leucomaenis leucomaenis, and 6
of S. malma malma collected in the Tawaramappu River (a tributary of the Shibetsu River,which is the next river on the north of the114

Takeshi Shimazu

Nishibetsu River, both ﬂowing into the OkhotskSea) in Nakashibetsu Town on 1 August 2011.
Although C. farionis was not found in O. masou
masou from the Nishibetsu River, it was found in
O. mykiss, S. leucomaenis leucomaenis, and S.
fontinalis from the Nishibetsu River and in O.
masou masou and S. malma malma from the
Tawaramappu River (see Material examined),
which indicates that C. farionis is certainly distributed in the Nishibetsu and Tawaramappu rivers in eastern Hokkaido. Furthermore, two contracted adult specimens (NSMT-Pl 5798–5799)
of C. farionis found in formalin-preserved individuals of S. leucomaenis leucomaenis and S.
fontinalis from the Nishibetsu River were very
similar to the contracted syntypes of C. uchimii
in morphology, having internally bent ventrolateral papillae. In conclusion, I now regard C.
uchimii as a junior synonym of C. farionis.
Seki (1975a, b) reported specimens of Crepidostomum from the intestine of salmonids collected in Hokkaido: (1) C. farionis (1975a, p. 10,
pl. 1, ﬁg. 2) found in S. leucomaenis leucomaenis(syn. S. leucomaenis) from Lake Panketo and O.
mykiss (syn. Salmo gairdneri irideus (Gibbons,1855)) from Lake Shikaribetsu; (2) Crepidostomum metoecus (Braun, 1900) (1975a, pp. 10–11,
pl. 1, ﬁg. 3) found in S. malma malma from Lake
Shikaribetsu; and (3) Crepidostomum sp. (1975a,
pp. 11–12, pl. 1, ﬁg. 4) found in S. malma malma
from Lake Shikaribetsu. Shimazu (1981, 1990)
reexamined part of Sekiʼs specimens, which werethen deposited in the Department of Parasitology,
Faculty of Veterinary Medicine, Hokkaido University, Sapporo. (1) Sekiʼs specimens (No. 374)
of C. farionis found in O. mykiss consisted of
specimens of C. farionis and those of C. metoecus,
including the ﬁgured one (ﬁg. 2). The uterus
occupied all the available space in the hindbody
in one of the specimens of C. farionis. (2) Sekiʼsspecimens (No. 375) of C. metoecus found in S.
malma malma consisted of specimens of C.
metoecus including the ﬁgured one (ﬁg. 3) andthose of C. farionis. (3) Sekiʼs specimen (No.
376) of Crepidotomum sp. (ﬁg. 4) found in S.
malma malma was identiﬁed as C. farionis. The

uterus descended into the testicular region in thisspecimen. It is desirable that all of Sekiʼs specimens be reexamined.
Shimazuʼs (1981, 1990) three specimens(NSMT-Pl 2174) of C. farionis found in S. leucomaenis leucomaenis from the Ashibetsu Riverand Shimazuʼs (1990) specimen (NSMT-Pl 3092)
of C. farionis found in Noemacheilus toni
(Homalopteridae) [sic] from the Shokanbestu
River are identiﬁed as C. metoecus in the present
study (see below).
Life cycle. Not known in Hokkaido.
Crepidostomum metoecus (Braun, 1900)(Figs. 12–18)
Distomum metoecus Braun, 1900a: 389.
Crepidostomum metoecus: Braun, 1900b: 230–231, ﬁg.
13; Shimazu, 1990: 6–7, ﬁgs. 10–19.
Crepidostomum salmonis Fujita, 1921b: 137–140, ﬁgs.
1–3.
Bunodera luciopercae (not of (Müller, 1776) Stiles andHassall, 1898): Shimazu, 1981: 19, 21, ﬁgs. 11–15.
Crepidostomum farionis (not of (Müller, 1780) Lühe,1909): Shimazu, 1981: 23–24, ﬁgs. 21–24; Shimazu,
1990, in part: 4, ﬁg. 9.
Crepidostomum salmonis Fujita, 1921, sp. inq.: Shimazu,
1990: 9, ﬁg. 20.
For other synonyms, see Hopkins (1934) and Caira(1989).

Hosts in Japan. Barbatula toni (Dybowski,
1869) (Nemacheilidae) (Shimazu, 1990; thispaper), Cottus nozawae (Cottidae) (Shimazu,
1981), Gasterosteus aculeatus Linnaeus, 1758
(Gasterosteidae) (Shimazu, 1990; this paper),Gymnogobius castaneus (OʼShaughnessy, 1875)(Gobiidae) (Shimazu, 1990; this paper), Gymnogobius urotaenia (Hilgendorf, 1879) (Shimazu,
1990; this paper), Oncorchynchus keta (Walbaum, 1792) (Salmonidae) (Fujita, 1916, 1921b;
Shimazu, 1990), Oncorchynchus masou masou(Kurata, 1992; this paper), Oncorchynchus
mykiss (Shimazu, 1981, 1990; Kurata, 1992; thispaper), Parahucho perryi (Brevoort, 1856) (Salmonidae) (Shimazu, 1981; this paper), Pungitius
pungitius (Linnaeus, 1758) (Gasterosteidae) (thispaper), Pungitius tymensis (Nikolskii, 1889)

