Rediscovery of a Fish Acanthocephalan, Acanthocephalus minor (Echinorhynchida: Echinorhynchidae), in the Lake Biwa Basin, Central Japan, with a Review of the Fish Acanthocephalan Fauna of the Basin

Abstract

Specimens of the echinorhynchid acanthocephalan Acanthocephalus minor
Yamaguti, 1935 were collected from the rectum of a dark sleeper, Odontobutis obscura (Temminck and Schlegel, 1845), in an irrigation canal near Lake Biwa, Shiga Prefecture, west-central Japan. This represents a rediscovery of A. minor in the Lake Biwa basin after a gap of nearly 80 years. It appears not to be distributed in Lake Biwa proper, but to occur rarely in rivers and irrigation canals of a limited coastal area around the lake. To date, 10 nominal species of acanthocephalan in four families and three orders have been reported from fish in the Lake Biwa basin. Among these, striking morphological similarities between Acanthocephalus aculeatus
Van Cleave, 1931 and its congener A. opsariichthydis
Yamaguti, 1935 are noted. It is furthermore suggested that A. gotoi
Van Cleave, 1925 could not maintain its population after the basin's wild population of its major host, Anguilla japonica Temminck and Schlegel, 1846, disappeared in the mid-1960s.

Full text

© 2015 e Japanese Society of Systematic Zoology
Species Diversity 20: 73–81
Rediscovery of a Fish Acanthocephalan, Acanthocephalus
minor (Echinorhynchida: Echinorhynchidae),
in the Lake Biwa Basin, Central Japan, with a Review
of the Fish Acanthocephalan Fauna of the Basin
Kazuya Nagasawa1,2 and Masato Nitta1
1 Graduate School of Biosphere Science, Hiroshima University,
1-4-4 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8528, Japan
E-mail: ornatus@hiroshima-u.ac.jp (KN); licht.bsn.mono@gmail.com (MN)
2 Corresponding author
(Received 28 January 2015; Accepted 30 April 2015)
Specimens of the echinorhynchid acanthocephalan Acanthocephalus minor Yamaguti, 1935 were collected from the
rectum of a dark sleeper, Odontobutis obscura (Temminck and Schlegel, 1845), in an irrigation canal near Lake Biwa, Shiga
Prefecture, west-central Japan. is represents a rediscovery of A. minor in the Lake Biwa basin aer a gap of nearly 80
years. It appears not to be distributed in Lake Biwa proper, but to occur rarely in rivers and irrigation canals of a limited
coastal area around the lake. To date, 10 nominal species of acanthocephalan in four families and three orders have been re-
ported from sh in the Lake Biwa basin. Among these, striking morphological similarities between Acanthocephalus aculea-
tus Van Cleave, 1931 and its congener A. opsariichthydis Yamaguti, 1935 are noted. It is furthermore suggested that A. gotoi
Van Cleave, 1925 could not maintain its population aer the basin’s wild population of its major host, Anguilla japonica
Temminck and Schlegel, 1846, disappeared in the mid-1960s.
Key Words: Acanthocephalus minor, Acanthocephala, Odontobutis obscura, sh parasite, faunistic review, Lake Biwa
basin, Japan.
Introduction
Lake Biwa is located in west-central Honshu, being the
largest (670 km2) and oldest (over four million years old)
lake in Japan (Horie 1984). e fauna of this lake and its
watershed has been intensively studied and includes many
endemic species (Timoshkin et al. 2011; Kawanabe et al.
2012). e acanthocephalan fauna of sh in the Lake Biwa
basin is also well studied: to date, 10 nominal species in
four families and three orders have been reported (Table
1). Among these species, the extent of occurrence of Acan-
thocephalus minor Yamaguti, 1935 in Lake Biwa and the
lake’s drainage basin remains poorly understood. is spe-
cies has not been reported since 1936, when it was collected
from the dark sleeper Odontobutis obscura (Temminck and
Schlegel, 1845) caught in Lake Biwa (Fukui and Morisita
1936). Amin (2005) and Amin et al. (2007) examined the
acanthocephalans isolated from more than 500 inspected
sh belonging to 30 species in 12 families collected in Lake
Biwa and its tributaries between 1997 and 2002 as part of a
large-scale survey involving 62 sh species in total from the
region, but did not recover A. minor from them; moreover,
they did not mention A. minor in their discussion of the sh
acanthocephalan fauna of the Lake Biwa basin.
Recently, we found 10 individuals of A. minor infecting
the rectum of a specimen of O. obscura collected in an ir-
rigation canal near the Ado River, one of the rivers ow-
ing into Lake Biwa. Here we report on this nd which rep-
resents a rediscovery of the species in the Lake Biwa basin
aer a gap of nearly 80 years. We also take this opportunity
to review the sh acanthocephalan fauna of the Lake Biwa
basin based on the literature published between 1918 and
2014.
