Bull. Natn. Sci. Mus., Tokyo, Ser. A, 30(2), pp. 61–66, June 22, 2004

A New Genus, Magniuterina (Digenea, Lecithodendriidae),with a Redescription of Adults of M. leoi
(Uchida, Uchida & Kamei, 1986) comb. nov. Parasitic in the
Salamander Onychodactylus japonicus from Japan
Takeshi Shimazu
Nagano Prefectural College, 8–49–7 Miwa, Nagano, 380–8525 Japane-mail: shimazu@nagano-kentan.ac.jp

Abstract A new genus, Magniuterina (Digenea, Lecithodendriidae), is created with Cephalouterina leoi Uchida, Uchida & Kamei, 1986 as the type and only species. This new genus is distinguished from the most closely related genus Cephalouterina Senger & Macy, 1953 by having the
genital pore situated ventral and the uterus occupying most of the hindbody. The genus
Cephalouterina is considered as different from the genus Cryptotropa Strand, 1928. Adults including the holotype of M. leoi (Uchida et al., 1986) comb. nov. found in the small intestine of Onychodactylus japonicus (Houttuyn) (Amphibia, Urodela, Hynobiidae) taken in Fukushima andNagano Prefectures, Honshu, Japan, are described and illustrated.
Key words : Magniuterina gen. nov., M. leoi (Uchida et al., 1986) comb. nov., Cephalouterina,
Cryptotropa, Digenea, Onychodactylus japonicus, Amphibia, Japan

Introduction
Senger & Macy (1953) described Cephalouterina dicamptodoni as a new genus and species
from the salamander Dicamptodon ensatus taken
at Cascade Range, Oregon, USA. Uchida et al.
(1986) added a second species of the genus, C.
leoi, from the salamander Onychodactylus japonicus taken at Hinoemata, Fukushima Prefecture,
Honshu, Japan.
Some samples of O. japonicus collected in
Honshu were examined for the monogenean
Pseudopolystoma dendriticum. Besides the monogenean, some specimens of C. leoi also were obtained in this examination. Close examination of
the specimens and some related ones led me topropose a new genus for C. leoi.
Materials and Methods
The samples of the salamander Onychodactylus japonicus (Houttuyn) (Amphibia, Urodela,Hynobiidae) collected were as follows: 100
adults collected at Hinoemata, Fukushima Prefecture, on 17 June 2003; 1 adult and 1 larva, 7adults and 4 larvae, and 6 adults collected at Utsukushigahara, Matsumoto, Nagano Prefecture,
Honshu, on 23 May 2001, 3 June 2001, and 1
June 2002, respectively; 1 adult and 5 larvae collected at Wada, Nagano Prefecture, on 24 May
2003; 2 adults collected in the Yakeyamasawa
River at Takeshi, Nagano Prefecture, on 30 May
2003; and 47 adults and 5 larvae collected in Hinokisawa, a tributary of the Yakeyamasawa
River, at Takeshi on 22 June 2003. The salamanders were examined for helminth parasites.
The digenean specimens obtained were fixedwith hot 10% neutralized formalin and stainedwith Mayer’s acid hematoxylin; slightly flattened,
fixed with AFA, and stained with Heidenhain’s
iron hematoxylin; or slightly flattened, fixed with
70% ethanol, and stained with Grenacher’s alumcarmine. These stained specimens were mounted
in Canada balsam.