Digeneans Parasitic in Freshwater Fishes of Japan115

Figs. 12–18. Crepidostomum metoecus, adult specimens. — 12, specimen (NSMT-Pl 5801) found in intestine ofSalvelinus fontinalis; entire body; 13, specimen (NSMT-Pl 5801), muscular papillae of oral sucker, dorsal
view; 14, specimen (NSMT-Pl 5801), terminal genitalia, ventral view; 15, specimen (NSMT-Pl 5826) found inintestine of Salmo trutta, ovarian complex, dorsal view; 16, specimen (NSMT-Pl 3092) found in intestine ofBarbatula toni, terminal genitalia, ventral view; 17, abnormal egg of specimen (NSMT-Pl 3092) (a), normal
egg of specimen (NSMT-Pl 5801) (b); 18, specimen of C. salmonis found in alimentary canal of Oncorhynchus keta (fry), entire body, ventral view, scale unknown, redrawn from Fujita (1921b). Scale bars: 0.5 mm inFig. 12; 0.2 mm in Figs. 13–16; 0.05 mm in Fig. 17.

(Shimazu, 1990; this paper), Salmo trutta Linnaeus, 1758 (Salmonidae) (this paper), Salvelinus fontinalis (Salmonidae) (this paper), Salvelinus leucomaenis leucomaenis (Shimazu, 1981,

1990; Kurata, 1992; this paper), and Salvelinus
malma malma (Seki, 1975a, b; Shimazu, 1990;
Kurata, 1992; this paper).
Sites of infection. Intestine and pyloric ceca,

116

Takeshi Shimazu

and also rectum (accidental (?)).
Geographical distribution. Hokkaido: Brooks
near Sapporo (Fujita, 1921b; Shimazu, 1990,
1994); Ashibetsu and Settsuri rivers in Tsurui
Village (Shimazu, 1981, 1990, 1994); Izari Riverat Eniwa City (this paper); Kushiro River (locality not speciﬁed) (Kurata, 1992; Shimazu, 1994);
Lake Panketo at Akan-cho, Kushiro City
(Shimazu, 1981, 1990; this paper); Lake Shikaribetsu at Shikaoi Town (Seki, 1975a, b; Shimazu,
1990, 1994); Lakes Shirarutoro and Toro at Toro,
Shibecha Town (Shimazu, 1990, 1994); Mamachi River at Aoba, Chitose City (this paper);Nishibestu River at Nijibetsu, Shibecha Town
(Kurata, 1992; Shimazu, 1994; this paper); ShinRiver in Hamanaka Town (Shimazu, 1990,
1994); Shokanbetsu River in Mashike Town
(Shimazu, 1990, 1994; this paper); Sorachi River(locality not speciﬁed) (Kurata, 1992; Shimazu,
1994); and Tawaramappu River in Nakashibetsu
Town (this paper).
In the Holarctic region (e.g., Caira, 1989).
Material examined. (1) 1 specimen (NSMTPl 3092) of C. farionis, adult, ex intestineof Barbatula toni (syn. Noemacheilus toni),
Shokanbetsu River, 31 July 1984 (Shimazu,
1990, 1994). (2) 4 (NSMT-Pl 5831), adult, ex
intestine of B. toni, Izari River, 1 June 2011.
(3) 34 (NSMT-Pl 5828–5830), immature, adult,
ex intestine of B. toni, Mamachi River, 18
April 2011, 20 May 2011, 9 August 2011.
(4) 36 (NSMT-Pl 1846–1849, B. luciopercae of
Shimazu (1981)) of C. metoecus, immature,adult, ex intestine of Cottus nozawae, Ashibetsu
River, 10 [not 19] May 1977 (Shimazu, 1981,
1990, 1994). (5) 1 (NSMT-Pl 3071) of C. metoecus,
adult, ex intestine of Gasterosteus aculeatus(syn. Ga. aculeatus aculeatus), Lake Shirarutoro,
19 September 1981 (Shimazu, 1990, 1994). (6)
11 (NSMT-Pl 3068) of C. metoecus, immature,adult, ex Gymnogobius castaneus (now not
Chaenogobius laevis (Steindachner, 1879)), ShinRiver, 28 May 1981 (Shimazu, 1990, 1994).
(7) 31 (NSMT-Pl 3066–3067) of C. metoecus,
immature, adult, ex intestine of G. urotaenia(Chaenogobius urotaenia (the freshwater type)of Shimazu (1990), Chaenogobius sp. 1 of Prince
Akihito), Shin River, 28 May 1981, 11 June 1981
(Shimazu, 1990, 1994). (8) 57 (NSMT-Pl 3057–3065) of C. metoecus, adult, ex intestine and rectum (accidental (?)) of G. urotaenia, Lake Toro,
28 June 1984 (Shimazu, 1990, 1994). (Thirtyone adult specimens (NSMT-Pl 3056) of
Shimazu (1990) were not reexamined. Probably,
they had been lost on loan.) (9) 6 (NSMT-Pl
3070) of C. metoecus, adult, ex intestine of
Oncorchynchus keta (smolt), Shin River, 11 June
1981 (Shimazu, 1990, 1994). (10) 13 (NSMT-Pl
5822–5823), adult, ex intestine of O. masou
masou, Mamachi River, 18 April 2011, 9 August
2011. (11) 1 (NSMT-Pl 5800), adult, ex intestineof O. masou masou, Nishibetsu River at Nijibetsu, 18 April 2011. (12) 8 (NSMT-Pl 5804),
immature, adult, ex intestine of O. masou masou,
Tawaramappu River, 1 August 2011. (13) 13(NSMT-Pl 5826), adult, ex intestine of Salmo
trutta, Mamachi River, 18 April 2011. (14) 77(NSMT-Pl 5799, 5801, HUNHM 61342), immature, adult, ex intestine of Salvelinus fontinalis(formalin-preserved and fresh), Nishibetsu Riverat Nijibetsu, 2 October 1986, 18 April 2011. (15)
3 (NSMT-Pl 2174) of C. farionis, adult, ex
pyloric ceca of S. leucomaenis leucomaenis (syn.
S. leucomaenis), Ashibetsu River, 10 May 1977
(Shimazu, 1981, 1990, 1994). (16) 34 (NSMT-Pl
2175, Bunodera luciopercae of Shimazu (1981))
of C. metoecus, immature, adult, ex intestine andpyloric ceca, S. leucomaenis leucomaenis (syn. S.
leucomaenis), Ashibetsu River, 10 May 1977
(Shimazu, 1981, 1990, 1994). (17) About 60(NSMT-Pl 3069) of C. metoecus, immature,adult, ex intestine of S. leucomaenis leucomaenis, Lake Toro, 15 May 1981 (Shimazu, 1990,
1994). (18) 1 (NSMT-Pl 5825), adult, ex intestine of S. leucomaenis leucomaenis, Mamachi
River, 18 April 2011. (19) 5 (NSMT-Pl 5798,
5802), immature, adult, ex intestine of S. leucomaenis leucomaenis (formalin-preserved andfresh), Nishibetsu River at Nijibetsu, 2 October
1986, 18 April 2011. (20) 1 (NSMT-Pl 5805),
adult, ex intestine of S. leucomaenis leucomaenis, Tawaramappu River, 1 August 2011. (21) 11