Materials and Methods
One specimen of O. obscura was collected using a hand
net on 14 July 2014 in an irrigation canal (35°19′54″N,
136°2′44″E) along the lower reaches of the Ado River at
Adogawacho-Kawashima, Takashima city, Shiga Prefec-
ture, Honshu, west-central Japan. e sh was transported
alive to the laboratory at Hiroshima University, Higashi-
Hiroshima city, Hiroshima Prefecture, where it was mea-
sured for standard length (SL) in millimeters and examined
for metazoan parasites. Of the 10 acanthocephalans found,
eight individuals were attened between slides and cover
glasses with slight pressure, xed in 70% ethanol, stained
in Heidenhain’s iron hematoxylin, dehydrated through a
graded ethanol series, cleared in xylene, and mounted in
Canada balsam, while the remaining two individuals were
preserved in 100% ethanol for future molecular study. e
stained specimens were used for measurements and counts.
25 May 2015
DOI: 10.12782/sd.20.1.073

74 K. Nagasawa and M. Nitta
Table 1. Acanathocephalans reported from sh in the Lake Biwa basin, Shiga Prefecture, Japan.
Order Family Genus and species Fish species (family) Reference
Gyracanthocephala Quadrigyridae Acanthosentis (Acanthosentis) alternatspinus
Amin, 2005
Rhodeus ocellatus ocellatus (Cyprinidae) Amin (2005), Amin et al. (2007), Nagasawa
and Grygier (2011, as Neoechinorhynchus
sp.)a
Acanthosentis (Acanthosentis) parareceptacilis
Amin, 2005
Cobitis biwae (Cobitidae) Amin (2005), Amin et al. (2007)
Echinorhynchida Echinorhynchidae Acanthocephalus aculeatus Van Cleave, 1931bPlecoglossus altivelis altivelis (as P. a lt iv el is ) (Plecoglossidae) Kataoka and Momma (1933, 1934)
Acanthocephalus gotoi Van Cleave, 1925 Gymnogobius urotaenia (as Chaenogobius annularis urotaenia) (Gobiidae) Yamaguti (1939)
Acanthocephalus minor Yamaguti, 1935 Odontobutis obscura (Odontobutidae) Fukui and Morisita (1936), this study
Acanthocephalus opsariichthydis Yamaguti, 1935 Cobitis biwae (Cobitidae); Gnathopogon elongatus elongatus, Hemibarbus barbus, Hemibarbus
labeo, Hemibarbus longirostris, Opsariichthys platypus (as Zacco platypus), Phoxinus oxycephalus
jouyi (as Rhynchocypris o. jouyi), Pseudogobio esocinus esocinus, Pseudorasbora parva, Pungtungia
herzi (Cyprinidae); Gasterosteus aculeatus subsp. 2 (as G. microcephalus) (
Gasterosteidae
);
Oncorhynchus masou ishikawae, Oncorhynchus mykiss (as Salmo gairdnerii irideus),
Oncorhynchus sp. (Salmonidae); Silurus asotus (as Parasilurus asotus) (Siluridae)
Yamaguti (1935)c, Ito (1959, as Acantho-
cepharus [sic] sp.), Nakajima et al. (1975),
Nakajima and Egusa (1975a), Amin et al.
(2007)
Echinorhynchus cotti Yamaguti, 1935dAnguilla japonica (Anguillidae); Tachysurus nudiceps (as Pelteobagrus nudiceps) (Bagridae);
Channa argus (Channidae); Cottus polluxe, Cottus reinii (Cottidae); Cyprinus carpio, Gnathopogon
caerulescens, Hemibarbus barbus, Opsariicthys uncirostris uncirostris, Sarcocheilichthys variegatus
microoculus (Cyprinidae); Gymnogobius isaza, Rhinogobius sp., Tridentiger brevispinis (Gobiidae);
Hypomesus nipponensis (as H. transpacicus nipponensis) (Osmeridae); Plecoglossus altivelis
altivelis (as P. altivelis) (Plecoglossidae); Silurus biwaensis (Siluridae)
Kataoka and Momma (1933, 1934, as
Echinorhynchus sp.), Yamaguti (1935, 1939),
Fukui and Morisita (1937), Shimazu (1999),
Amin et al.(2007)
Echinorhynchus parasiluri Fukui, 1929 Silrus asotus (as Parasilurus asotus) (Siluridae) Fukui (1929)
Echinorhynchus sp. Anguilla japonica (Anguillidae); Cyprinus carpio (Cyprinidae) Kawamura (1918)
Illiosentidae Pseudorhadinorhynchus samegaiensis Nakajima
and Egusa, 1975
Anguilla japonica (Anguillidae); Hemibarbus barbus, Opsariichthys uncirostris uncirostris,
Tribolodon hakonensis (Cyprinidae); Gasterosteus aculeatus subsp. 2 (as G. microcephalus)
(Gasterosteidae); Gymnogobius isaza (Gobiidae); Oncorhynchus mykiss (as Salmo gairdnerii
irideus), Oncorhynchus masou ishikawae (Salmonidae)
Nakajima et al. (1975), Nakajima and Egusa