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Specimens borrowed for comparison were as
follows: the holotype (stained and whole-mounted adult) of Cephalouterina leoi Uchida et al.,1986 (Akihiko Uchida’s personal collection),found in the small intestine of O. japonicus taken
at Hinoemata (Uchida et al., 1986); a paratype(stained and whole-mounted adult) of C.
dicamptodoni Senger & Macy, 1953 (U.S. National Parasite Collection, USNPC No.
047554.00) found in the small intestine of thesalamander Dicamptodon ensatus (Eschscholtz)(Cryptobranchidae) taken at Cascade Range,
Oregon, USA (Senger & Macy, 1953); 1 specimen (serially-sectioned adult) of Cryptotrema
kuretanii Ozaki, 1926, namely now Cryptotropa
kuretanii (Ozaki, 1926) Strand, 1928 [Yoshimasa
Ozaki’s collection deposited in Meguro Parasitological Museum (MPM), Tokyo, MPM Coll. No.
30138] [most presumably found in the small intestine of Polypedates buergeri (Schlegel)[Buergeria buergeri (Schlegel)] (Amphibia,
Anura, Rhacophoridae) taken in the vicinity ofYasuhara, Kagawa Prefecture, Shikoku, Japan](Ozaki, 1926); and many unpublished specimens(stained and whole-mounted adults) of C. kuretanii collected on Okinawa Island, Okinawa Prefecture, Japan [Hideo Hasegawa’s personal collection, now deposited in the National Science
Museum, Tokyo (NSMT)]. The last mentioned
included: 4 (NSMT-Pl 5234) found in the small
intestine of Rhacophorus viridis viridis (Hallowell) (Rhacophoridae) taken at the upper reachesof the Benoki River at Kunigamison on 16 January 1984; 6 (NSMT-Pl 5233) found in the small
intestine of R. viridis viridis taken at Benoki, Kunigamison, on 24 February 1989; 4 (NSMT-Pl
5235) found in the small intestine of Rana (Hylarana) narina narina Stejneger (Amphibia,
Anura, Ranidae) taken at the upper reaches of the
Benoki River at Kunigamison on 15 January
1984 (see Hasegawa & Iwatsuki, 1986); 23(NSMT-Pl 5236) found in the small intestine of
Japalura polygonata polygonata (Hallowell)(Reptilia, Squamata, Agamidae) taken at Mt.
Yonaha-dake, Yonaha, in August 1984; and 29(NSMT-Pl 5237). found in the small intestine ofJ. polygonata polygonata taken at Yonaha on 14
September 1984.
Drawings were made with the aid of a drawing
tube. Measurements are given in millimeters unless stated otherwise. The specimens studied
have been deposited in the NSMT.
Magniuterina gen. nov.
Generic diagnosis. Digenea, Lecithodendriidae. Body elliptical, spinose. Oral sucker subterminal. Prepharynx short. Pharynx elliptical.
Esophagus bifurcating anterior to ventral sucker.
Intestinal ceca ending at level of ventral sucker.
Ventral sucker median, pre-equatorial. Testes
symmetrical, separated, post-equatorial. Cirrus
pouch clavate, with its posterior end overlapping
ventral sucker, including a bipartite seminal vesicle, a small pars prostatica surrounded by prostatic cells, and a protrusible cirrus. Genital atrium
small. Genital pore ventral on left side of body,
bifurcal, pre-cecal. Ovary postero-dextral to ventral sucker, pre-testicular. Seminal receptacleoval, between ovary and right testis. Laurer’s
canal present. Ootype median, posterior to ventral sucker. Uterus coiling in most of hindbody;
metraterm well developed. Eggs operculate, notembyonated when laid. Vitelline follicles usuallyconfined to field between oral sucker and ovary
and left testis. Excretory vesicle Y-shaped, extending anteriorly to ootype. Parasitic in small
intestine of salamanders.
Type and only species: Cephalouterina leoi
Uchida, Uchida & Kamei, 1986.
Etymology. The generic name is derived froma combination of the Latin words magnus anduterinus, meaning “large” and “uterine”, respectively. The gender of the genus is feminine.
Discussion. This new genus is different fromthe genus Cephalouterina in that the genital poreis ventral instead of dorsal (Senger & Macy,
1953) and the uterus coils entirely in the hindbody instead of mostly in the forebody (Senger& Macy, 1953). My re-examination of theparatype of C. dicamptodoni, the type species of
the genus, has confirmed that the descriptions ofMagiuterina gen. nov. and Adults of M. leoithese respects by Senger & Macy (1953) are correct.
The new genus is differentiated from the genus
Cryptotropa Strand, 1928 [syn. Cryptotrema
Ozaki, 1926, preoccupied by Cryptotrema
Gilbert, 1890 (Pisces)] (Lecithodendriidae),whose type species is Cryptotrema kuretanii
Ozaki, 1926, namely now Cryptotropa kuretanii(Ozaki, 1926) Strand, 1928, by the genital pore
opening ventrally instead of dorsally (Ozaki,
1926; Hasegawa & Iwatsuki, 1984; this study),
the uterus occupying all available space of thehindbody in stead of the space between the bifurcal level and the testis on each side of the bodyand the inter-testicular space (Ozaki, 1926;
Hasegawa & Iwatsuki, 1984; this study), and thevitelline follicles being restricted to the field between the oral sucker and the ovary and left testis
instead of the field between the pharyngeal level
and the junction of the middle and posterior
thirds of the post-testicular region (Ozaki, 1926;
Hasegawa & Iwatsuki, 1984; this study).
Khotenovskiï (1965) and Prudhoe and Bray
(1982) synonymize the genus Cephalouterinawith the genus Cryptotropa. The type species ofthe latter, Cryptotrema kuretanii, was originallydescribed as a new genus and species by Ozaki(1926) from the [small] intestine of the frog
Polypedates buergeri (Buergeria buergeri)
caught in the vicinity of Yasuhara, Kagawa Prefecture, Shikoku, Japan. As Yamaguti (1971)
points out, however, the genus Cephalouterina(type species Cepahalouterina dicamptodoni) is
distinguished from the genus Cryptotropa by the
distribution area of the vitelline follicles. The
vitelline follicles are distributed mostly in thespace between the oral sucker and the testes in
the genus Cephalouterina (Senger & Macy,
1953; this study), though rarely more posteriorly
as far as the mid-level of the post-testicular region on each side of the body (Khotenovskiï,1965). However, they fill most of the body, always entering the post-testicular region, in thegenus Cryptotropa (Ozaki, 1926; Hasegawa &Iwatsuki, 1984; this study). Moreover, the uterus
coils only in the forebody in the genus