Digeneans Parasitic in Freshwater Fishes of Japan(NSMT-Pl 5806), immature, adult, ex intestine of
S. malma malma, Tawaramappu River, 1 August
2011. (22) 28 (NSMT-Pl 2176, Bunodera
luciopercae (?) of Shimazu (1981)) of C.
metoecus, immature, adult, ex intestine of
Parahucho perryi (syn. Hucho perryi) (formalinpreserved), Settsuri River, 10 April 1976
(Shimazu, 1981, 1990, 1994). (23) Kurataʼs(1992) specimens of C. metoecus, adult: 1(NSMT-Pl 3986), ex intestine of S. malma
malma, Sorachi River (locality not speciﬁed), 6
September 1992; 2 (NSMT-Pl 3987–3988), ex
intestine of S. leucomaenis leucomaenis, Nishibetsu River at Nijibetsu, 24 July 1992; and 1(NSMT-Pl 3989), ex intestine of O. masou
masou (syn. O. masou), Nishibetsu River at
Nijibetsu, 24 July 1992 (Shimazu, 1994). (24) 3(NSMT-Pl 5827), adult, ex intestine of Pungitius
pungitius, Mamachi River, 18 April 2011. (25) 3(Ozakiʼs Collection, MPM Coll. No. 30010,
labeled “Crepidostomum uchimii”) of C. metoecus,
immature, adult, ex Pungitius tymensis (syn. P.
pungitius tymensis), Hokkaido (other data notgiven) (Shimazu, 1990, 1994).
Description. 1) Based on specimens (NSMTPl 5798–5802, 5804–5806, 5822–5823, 5825–
5827), relatively large ones of them measured(Figs. 12–15). Body elongate-ovate, more tapering posteriorly, small, 1.62–3.33 by 0.52–0.92;
forebody 0.55–1.03 long, occupying 28–34% ofbody length. Eyespot pigment solid or dispersed
in forebody. Oral sucker small, 0.18–0.28 by
0.20–0.31; ventrolateral papillae ear-shaped,
fairly large, 38–55 by 40–48 μm in Fig. 13; dorsolateral papillae horn-shaped, fairly large, 37–48
by 30–32 μm in Fig. 13; dorsomedial papillae
broad elliptical, fairly large, 24 by 40–43 μm in
Fig. 13. Pharynx small, 0.08–0.13 by 0.06–0.12;
ratio of oral sucker width to pharynx width
1 : 0.3–0.4. Esophagus bifurcating anterior toventral sucker. Intestines terminating at about
middle of post-testicular region. Ventral sucker
0.25–0.43 by 0.28–0.43, located at about junction of anterior and second thirds of body; sucker
width ratio 1 : 1.3–1.4. Testes round or slightly
indented irregularly, large, 0.22–0.47 by 0.32–