(1975b), Grygier (2004), Amin et al. (2007),
Nagasawa and Grygier (2011)
Polymorphida Polymorphidae Southwellina hispida (Van Cleave, 1925) Micropterus salmoides (Centrarchidae); Lefua echigonia (Cobitidae); Cottus reinii (Cottidae);
Candidia sieboldii (as Zacco sieboldii), Tanakia lanceolata, Tanakia limbata (Cyprinidae);
Coreoperca kawamebari (Sinipercidae)
Amin et al. (2007), Nagasawa and Grygier
(2011)
Unidentied
Acanthocephala
Tachysurus nudiceps (as Fluvidraco nudiceps) (Bagridae); Misgurnus anguillicaudatus
(Cobitidae); Candidia platypus (as Zacco platypus), Gnathopogon caerulescens (as Leucogobio
mayedae), Sarcocheilichthys sp. (as S. variegatus)f, Opsariichthys uncirostris uncirostris (as
Opsar ichthys [sic] uncirostris) (Cyprinidae); Gymnogobius isaza (as Chloea castanea)
(Gobiidae); Salvelinus leucomaenis japonicus (as S. pluvius) (Salmonidae)
Fujita (1927), Amin et al. (2007)
ae manuscript of Nagasawa and Grygier’s report, including information on Neoechinorhynchus sp., was rst prepared in 1998 but was not published until 2011. is acanthocephalan was described as Acanthosentis
(Acanthosentis) alternatspinus by Amin (2005). bAcanthocephalus aculeatus had been synonymized with Acanthocephalus echigoensis by Harada (1935), but Petrochenko (1956) and Yamaguti (1963) listed the former spe-
cies as valid. cYamaguti (1935) described Acanthocephalus opsariichthydis using specimens from seven species of sh (P. curta, C. carpio, H. barbus, O. uncirostris uncirostris, O. platypus, P. parva, and P. asotus) caught in
three localities, Lake Biwa (Shiga Prefecture), Lake Ogura (Kyoto Prefecture), and the Yodo River (Osaka Prefecture), all of which belong to the same river system, but he did not dierentiate these localities from each
other in his description of the species. However, according to Amin et al. (2007), only P. parva was collected in Lake Biwa. us, this sh is cited here from Yamaguti (1935). dGolvan (1969) described a new species, Echi-
norhynchus oblitus, by citing Kataoka and Momma (1937), but Nagasawa et al. (2007) relegated E. oblitus to a junior synonym of E. cotti. e paper of Kataoka and Momma (1937) was part of a set of collected papers, and
the original work was Kataoka and Momma (1934), in which Echinorhynchus sp. was described. ee sh reported as Cottus pollux by Yamaguti (1939) from Lake Biwa was actually C. reinii (Amin et al. 2007). fBecause
three species and subspecies of Sarcocheilichthys (S. biwaenisis, S. variegatus variegatus, and S. variegatus microoculus) occur in Lake Biwa and its watershed (Hosoya 2013), the sh reported by Fujita (1927) as S. variega-
tus cannot be exactly identied.

A sh parasite from the Lake Biwa basin 75
All measurements in the text are given in millimeters as the
range followed by the mean in parentheses, unless other-
wise stated. Drawings were made with the aid of a drawing
tube tted on an Olympus BX 51 compound microscope.
e mounted specimens are deposited in the Aschelmin-
thes (As) collection of the National Museum of Nature and
Science (NSMT–As 4293), Tsukuba city, Ibaraki Prefecture,
Japan. e scientic names of sh, amphipods, and isopods
used in this paper follow those recommended by Nakabo
(2013), Tomikawa and Morino (2012), and Matsumoto
(1973), respectively.
Acanthocephalus minor Yamaguti, 1935
(Fig. 1)
Acanthocephalus minor Yamaguti, 1935: 253–254, gs 3–5
(type locality: Toyama Prefecture, Japan); Fukui and
Morisita 1936: 761; Yamaguti 1939: 322–323; Petro-
chenko 1956: 311, g. 126; Fukui 1962: 128; Yamada
1962: 277, g. H; Yamaguti 1963: 47; Fukui 1965: 468,
gs 1–3; Golvan 1969: 276, g. 213; Awakura 1972: 1–12,
gs 1–8; Fukui 1973: 275, g. 14-5; Uchida 1979: 149, g.
6; Awakura 1980: 207; Nagasawa et al. 1982: 229–231;
Awakura et al. 1984: 10; Amin 1985: 42; Nagasawa et al.
1987: 35; Awakura 1989: 608; Golvan 1994: 137; Shima-
zu 1999: 23–24; Araki 1999: 159; Araki 2003: 149; Amin
2013: 285; Yokoyama and Nagasawa 2014: 84.