63

Cephalouterina (Senger & Macy, 1953; Khotenovskiï, 1965; Anderson et al., 1966; this study)
instead of in the space between the bifurcal level
and the testes on each side of the body and in theinter-testicular space of the body in the genus
Cryptotropa (Ozaki, 1926; Hasegawa & Iwatsuki, 1984; this study). The genus Cephalouterina
is regarded as distinct from the genus Cryptotropa.
Magniuterina leoi
(Uchida, Uchida & Kamei, 1986) comb. nov.
Syn. Cephalouterina leoi Uchida, Uchida & Kamei, 1986

Occurrence. Specimens of this species were
found in the small intestine of salamanders: 10 (2senile and 8 gravid adults) (NSMT-Pl 5229) in 1of the 100 adults from Hinoemata on 17 June
2003; and 9 gravid adults (NSMT-Pl 5230) in thelarva from Utsukushigahara on 23 May 2001.
Description (Fig. 1). Ten flattened specimensfrom Hinoemata measured. Body elliptical, spinose, 2.50–3.30 long by 1.20–1.52 wide; forebody
0.94–1.42 long, 36–44% of body length. Numerous gland cells present in lateral field of prececal space on each side of body, possibly each
opening at anterior tip of body. Oral sucker depressed round, subterminal, 0.26–0.35 long by
0.35–0.39 wide. Prepharynx very short. Pharynx
oval, with 2 lateral, 1 ventral and 1 dorsal muscular processes at its anterior tip, 0.10–0.14 long by
0.14–0.16 wide. Esophagus 0.08–0.27 long, bifurcating about midway between two suckers. Intestinal ceca short, ending at level of ventral
sucker. Ventral sucker round, median, slightly
posterior to junction of anterior and middle thirdsof body, bearing spines especially on peripheral
region of internal surface, 0.35–0.39 long by
0.33–0.39 wide; sucker width ratio 1 : 0.9–1.0.
Testes oblong, almost symmetrical, separated, located at about junction of middle and posterior
thirds of body, 0.47–0.78 long by 0.16–0.39
wide. Cirrus pouch claviform, curved, ventral todigestive tract, with its posterior end overlapping
ventral sucker, 0.51–0.82 long. Seminal vesicle
internal, bipartite; anterior portion round; poste-

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Takeshi Shimazu

Figs. 1–3. Magniuterina leoi found in the small intestine of Onychodactylus japonicus. 1. Gravid adult, newspecimen from Hinoemata, flattened, entire body, ventral view. The uterus was so convoluted that its runningcourse could not be traced accurately. Uterine eggs are omitted. 2. Senile adult, holotype from Hinoemata,flattened, entire body, ventral view. The uterus was so convoluted that its running course could not be traced
accurately. 3. Ovarian complex, holotype, ventral view. Scale bars: 1 mm in Figs. 1 and 2; 0.5 mm in Fig. 3.