117

0.54, tandem, in middle third of hindbody, contiguous. Cirrus pouch clavate, fairly thickwalled, muscular, 0.35–0.63 by 0.09–0.16,
extending posteriorly beyond ventral sucker
sometimes to ovary. Seminal vesicle short, thickened posteriorly, fairly thick-walled, muscular,
sinuous in about posterior third of cirrus pouch(Figs. 12 and 14). Pars prostatica elliptical,
small; prostatic cells well developed. Ejaculatoryduct long, undulating in anterior two-thirds to
one-half of cirrus pouch, sometimes everted.
Genital atrium large. Genital pore at intestinal
bifurcation or slightly anterior to it. Ovary triangular, elliptical, or globular, rather small, 0.20–
0.28 by 0.20–0.32, dextrally or sinistrally submedian. Seminal receptacle club-shaped, 0.19–0.32
by 0.08–0.13. Laurerʼs canal short, sometimes
dilated proximally to store sperm in it. Ootype
large; Mehlisʼ gland well developed. Uterus
coiled between anterior testis and ventral sucker,
often entering testicular or rarely post-testicularspace, between intestines, slightly overlapping
intestines; metraterm well developed, much
shorter than cirrus pouch. Eggs numerous, broadovate, thin-shelled, light brown, 56–68 by
40–48 μm; eggshells smooth. Vitelline follicles
distributed from pharyngeal level to posterior
extremity of body, close but separate anteriorly,
conﬂuent post-testicularly. Excretory vesicle
ending at middle of anterior testis; excretory pore
postero-dorsal or -terminal.
Remarks. The present specimens closely
resemble Crepidostomum metoecus as describedby Hopkins (1934), Ślusarski (1958), and Caira(1989). Furthermore, they were consistent inmorphology with the following whole-mounted
adult specimens of C. metoecus borrowed fromthe Institute of Parasitology, Czech Republic: 1(No. Coll. D-42/1, 1247-36), ex pyloric cecum of
Salmo trutta fario, Petrovický Brook, former
Czechoslovakia, 30 March 1961; 6 (No. Coll.
D-42/1, 1714a, b), ex intestine of S. trutta fario,Černovický Brook, former Czechoslovakia, 13
April 1978; and 1 (Coll. No. D-42/1), ex intestineof S. trutta fario, Velke Březno, Homolský Brook,
Czech Republic, 12 April 2000. Consequently.

118

Takeshi Shimazu

I identiﬁed them as C. metoecus.
Crepidostomum metoecus differs from C.
chaenogobii (see above) mainly in that the oral
sucker is smaller, instead of usually larger, thanthe ventral sucker; the ventrolateral papillae ofthe oral sucker are ear-shaped instead of conical;
the dorsolateral papillae are horn-shaped andsmall instead of bluntly rounded and large; thedorsomedial papillae are broad elliptical andsmall instead of bluntly rounded and large; thevitelline follicles are separate, instead of conﬂuent, between the two testes; and the excretory
vesicle extends anteriorly to the middle of theanterior testis instead of to the seminal receptacle
beyond the anterior testis. Further, C. metoecus isalso different from C. farionis (see above)
mainly in that the dorsomedial papillae of theoral sucker are broad elliptical instead of narrow
elliptical; the ratio of the oral sucker width to thepharynx width is lower, 1 : 0.3–0.4 instead of
1 : 0.5–0.8; the seminal vesicle is short and sinuous in the posterior third of the cirrus pouch
instead of long and convoluted in the posterior
two-thirds; the ejaculatory duct is long in theanterior two-thirds of the cirrus pouch instead ofshort in the anterior third; the genital pore opensat the intestinal bifurcation or slightly anterior to
it instead of ventral to the pharynx or slightly
posterior to it; eggshells are smooth instead ofsometimes warty; and the excretory vesicle
extends anteriorly to the middle of the anterior testis instead of slightly beyond the anterior testis.
Fujita (1916) found a digenean (Crepidostomum sp.), a nematode (Cucullanus sp.), and an
acanthocephalan (Acanthocephalus sp.) in thealimentary canal of fry of Oncorhynchus keta
collected in a brook about 300 m west of thecampus of the Agricultural College, Tohoku
Imperial University (currently the Faculty ofAgriculture, Hokkaido University), Sapporo, in
1913–1915. These three parasites were describedas new species: the acanthocephalan as Acanthocephalus oncorhynchi Fujita, 1921 from the“Hassabu River near Sapporo” (Fujita, 1921a),the digenean as Crepidostomum salmonis Fujita,
1921 from “brooks near Sapporo” (Fujita,