Acanthocephalus echigoensis: Anonymous 1972: 146–148;
Awakura 1973: 12–14, unnumbered g.
Description. General. Trunk subcylindrical, unarmed,
slightly tapering posteriorly. Body wall thick. Proboscis cy-
lindrical, armed with 12–14 (usually 13) longitudinal rows
of 5–7 (usually 5 or 6) hooks in both sexes. Second or third
hook from distal end largest and basal hook smallest in each
row. Hook blade longer than root. Neck short. Proboscis re-
ceptacle double-walled, with cerebral ganglion near its pos-
terior end. Lemnisci saccular or elongate, longer than pro-
boscis receptacle. Genital pore terminal.
Male (based on four specimens). Trunk 2.45–3.03 (2.72)
long, 0.79–0.91 (0.84) wide. Proboscis 0.35–0.45 (0.39) long,
0.21–0.23 (0.21) wide. Blade of largest (i.e. second or third)
hook in each row 65–74 (70) µm long; blade of smallest (i.e.
basal) hook in each row 38–51 (47) µm long. Neck 0.15–
0.21 (0.18) long (n = 2), 0.37–0.41 (0.39) wide at junction
with trunk (n = 2). Proboscis receptacle 0.34–0.40 (0.38)
long, 0.19–0.23 (0.21) wide. Lemnisci 0.26–0.48 (0.36) long,
0.6–0.18 (0.11) wide. Testes oval, slightly oblique. Anterior
testis 0.34–0.35 (0.34) long, 0.22–0.28 (0.25) wide; posterior
testis 0.30–0.34 (0.33) long, 0.20–0.27 (0.22) wide. Cement
glands pyriform, close together, 0.10–0.18 (0.12) wide in
diameter, immediately behind posterior testis. Saeigen’s
pouch bulb-shaped, 0.35–0.43 (0.39) long, 0.20 (0.20) wide
(n = 2).
Female (based on four specimens). Trunk 2.05–3.35
(2.62) long, 0.88–1.18 (1.03) wide. Proboscis 0.40–0.50
(0.47) long, 0.19–0.29 (0.24) wide. Blade of largest (i.e. sec-
ond or third) hook in each row 85–92 (87) µm long; blade
Fig. 1. Acanthocephalus minor Yamaguti, 1935, NSMT–As 4293,
from rectum of Odontobutis obscura (Temminck and Schlegel,
1845). A, Entire body of male; B, proboscis of female. Scale bars: A,
1 mm; B, 100 µm.

76 K. Nagasawa and M. Nitta
of smallest (i.e. basal) hook in each row 43–75 (60) µm long.
Neck 0.17–0.23 (0.19) long, 0.38–0.53 (0.44) wide at junc-
tion with trunk. Proboscis receptacle 0.30–0.54 (0.42) long,
0.19–0.26 (0.24) wide. Lemnisci 0.23–0.48 (0.36) long, 0.8–
0.15 (0.10) wide. Reproductive system 0.50–0.73 (0.61) long,
21.6–25.5% (23.6%) of trunk length. Mature eggs with polar
prolongations of middle shell 96–104 (99) µm long, 17–20
(18) µm wide when measured through body wall.
Host. Dark sleeper Odontobutis obscura (Perciformes:
Odontobutidae).
Locality. Irrigation canal near Ado River at Adogawa-
cho-Kawashima, Takashima city, Shiga Prefecture, Honshu,
Japan.
Site of infection. Rectum.
Occurrence in sh. Ten individuals of A. minor were
found in one specimen of O. obscura (64.3 mm SL). e
eight stained specimens comprised four individuals of each
sex.
Remarks. e morphology of the specimens collected
in this study almost fully corresponds to the original de-
scription of A. minor by Yamaguti (1935) and the subse-
quent brief descriptions of the species by Fukui and Morisita
(1936), Yamaguti (1939), and Awakura (1972), except that
the number (5–7) of hooks per longitudinal row is fewer
than in previous reports (7–9: Yamaguti 1935; 6–7: Fukui
and Morisita 1936; 6–8: Yamaguti 1939; 7–9: Awakura
1972).
Acanthocephalus minor was originally described based
on specimens from Amur catsh Silurus asotus Linnaeus,
1758 (as Parasilurus asotus) in Toyama Prefecture, central
Honshu, Japan (Yamaguti 1935). Subsequently, this acantho-
cephalan has been recorded from various freshwater sh in
central Honshu and Hokkaido, Japan (Fukui and Morisita
1936; Yamaguti 1939; Awakura 1972; Nagasawa et al. 1982).
ere is no record of this species from other countries. Pet-
rochenko (1956: 293) doubted the generic assignment of the
species, but subsequent authors (e.g., Yamaguti 1963; Gol-
van 1969, 1994; Amin 1985, 2013) have continued to place it
in Acanthocephalus Koelreuther, 1771. Awakura (1973) used
Acanthocephalus echigoensis Fujita, 1920 as the scientic
name of acanthocephalans that had heavily infected sh at a
trout hatchery in Hokkaido (see also Anonymous 1972), but
this was denitely wrong because the same author (Awakura
1972) had already identied the parasite as A. minor based
on its morphological characteristics.