Magiuterina gen. nov. and Adults of M. leoirior elliptical, larger than anterior. Pars prostatica
oval, surrounded by prostatic cells. Cirrus (orejaculatory duct) long, slightly sinuous, protrusible, armed with dense fine spines. Genital atrium
small. Genital pore opening ventrally, to left ofmedian line, about bifurcal, anterior to left intestinal cecum. Ovary elliptical or triangular, located postero-dextral to ventral sucker, anterior
to right testis, 0.33–0.41 long by 0.20–0.47 wide.
Seminal receptacle oval, located between ovary
and right testis, 0.25–0.37 by 0.16–0.29 wide.
Laurer’s canal opening dorsally, surrounded bygland cells. Ootype almost median, posterior toventral sucker; Mehlis’ glands free in parenchyma, developed well. Uterus long, inflated, convoluted in all available space (pre-, inter-, and posttesticular spaces) of hindbody, not reaching posterior extremity of body; sphincter not seen at
distal end of uterus; metraterm long, surroundedby gland cells. Eggs operculate, numerous, witha short spine at anopercular pole, 32–36 by
12–14 m m, not embyonated when laid. Vitelline
follicles arranged in two lateral groups, usuallyconfined to field between oral sucker and ovary
and left testis, sometimes extending only slightly
farther beyond left testis, usually confluent acrossforebody, present mostly dorsal to digestive tract.
Excretory vesicle Y-shaped, with a long smooth
stem and short arms, extending anteriorly toootype; excretory pore postero-terminal.
Discussion. The present specimens are identified as C. leoi. Uchida et al. (1986) described andillustrated (fig. 1), for this species: the cirrus
pouch as dorsal to the digestive tract and extending from “the level of intestinal bifurcation” [butthe mid-level of the ventral sucker (fig. 1)] to“that of esophagus”; the genital pore as “dorsolateral to esophagus” [namely dorsal]; Laurer’s
canal as undulating; and the right arm of the excretory vesicle as anterior to the seminal receptacle. My re-examination of the holotype of thespecies (Figs. 2 and 3), apparently a senile adultwith eggs only in several parts of the uterus, has
shown that: the cirrus pouch is ventral to the digestive tract and extends from the mid-level ofthe ventral sucker to the bifurcal level; the genital

65

pore is ventral, to the left of the median line, bifurcal, and anterior to the left intestinal cecum;
Laurer’s canal is smoothly curved; the uterus
coils in much more of the hindbody than figured(fig. 1); and the right arm of the excretory vesicle
is ventral to the seminal receptacle.
Magniuterina leoi has been known to occur in
O. japonicus from Honshu, Japan (Uchida et al.,
1986; this study). Its life cycle has not yet been
elucidated.
In the present examination of the salamanders,the following helminth parasites were obtained aswell.
Specimensofthemonogenean
Pseudopolystoma dendriticum (Ozaki, 1948) Yamaguti, 1963 (Polystomatidae) were found in theurinary bladder of salamanders: 1, 1, 1, 1, and 2
each in 5 of the 100 adults from Hinoemata on
17 June 2003; 2 and 1 each in the two adults
from Utsukushigahara on 23 May 2001 and 3
June 2001, respectively; and 1, 1, 1, and 3 eachin 4 of the 47 adults from Hinokisawa on 22 June
2003. These specimens were sent to Dr. Sophie
Bentz and Prof. Claude Combes (Perpignan Universitaire, Perpignan, France) for molecular phylogenetic analysis. Specimens of the digenean
Mesocoelium brevicaecum Ochi, 1930 (Brachycoelidae) were found in the small intestine ofsalamanders: 2, 7, and 10 each (NSMT-Pl 5232)
in 3 of the 100 adults from Hinoemata; and 4(NSMT-Pl 5231) in the adult from the Yakeyamasawa River on 30 May 2003. Specimens of nematodes were found in the stomach, small intestine,large intestine, and rectum of salamanders. They
remain to be identified.
Acknowledgments
I thank Mr. Syu Sakai and Mr. Taiki Kojima(Matsumoto), for collecting the salamanders in
Nagano Prefecture; Prof. Akihiko Uchida (Azabu
University, Sagamihara), Prof. Hideo Hasegawa(Oita University, Hasama), Dr. Eric P. Hoberg(USDA, Agricultural Research Service, Beltville,USA), and Mr. Jun Araki (MPM, Tokyo), forlending me the specimens; and Dr. David I. Gibson (The Natural History Museum, London, UK)

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and Dr. Keiichi Matsuura (NSMT) for informing
me about the nomenclature and reference, respectively.
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