1921b), and the nematode as Cystidicola
oncorhynchi Fujita, 1921 from “brooks in Sapporo” (Fujita, 1921c). Therefore, the name of thebrook is uncertain.
Crepidostomum salmonis was described by
Fujita (1921b) on the basis of four wholemounted and sectioned adult specimens, but
none of them are deposited in Fujitaʼs Collection
today (see also Shimazu, 1990). According to his
description and ﬁgures of C. salmonis (thispaper, Fig. 18), (1) the oral sucker has six muscular papillae, though they are diagrammaticallydrawn and lack morphological details; (2) aneyespot is present on either side of the pharynx;(3) the ventral sucker is larger than the oral
sucker, with the width ratio of 1 : 1.4 (my calculation); (4) the pharynx is small, with the ratio of
the oral sucker width to the pharynx width of
1 : 0.3 (my calculation); (5) the testes are slightly
larger than the ventral sucker and ovary [butsmaller in ﬁg. 1]; (6) the cirrus pouch extends
posteriorly to the posterior border of the ventral
sucker; (7) the seminal vesicle is long and convoluted in the posterior half of the cirrus pouch; (8)the ejaculatory duct is long in the anterior half ofthe cirrus pouch; (9) the genital pore opens at theintestinal bifurcation (ﬁg. 1); (10) the uterus
extends posteriorly to the posterior border of theanterior testis; (11) eggs are elliptical and 0.08 by
0.07 mm; and (12) the excretory vesicle reaches
to the middle of the anterior testis. Margolis(1982) said that C. salmonis might well be a synonym of C. metoecus. Shimazu (1990) preferred
to retain C. salmonis as a species inquirenda
until reexamination of Fujitaʼs original specimens.
Since they were lost, it is now impossible toreexamine them. Crepidostomum salmonis is very
similar to the present specimens of C. metoecus
especially in the size of the pharynx, size of theseminal vesicle, size of the ejaculatory duct,
position of the genital pore, and anterior extent
of the excretory vesicle. The egg size (0.08 by
0.07 mm) given is probably erroneous. Although
I found no specimen of Crepidostomum in 18
smolts of O. keta and 5 individuals of O. masou
masou collected in the Kotonihassamu River onDigeneans Parasitic in Freshwater Fishes of Japan

7 April 2011 (my unpublished data), the present
specimens of C. metoecus were obtained from avariety of freshwater ﬁshes in a wide range in
Hokkaido and include those (NSMT-Pl 3070)
found in smolts of O. keta from the Shin River inHamanaka Town. Consequently, I now consider
C. salmonis a junior synonym of C. metoecus.
Shimazu (1990, ﬁg. 9) identiﬁed an adult specimen (NSMT-Pl 3092) found in Barbatula toni(syn. Noemacheilus toni) from the Shokanbetsu
River as C. farionis. Further, he regarded it as
Crepidostomum nemachilus Krotov, 1959, which
was originally described from Nemachilus barbatulus toni on Sakhalin Island, Russian Far East
(Krotov, 1959). However, my present reexamination of the specimen shows that the pharynx was
small, 0.14 [not 0.16] mm in diameter, with theratio of the oral sucker width to the pharynx
width of 1 : 0.4; the seminal vesicle was short[not long] and S-shaped in the posterior third[not two-thirds] of the cirrus pouch; and the ejaculatory duct was long [not short] in the anterior
two-thirds [not third] of the cirrus pouch (Fig.
16); and eggs were broad-elliptical, 52–57 by
46–48 μm (Fig. 17a). The specimen is consistent
with the present specimens of C. metoecus
including new ones found in B. toni (see Material examined) in every essential feature, except
for that the eggs were broad-elliptical, 52–57 by
46–48 μm (Fig. 17a) instead of elliptical to ovate,
59–70 by 40–48 μm (Fig. 17b). Evidently,
Shimazu (1990) misidentiﬁed the specimen as C.
farionis owing to his misinterpretation of theseminal vesicle and ejaculatory duct, or the position of the pars prostatica, in it. It has smaller
abnormal eggs unlike the other specimens foundin B. toni as mentioned above.
Seki (1975a, b) reported C. metoecus and C.
farionis from salmonids caught in Hokkaido, as
mentioned in Remarks in C. farionis. Kurata(1992) also found C. metoecus in O. masou masou,
O. mykiss, and S. leucomaenis leucomaenis fromthe Nishibetsu River at Nijibetsu; S. leucomaenis
leucomaenis from the Kushiro River (locality not
speciﬁed); and S. malma malma from the Sorachi
River (locality not speciﬁed) (see also Material

examined).
Life cycle.

119

Not known in Japan.