In 1936, A. minor was found in Odontobutis obscura in
“Lake Biwa” (Fukui and Morisita 1936; see the Discussion
section herein concerning this locality), but this acantho-
cephalan has not been reported from the lake or associated
waters by any subsequent researcher (e.g., Fukui and Moris-
ita 1937; Yamaguti 1939; Amin et al. 2007). e nding of
A. minor in this study conrmed its occurrence in the Lake
Biwa basin.
All of the present individuals of A. minor were found in
the rectum of the sh examined. is site specicity of A.
minor within the host’s intestine was previously noticed by
Nagasawa et al. (1982).
Discussion
Occurrence and geographical distribution of Acan-
thocephalus minor in the Lake Biwa basin. ere is a
nearly 100-year history of research on the sh acantho-
cephalans of Lake Biwa and its drainage basin (Kawamura
1918; Fujita 1927; Fukui 1929; Kataoka and Momma 1933,
1934; Yamaguti 1935, 1939; Fukui and Morisita 1936, 1937;
Ito 1959; Nakajima et al. 1975; Nakajima and Egusa 1975a,
1975b; Shimazu 1999; Grygier 2004; Amin 2005; Amin et
al. 2007a, 2007b). In particular, during the 1930s, Yamaguti
(1935, 1939) conducted a systematic survey of sh parasites
in Japan including the Lake Biwa basin but did not report
A. minor from the basin. Later, Amin et al. (2007) reported
acanthocephalans recovered from an examination of over
500 individuals of sh belonging to 30 species in 12 families
collected from 22 localities including Lake Biwa proper and
various rivers, irrigation canals, and ponds in Shiga Prefec-
ture during 1997–2002, but did not report A. minor among
them. Only Fukui and Morisita (1936) found A. minor in O.
obscura from the Lake Biwa basin 80 years ago, which sug-
gests that this acanthocephalan is a rare species occurring in
a limited area of this basin.
Fukui and Morisita (1936) simply reported “Lake Biwa”
as the sampling locality of A. minor, but this may not be
wholly accurate because Lake Biwa is the largest lake in
Japan and many rivers, streams, and irrigation canals ow
into it. e acanthocephalan specimens were not collected
by these authors but were given to them by a colleague. e
host, Odontobutis obscura, is usually found in the upper and
middle reaches of the lake’s tributaries and only rarely oc-
curs in coastal waters of the lake (Shiga-Kenritsu Biwako-
Bunkakan 1980). Two large-scale surveys of the freshwa-
ter sh fauna of Lake Biwa and its tributaries conducted in
1994–1995 and 2002–2003 also showed that the sh does
not occur in Lake Biwa proper (Anonymous 1996, 2004).
erefore, the specimen of O. obscura reported by Fukui
and Morisita (1936) most probably was not caught in “Lake
Biwa” but in one of the rivers owing into the lake. Since A.
minor utilizes the asellid isopod Asellus hilgendori Boval-
lius, 1886 as its intermediate host (Awakura 1972; Nagasawa
et al. 1982), it is desirable to clarify the distribution pattern
of infected isopods in those rivers and irrigation canals.
Currently, some irrigation canals close to the shore of
Lake Biwa have been recognized as habitats of O. obscura
(Funao et al. 2010; Natsuhara and Akiyama 2012). In the
present study, the infected specimen of O. obscura came
from an irrigation canal in Takashima city, near (7–8 km
away from) an other irrigation canal in which Amin et al.
(2007: g. 1) found four species of acanthocephalan, viz.,
Acanthocephalus opsariichthydis Yamaguti, 1935; Echino-
rhynchus cotti Yamaguti, 1935; Pseudorhadinorhynchus sa-
megaiensis Nakajima and Egusa, 1975; and Southwellina
hispida (Van Cleave, 1925). e irrigation canals sampled
are both located near the northwestern shore of Lake Biwa.
Abundant water is stably supplied from springs to the irri-
gation canals throughout the year (Yasuhiro Fujioka, Lake

A sh parasite from the Lake Biwa basin 77
Biwa Museum, personal communication). Considering the
fact that as many as ve species of acanthocephalan oc-
curred in such irrigation canals, it is likely that the canals
provide favorable environmental and biological conditions
for the parasites to complete their life cycles.
e sh acanthocephalan fauna of the Lake Biwa
basin. To date, 10 nominal species of sh acanthocepha-
lan have been reported from the Lake Biwa basin (Table 1).
Nishino (2012) made a similar list of sh acanthocephalans
of the basin, but some references (viz., Kawamura 1918;
Fujita 1927; Fukui and Morisita 1936; Ito 1959; Amin et al.
2007b; Nagasawa and Grygier 2011) were not cited. Because
Lake Biwa is an ancient lake (over four million years old;
Horie 1984) and many endemic species occur in it (Nishino
and Watanabe 2000; Kawanabe et al. 2012), potential ende-
mism of sh acanthocephalans has also been discussed. In
particular, Pseudorhadinorhynchus samegaiensis has been
suggested to have such a status (Grygier 2004; Amin et al.
2007; Nagasawa and Grygier 2011). is acanthocephalan
was originally described from rainbow trout Oncorhynchus
mykiss (Walbaum, 1792) (as Salmo gairdnerii iredeus Gib-
bons, 1885) at a trout hatchery in the basin (Nakajima and
Egusa 1975b), but this salmonid is not a native host, hav-
ing been introduced into Japan from North America from
1877–1934 and 1951–1955 as eyed eggs (Maruyama et al.
1987). Pseudorhadinorhynchus samegaiensis does not occur
in North America (Homan 1999), and is surely native to
Japan. Among seven other species of infected sh in the
basin reported by Amin et al. (2007), only big-scaled redn
Tribolodon hakonensis (Günther, 1877) harbored gravid fe-
males, so this cyprinid may be the native preferred host. If
so, endemic status of P. samegaiensis in the Lake Biwa basin
would be doubtful because T. hakonensis is not endemic to
the basin but is widely distributed in Japan, ranging from
Hokkaido to Kyushu (Kurawaka 1977; Sakai 1995). e
acanthocephalan fauna of T. hakonensis in other parts of its
range should be intensively examined.
Of the four species of Acanthocephalus reported in the
Lake Biwa basin, A. opsariichthydis has been found in a total
of 15 species of sh in ve families, while A. aculeatus Van
Cleave, 1931 was collected only from ayu Plecoglossus altive-
lis altivelis (Temminck and Schlegel, 1846) (as P. a lt iv el i s ) in
the early 1930s (Kataoka and Momma 1933, 1934). e tax-
onomic status of A. aculeatus remains poorly understood. It
was originally described from sockeye salmon (as the land-
form of blue-back salmon) Oncorhynchus nerka (Walbaum,
1792) in Lake Aoki (as Aoki Lake), Nagano Prefecture (as
Shinano Province), central Japan (Van Cleave 1931). Harada
(1935) synonymized it with A. echigoensis, but since then
its taxonomic relations with other Japanese species of the
genus, including A. opsariichthydis, have not been examined
or discussed.
Morphologically, A. aculeatus and A. opsariichthydis are
quite similar to each other. e proboscis armament, for
example, is 8–10 longitudinal rows of seven or eight hooks
in A. aculeatus (Van Cleave 1931), and nine longitudinal
rows of 5–7 hooks in A. opsariichthydis (Yamaguti 1935); the
blade of the longest hook is 94–161 µm long in A. aculeatus
(Van Cleave 1931), and 72–150 µm long in A. opsariichthy-
dis (Yamaguti 1935). e specimens reported as A. aculea-
tus from Lake Biwa possessed 8–10 longitudinal rows of 3–6
hooks (Kataoka and Momma 1933, 1934), fewer hooks per
row than Van Cleave (1931) reported. A clarication of the
taxonomic status of A. aculeatus vis-à-vis A. opsariichthydis
is necessary but is beyond the scope of this paper.
No similar suggestion of synonymy applies to two other
species of Echinorhynchus Zoega in Müller, 1776: E. cotti
and E. parasiluri Fukui, 1929. Like A. opsariichthydis, E. cotti
is a common parasite of sh in the Lake Biwa basin (Amin
et al. 2007; see Table 1 herein), but there is only one record
of E. parasiluri from this basin (Fukui 1929). Both species
are easily dierentiated from each other by the proboscis ar-
mament: 16–20 longitudinal rows of 11–13 hooks in E. cotti
(Yamaguti 1935, 1939) versus 22–26 longitudinal rows of
10–11 hooks in E. parasiluri (Fukui 1929). Fukui (1929) re-
ported the host of E. parasiluri as Amur catsh Silurus aso-
tus, but because two other, endemic species of Silurus were
later described from Lake Biwa, and the identity of Fukui’s
sh could not be checked, this host was later reported as “Si-
lurus sp. (presumably S. asotus Linnaeus, 1758)” (Amin et
al. 2007). Amin et al. (2007) did not nd E. parasiluri in ve
specimens of S. asotus and two specimens of rocky catsh S.
lithophilus (Tomoda, 1961) but these authors attributed the
absence of infection to the small number of sh examined.