Discussion on Crepidostomum
The present study shows that, in Japan, the following three species of Crepidostomum are
distributed in Hokkaido only: C. chaenogobii,
C. farionis, and C. metoecus. Crepidostomum
chaenogobii occurs in Hokkaido and Sakhalin
Island, Russian Far East. Crepidostomum farionis
and C. metoecus occur widely in the Holarctic
region including Hokkaido. These three species
are easily distinguished from one another inmorphology (see above and below). Atopkin and
Shedko (2010, 2014) demonstrated that thegroup (C. farionis) and the group (C. metoecus＋
C. nemachilus) in the Russian Far East also
differed from each other in partial 28S ribosomal
DNA sequences. However, they neither sequenced
any specimens of C. chaenogobii from Sakhalin
Island nor used any molecular data on C. farionis
and C. metoecus from Europe or North America.
The life cycle has not yet been studied for anyof the three species in Japan. In C. farionis andC. metoecus, ﬁrst intermediate hosts are small
bivalves of Sphaerium and Pisidium (Sphaeriidae), in which ophthalmoxiphidiocercariae areproduced in daughter rediae; second intermediate
hosts are aquatic arthropods (amphipods andephemerids), in which metacercariae encyst; andﬁnal hosts are freshwater ﬁshes, in the intestineof which adults live (e.g., Brown, 1927; Crawford, 1943; Stenko, 1982; Moravec, 1982; Margolis and Moravec, 1982; Caira, 1989; Sokolov
and Gordeev, 2014). Transmission from smallﬁsh to large ﬁsh-eating ﬁsh also occurs(Moravec, 1982). Awachie (1968) recorded cercariae of C. metoecus from the pulmonate snail
Lymnaea peregra, but this species identiﬁcationof the cercaria is doubtful (Moravec, 1982). On
Sakhalin Island, C. chaenogobii uses a bivalve,possibly Henslowiana sp. (Euglesidae), as a ﬁrst
intermediate host; Gammarus koreanus (Amphipoda) as a second intermediate host; and Pungitius
pungitius tymensis as a ﬁnal host (Shedko, 2003).

120

Takeshi Shimazu

Perhaps, neither the cercaria nor the metacercaria
nor the adult has yet been described.
Crepidostomum metoecus was ﬁrst describedby Braun (1900a) as a new species, Distomum
metoecus, on the basis of adult specimens foundin bats of two species (type hosts) (see Hopkins,
1934; Caira, 1989). Soon after that Braun(1900b) created a new genus, Crepidostomum,
with D. metoecus, or now C. metoecus (Braun,
1900), as the type species. Subsequent records of
C. metoecus have been appeared from ﬁshes only
but not from bats. Most probably, ﬁshes are the“natural hosts” of C. metoecus and bats are only
“occasional” or “accidental” hosts (Hopkins,1934). The bats may merely have eaten second
intermediate hosts that harbored oviferous proge-

netic metacercariae (Hopkins, 1934). However,no progenetic metacercariae of C. metoecus havebeen reported. Adults of the present three speciesof Crepidostomum are found usually in the intestine and pyloric ceca of ﬁshes but sometimes in
the rectum and gall bladder (Faust, 1918; Brown,
1927; Hopkins, 1934; this paper). Since worms
grow into fully gravid adults in the gall bladder,
the gall bladder may also be a normal site of
infection. Gibson and Valtonen (1988) referred toprevious records of worms from the gall bladder.
According to them, most of the ovigerous adultsof their new species Credidostomum wikgreni
occurred in the gall bladder of Coregonus acronius (Salmonidae) from Lake Yli-Kitka in northeastern Finland.

Key to the three species of Crepidostomum in Japan
1.1. Oral sucker usually larger than ventral sucker; ventrolateral papillae of oral sucker conical, small;dorsolateral and ventromedial papillae bluntly rounded, large ................................. C. chaenogobii
1.2. Oral sucker smaller than ventral sucker; ventrolateral papillae ear-shaped, fairly large; dorsolateral papillae horn-shaped fairly large or small .............................................................................2
2.1. Dorsomedial papillae narrow elliptical; pharynx large, with ratio of oral sucker width to pharynx
width of 1 : 0.5–0.8; seminal vesicle long, convoluted, in posterior two-thirds to half of cirrus pouch;ejaculatory duct short, in anterior third to half of cirrus pouch; genital pore ventral to pharynx orslightly posterior to it; excretory vesicle extending slightly beyond anterior testis ............ C. farionis
2.2. Dorsomedial papillae broad elliptical, large; pharynx small, with ratio of 1 : 0.3–0.4; seminal vesicle
short, sinuous, in posterior third to half of cirrus pouch; ejaculatory duct long, in anterior twothirds to half of cirrus pouch; genital pore at intestinal bifurcation or slightly anterior to it; excretory vesicle extending to middle of anterior testis ......................................................... C. metoecus