Acanthocephalus gotoi Van Cleave, 1925 was reported,
similarly to A. aculeatus, only once in the late 1930s in the
Lake Biwa basin (Yamaguti 1939; see Table 1 herein). Since
its original description from Japanese eel Anguilla japonica
Temminck and Schlegel, 1846 in Tokyo, Japan (Van Cleave
1925), this acanthocephalan has been found in several
freshwater sh, especially from A. japonica, in various parts
of Japan (Yamaguti 1935, 1939; Fukui and Morisita 1936;
Katahira and Nagasawa 2014; Nagasawa unpublished data),
so it cannot be said to be rare in Japan. e current appar-
ent absence of A. gotoi in the Lake Biwa basin is, therefore,
unusual. One reason for this absence may be that the wild
population of A. japonica disappeared in the basin aer
1964 when the Amagase Dam was completed in the Uji
River, which ows, rst as the Seta River, from Lake Biwa.
As a result, the acanthocephalan might have lost its major
(perhaps preferred) host (A. japonica), resulting in its disap-
pearance from the basin. Since the dam prevents juveniles
of A. japonica from migrating upstream to the lake (Anony-
mous 2007), no wild population of eels has existed in Lake
Biwa and its watershed since the mid-1960s. Currently, A.
japonica is found in the lake, released by shermen aer
having been raised at sh farms. No infection by A. gotoi
was actually detected in recently collected individuals of
A. japonica in the Lake Biwa basin (Amin et al. 2007). is
may imply, in other words, that A. gotoi needs A. japonica to
sustainably maintain its population even though this worm
can infect various freshwater sh.
Unidentied acanthocephalans were found by Fujita
(1927) in eight species of sh in Lake Biwa (see Table 1).
ese sh were reported as “the most common in Lake
Biwa” (Fujita 1927: 39), but yamato char Salvelinus leu-

78 K. Nagasawa and M. Nitta
comaenis japonicus Oshima, 1961 (as S. pluvius (Hilden-
dorf, 1876)), one of the sh examined by him, could not
have been caught in the lake proper, because this species
is restricted to the upper reaches of rivers in the lake basin
(Shiga-Kenritsu Biwako-Bunkakan 1980; Anonymous 1996,
2004). e sh parasite surveys on which Amin et al. (2007)
was based included as many as 62 species of sh from Lake
Biwa and its tributaries, but not S. leucomaenis japonicus.
An appraisal of its acanthocephalan parasites is desirable.
Another sh from which Fujita (1927) reported an un-
identied acanthocephalan was pond loach Misgurnus an-
guillicaudatus (Cantor, 1842), but this sh is rare in the lake
proper and occurs in shallow swamps, ponds, brooks, and
paddy elds around it (Shiga-Kenritsu Biwako-Bunkakan
1980). Knowledge of the acanthocephalan fauna of M. an-
guillicadatus is quite limited in Japan, with only the descrip-
tion of the pomphorhynchid (originally referred to as an
echinorhynchid) Tenuiproboscis misgurni Yamaguti, 1935
from an unknown locality (Yamaguti 1935). As Amin et al.
(2007: 250) pointed out, M. anguillicaudatus is a future tar-
get for better understanding the sh acanthocephalan fauna
of Japan as well as the Lake Biwa basin.
As a result of the large-scale parasitological survey of sh
in and around Lake Biwa on which Amin et al. (2007) was
based, information on the comparative host utilization, oc-
currence, and maturity between two seasons (spring and
autumn) and on geographical distribution of sh acantho-
cephalans in this region is now available. Of the three most
common acanthocephalans (viz., A. opsariichthydis, E. cotti,
and P. samegaiensis) in this region, E. cotti has been sug-
gested to be restricted to “Lake Biwa proper, including river
mouths” (Amin et al. 2007: 251, g. 1). is acanthocepha-
lan was originally described by Yamaguti (1935) from Japa-
nese uvial sculpin Cottus pollux Günther, 1873 in Shiga
Prefecture (in the Lake Biwa basin) and later collected by
the same author (Yamaguti 1939) from the same host spe-
cies (C. pollux) in the lake. Two species of the genus Cottus
Linnaeus, 1758, C. pollux and C. reinii Hilgendorf, 1879 (the
latter called utsusemi-kajika), occur in the Lake Biwa basin,
but their distribution ranges do not overlap: C. pollux in-
habits the upper reaches of rivers, while C. reinii is distrib-
uted in the lake and the lower reaches of rivers (Anonymous
1996, 2004; Fujioka and Kido 1998; Fujioka et al. 2014).
us, the host reported by Yamaguti (1939) was denitely
not C. pollux but C. reinii, and as suggested by Amin et al.
(2007), the host in the original description (Yamaguti 1935)
was perhaps also C. reinii. e observed high proportion
(63%) of gravid females of E. cotti in C. reinii (Amin et al.
2007: table 1) implies that this acanthocephalan should be
able to use its close relative C. pollux as a preferred host as
well. However, seven specimens of C. pollux from the Seri
River examined in November, 2000, in the course of the
above-mentioned surveys were not infected (Mark J. Grygi-
er, Lake Biwa Museum, personal communication).
Little information is available as to the life history of sh
acanthocephalans in the Lake Biwa basin. Ito (1959) found
larval acanthocephalans, identied as Acanthocephalus sp.
(misspelled as Acanthocepharus sp.) in the gammarid am-
phipod Gammarus sp. (misspelled as Gonmarus sp. and
Ganmarus sp.) and the asellid isopod Asellus hilgendori (as
A. nipponensis Nicholas, 1929) at a trout hatchery. However,
two species of acanthocephalan, Acanthocephalus opsariich-
thydis and Pseudorhadinorhynchus samegaiensis, and the an-
isogammarid amphipod Jesogammarus (Annanogammarus)
uvialis Morino, 1985 (as J. uvialis) are known to occur at
this hatchery (Nakajima et al. 1975; Nakajima and Egusa
1975a, 1975b for the acanthocephalans: Morino 1985; Ku-
sano 2009 for the amphipod), thus Ito’s (1959) work needs
a re-study.
Without providing any information on the larval mor-
phology of E. cotti, sampling locality, or date, Shimazu
(1999) stated that the intermediate host of E. cotti in Lake
Biwa is the anisogammarid amphipod Jesogammarus (An-
nanogammarus) naritai Morino, 1985 (as J. naritai). is
amphipod is found in coastal waters of the lake throughout
the year (Narita 1976; Morino 1985, 1994). A detailed life-
history study of E. cotti using this amphipod intermediate
host is desired in the eld and the laboratory. In addition,
another species of anisogammarid amphipod Jesogammarus
(Annanogammarus) annandalei (Tattersall, 1922) occurs in
oshore, deeper waters of Lake Biwa (Narita 1976; Morino
1985, 1994; Ishikawa and Urabe 2002). It is thus important
to search for larval E. cotti in material of this amphipod as
well, and assess a dierence in host utilization by the acan-
thocephalan in these congeneric amphipods at various
depths in the lake.
Asakawa and Nishino (2011) reported 10 juveniles of a
polymorphid acanthocephalan collected in a free condition
from a benthos sample taken in Lake Biwa. ese authors
stated that the juveniles resembled an acanthocephalan of
aquatic-birds, Polymorphus (Polymorphus) strumosoides
Lundström, 1942, but based on the morphological features
given by the authors, they seem almost identical with Pseu-
dorhadinorhynchus samegaiensis. e only dierence is the
number of hook rows on the proboscis, i.e., 16 rows in the
benthic-caught juveniles (Asakawa and Nishino 2011) and
13–14 rows in P. samegaiensis (Nakajima and Egusa 1975b;
Amin et al. 2007). It is desirable to re-examine Asakawa and
Nishino’s (2011) specimens to ascertain their identity at the
generic and specic levels.
Amin et al. (2007) examined well-developed cystacanths
of S. hispida from the body cavity of six species of sh in the
Lake Biwa basin. e nal hosts of this acanthocephalan
are sh-eating birds (García-Verela et al. 2012), and the sh
reported by Amin et al. (2007) are considered to serve as
paratenic hosts for the parasite. Yamaguti (1935, 1939) and
Katahira and Nagasawa (2014) provide the other known sh
hosts from Japan. It is necessary to discover the rst inter-
mediate hosts of this species (e.g., amphipods; see Lisitsyna
2011) in order to clarify its life cycle in the basin. No infor-
mation is yet available on the life history of the two quad-
rigyrids, Acanthogyrus (Acanthosentis) alternatspinus Amin,
2005 and A. (A.) parareceptaclis Amin, 2005, which were
recently described from the basin (Amin 2005). Acantho-
gyrus (A.) alternatspinus was from an introduced sh host,
Rhodeus ocellatus ocellatus (Kner, 1866), but it is unknown

A sh parasite from the Lake Biwa basin 79
whether this acanthocephalan is an introduced species.
In conclusion, the Lake Biwa basin is the best studied
body of freshwater in Japan as concerns the sh acantho-
cephalan fauna, and no other lake basin in Japan has been
reported to bear such a rich fauna of these parasites. Nev-
ertheless, the past investigations of sh acanthocephalans
in this basin have focused on their taxonomy. As reviewed
above, no paper except Amin et al. (2007) has treated their
ecology and host-parasite relationships, and much remains
poorly understood about their life cycles. More work is
needed on various aspects of the biology of sh acantho-
cephalans in the Lake Biwa basin.
Acknowledgments
We thank Tomohiko Morimune, Taiki Ito, and Kazuhiro
Tanaka, Faculty of Agriculture, Kinki University, for as-
sistance in sh sampling. We are also grateful to Yasuhiro
Fujioka, Lake Biwa Museum (LBM), for support during the
study. anks go to Mark J. Grygier, LBM, and two anony-
mous reviewers for valuable comments to improve the man-
uscript.
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