Acknowledgments
I am grateful to Dr. Shigehiko Urawa and Dr.
Koh Hasegawa (Hokkaido National Fisheries
Research Institute, Sapporo) for collecting someof the ﬁsh examined and laboratory facilities, Mr.
Fumihito Takaya (Botanic Garden, Field Science
Center for Northern Biosphere, Hokkaido University, Sapporo) for the loan of the specimens of
C. uchimii, Dr. František Moravec (Institute ofParasitology, Biology Centre of the Czech Academy of Sciences, Branišovská, České Budějovice,
Czech Republic) for the loan of the specimens of

C. farionis and C. metoecus, and Dr. Thomas H.
Cribb (School of Biological Sciences, The University of Queensland, Brisbane, Australia) for
reviewing a draft of the manuscript.
References
Atopkin, D. M. and M. B. Shedko 2010. Phylogenetic
relationships of trematodes of the genus Crepidostomum(Trematoda: Allocreadiidae) from the south of Russian
Far East. Parasites of the Holarctic Region. Proceedings of the International Symposium (October 4–8,
2010, Petrozavodsk, Karelia, Russia), pp. 20–23. (InRussian with English abstract.)Digeneans Parasitic in Freshwater Fishes of Japan
Atopkin, D. M. and M. B. Shedko 2014. Genetic characterization of far eastern species of the genus Crepidostomum (Trematoda: Allocreadiidae) by means of 28S
ribosomal DNA sequences. Advances in Bioscienceand Biotechnology, 5: 209–215.
Awachie, J. B. E. 1968. On the bionomics of Crepidostomum metoecus (Braun, 1900) and Crepidostomum
farionis (Müller, 1784) (Trematoda: Allocreadiidae).
Parasitology, 55: 307–324.
Braun, M. 1900a. Einige Bemerkungen über die Fascioliden der Chiroptera. Zoologischer Anzeiger, 23: 387–
391.
Braun, M. 1900b. Trematoden der Chiroptera. Annalen
des Kaiserlichen Königlichen Naturhistorischen Hofmuseums, Wien, 15: 217–236, pl. 10, ﬁgs. 1–13.
Brown, F. J. 1927. On Crepidostomum farionis O. F.
Müll. (＝Stephanophiala laureata Zeder), a distome
parasite of the trout and grayling. I. The life history.
Parasitology, 19: 86–99.
Caira, J. N. 1989. A revision of the North American papillose Allocreadiidae (Digenea) with independent cladistic analyses of larval and adult forms. Bulletin of the
University of Nebraska State Museum, 11: 1–58, ﬁgs.
1–195.
Caira, J. N. and T. Bogéa 2005. Family Allocreadiidae
Looss, 1902. In Jones, A., R. A. Bray and D. I. Gibson(eds.): Keys to the Trematoda, 2, pp. 417–436. CAB
International and The Natural History Museum, Wallingford.
Crawford, W. W. 1943. Colorado trematode studies. I. A
further contribution to the life history of Crepidostomum
farionis (Müller). Journal of Parasitology, 29: 379–384.
Cribb, T. H. 2005. Superfamily Allocreadioidea Looss,
1902. In Jones, A., R. A. Bray and D. I. Gibson (eds.):
Keys to the Trematoda, 2, pp. 413–416. CAB International and The Natural History Museum, Wallingford.
Faust, E. C. 1918. Studies on American Stephanophialine.
Transactions of the American Microscopical Society,37: 183–198.
Fujita, T. 1916. [Helminths parasitic in the fry of
Oncorhynchus keta.] Dobutsugaku Zasshi, 28: 175–
177. (In Japanese.)
Fujita, T. 1920. [On a species of trematode of Crepidostomum parasitic in Oncorhynchus masou from Hokkaido.] Dobutsugaku Zasshi, 32: 105–108, pl. 2, ﬁgs.
1–5. (In Japanese with the speciﬁc diagnosis in English.)Fujita, T. 1921a. On the parasites of Japanese ﬁshes II.
Dobutsugaku Zasshi, 33: 1–8. (In Japanese with English speciﬁc diagnoses.)
Fujita, T. 1921b. On the parasites of Japanese ﬁshes. III.
Dobutsugaku Zasshi, 33: 137–141. (In Japanese withEnglish speciﬁc diagnosis.)
Fujita, T. 1921c. On the parasites of Japanese ﬁshes, IV.
Dobutsugaku Zasshi, 33: 292–300. (In Japanese with

121

English speciﬁc diagnoses.)
Gibson, D. I. and E. T. Valtonen 1988. A new species ofCrepidostomum (Allocreadiidae: Digenea) from northeastern Finland, with comments on its possible origin.
Systematic Parasitology, 12: 31–40.
Hopkins, S. H. 1934. The papillose Allocreadiidae. A
study of their morphology, life histories, and relationships. Illinois Biological Monographs, 13: 1–80.
Krotov, A. I. 1959. [Two new parasitic worms from vertebrates of Sakhakin Island.] Acta Veterinaria Hungarica,
9: 7–12. (In Russian.)
Kurata, T. 1992. [Parasites found in ﬁshes of the family
Salmonidae caught in rivers of Hokkaido.] Unpublished graduation thesis, 37 pp. Department of Veterinary Medicine, Rakuno Gakuen University, Ebetsu,
Hokkaido. (In Japanese.)
Lühe, M. 1909. Parasitische Plattwürmer. I: Trematodes.
Süsswasserfauna Deutschlands, 17: 1–217.
Margolis, L. 1982. Parasitology of Paciﬁc salmon — an
overview. In Meerovitch, E. (ed.): Aspects of Parasitology — a Festschrift Dedicated to the Fiftieth Anniversary of the Institute of Parasitology of McGill University, 1932–1982, pp. 135–226. McGill University,
Montreal.
Margolis, L. and F. Moravec 1982. Pamellogammarus
vancouverensis (Bousﬁeld) (Amphipoda) as an intermediate host for salmonid parasites in British Columbia. Canadian Journal of Zoology, 60: 1100–1104.
Moravec, F. 1982. A contribution to the bionomics ofCrepidostomum metoecus (Trematoda: Allocreadiidae).
Věstnik Československé Společnosti Zoologické, 46:
15–24.
Müller, O. F. 1780. Zoologiae Danicae seu animalium
Daniae et Norvegiae rariorum ac minus notorum
icones. Fascicle 2, pp. [3]–4, pls. 41–80. Havniae.
Cited by Index-Catalogue of Medical and Veterinary
Zoology, 1948, Part 10, Authors: M to Mysh, p. 3456;
1965, Subjects: Trematoda and Trematode diseases.
Part 4: Supergenera and genera E–G, p. 677.
Seki, N. 1975a. Studies on Helminth Parasites of Salmonoid Fishes in Hokkaido. 42 pp., pls. 1–8, ﬁgs. 1–47.
Unpublished Thesis for Masterʼs Degree submitted to
the Division of Morphology and Functional Medicine,
Post-Graduate School of Veterinary Medicine, Hokkaido University, Sapporo.
Seki, N. 1975b. [Parasitic helminths of salmonoid ﬁshesin Hokkaido, with special reference to the plerocercoidof Diphyllobothrium latum.] Hokkaido Juishikai
Zasshi, 19: 119–123. (In Japanese.)
Shedko, M. B. 2003. [On the biology and distribution ofCrepidostomum chaenogobii (Digenea: Allocreadiidae).] In Izvekova, G. I. (ed.): [Fish Parasites: Contemporary Aspects of the Study: Conference dedicatedto the Memory of Doctor of Biological Sciences,
Professor B. I. Kuperman (1933–2002).] pp. 58–59.

122

Takeshi Shimazu

Borok. (In Russian.)
Shimazu, T. 1981. Some digenetic trematodes of freshwater ﬁshes from eastern Hokkaido, Japan. Journal of
Nagano-ken Junior College, (36): 13–26.
Shimazu, T. 1990. Trematodes of the genus Crepidostomum (Digenea: Allocreadiidae: Crepidostominae) from
freshwater ﬁshes of Japan. Journal of Nagano Prefectural College, (45): 1–14.
Shimazu, T. 1994. Adult digenetic trematodes parasitic infreshwater ﬁshes of Hokkaido, Japan: a review. Scientiﬁc Reports of Hokkaido Fish Hatchery, (48): 69–78.
Shimazu, T. 2013. Digeneans parasitic in freshwaterﬁshes (Osteichthyes) of Japan. I. Aporocotylidae, Bivesiculidae and Haploporidae. Bulletin of the National
Museum of Nature and Science, Series A (Zoology),
39: 167–184.
Shimazu, T. 2016. Digeneans parasitic in freshwaterﬁshes (Osteichthyes) of Japan. VII. Allocreadiidae:
Allocreadium. Bulletin of the National Museum of
Nature and Science, Series A (Zoology), 42: 55–79.
Ślusarski, W. 1958. The adult Digenea from Salmonidaeof the basin of the Vistula and of the South Baltic. Acta
Parasitologica Polonica, 6: 247–528. (In Polish withEnglish summary.)
Sokolov, S. G. and I. I. Gordeev 2014. Occurrence of helminths in amphipods Gammarus lacustris Sars, 1863
(Amphipoda: Gammaridae) from Kronotskoe Lake
(Kamchatka). Parazitologiya, 48: 325–332. (In Russianwith English summary.)
Sokolov, S. G., M. B. Shedko, E. N. Protasova and E. V.
Frolov 2012. [Parasites of the inland water ﬁshes of
Sakhalin Island.] Rastitelʼnyi i zhivotnyi mir severozapadnoi chasti Tikhogo okeana, pp. 179–216. Vladivostok. (In Russian.)
Stenko, R. P. 1982. [Life cycle of Crepidostomum metoecus (Trematoda: Bunoderidae).] In Parazity i parazitozy cheloveka i zhivotnykh, pp. 198–204. Naukova
Dumka, Kiev. (In Russian.)
Yamaguti, S. and H. Matumura 1942. Two new species ofﬁsh trematodes from Hokkaido. Transactions of the
Sapporo Natural History Society, 17: 117–122.