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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

Authors:
  • Setouchi Parasite Biodiversity Laboratory

Abstract and Figures

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.
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© 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 basins 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°1954N,
136°244E) 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 Heidenhains 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 Grygiers 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 lakes 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.
References
Amin, O. M. 1985. Classication. Pp. 27–72. In: Crompton, D. W. T.
and Nickol, B. B. (Eds) Biology of the Acanthocephala. Cambridge
University Press, Cambridge.
Amin, O. M. 2005. Occurrence of the subgenus Acanthosentis Verma &
Datta, 1929 (Acanthocephala: Quadrigyridae) in Japan, with the
description of Acanthogyrus (Acanthosentis) alternatspinus n. sp.
and A. (A.) parareceptaclis n. sp. from Lake Biwa drainage shes
and a key to the species of the subgenus. Systematic Parasitology
60: 125–137.
Amin, O. M. 2013. Classication of the Acanthocephala. Folia Parasito-
logica 60: 273–305.
Amin, O. M., Nagasawa, K., and Grygier, M. J. 2007a. Host and sea-
sonal distribution of sh acanthocephalans from Lake Biwa basin,
Japan. Comparative Parasitology 74: 244–253.
Amin, O. M., Heckman, R., and Standing, M. D. 2007b. e structural-
functional relationship of the para-receptacle structure in Acan-
thocephala. Comparative Parasitology 74: 383–387.
Anonymous. 1972. [On the occurrence and countermeasures of sh
diseases at Mori Branch]. Pp. 132–150. In: Showa 46-nendo Jigyo
Seisekisho [Annual Report for Fiscal Year 1992]. Hokkaido Fish
Hatchery, Sapporo. [In Japanese]
Anonymous. 1996. Heisei 67-nendo Biwako oyobi Kasen no Gyorui to
no Seisoku Jokyo Chosa Hokokusho [Survey Report for Fiscal Years
19941995 on the Habitats of Fish, etc. in Lake Biwa and Rivers].
Shiga Prefectural Fishery Experiment Station, Hikone, 176 pp. [In
Japanese]
Anonymous. 2004. Heisei 14–15-nendo Biwako oyobi Kasen no Gyorui
to no Seisoku Jokyo Chosa Hokokusho [Survey Report for Fiscal
Years 2002–2003 on the Habitats of Fish, etc. in Lake Biwa and Riv-
ers]. Shiga Prefectural Fishery Experiment Station, Hikone, 138
pp. [In Japanese]
Anonymous. 2007. Amagase Damu Gyorui to Sojo-koka Eikyo Hyoka
ni kansuru Hokokusho [Report of Evaluation of the Impact of the
Amagase Dam on Upstream and Downstream Migration of Fish,
etc.]. e Investigative Commission on Evaluation of the Impact
of the Amagase Dam on Upstream and Downstream Migration of
Fish, etc., Osaka, 380 pp. [In Japanese]
Araki, J. 1999. [Acanthocephalans from Japan]. Pp. 147–162. In: Otsu-
ru, M., Kamegai, S. and Hayashi, S. (Eds) Nihon ni okeru Kisei-
chugaku no Kenkyu [Progress of Medical Parasitology in Japan],
Vol. 6. Meguro Parasitological Museum, Tokyo. [In Japanese]
Araki, J. 2003. Acanthocephalans from Japan. Pp. 147–159. In: Otsuru,
M., Kamegai, S., and Hayashi, S. (Eds) Progress of Medical Para-
sitology in Japan, Vol. 7. Meguro Parasitological Museum, Tokyo.
Asakawa, M. and Nishino, M. 2011. A case report of acanthocephalans
found in dredging samples derived from Lake Biwa, Japan. Jour-
nal of Rakuno Gakuen University 35: 91–94. [In Japanese with
English abstract]
Awakura, T. 1972. Studies on acanthocephaliasis of the salmonid shes
infected by Acanthocephalus minor Yamaguti, 1935. Scientic Re-
ports of the Hokkaido Fish Hatchery 27: 1–12. [In Japanese with
English abstract]
Awakura, T. 1973. [Acanthocephaliasis]. Uo to Mizu 8: 12–14. [In
Japanese]
Awakura, T. 1980. On the parasites and parasitic diseases of salmonid
sh in Hokkaido. Fish Pathology 14: 207–209. [In Japanese with
English abstract]
Awakura, T. 1989. Parasitology of masu salmon, Oncorhynchus masou,
in northern Japan. Physiology and Ecology Japan, Special Volume
1: 605–614.
Awakura, T., Tanaka, T., Sakai, K., and Koide, N. 1984. [Survey of
pathogens in masu and amago salmon in rivers. 1. Masu salmon
of Hokkaido, 2. masu salmon of Honshu (the Sea of Japan side)].
Pp. 3–12. In: Showa 5557-nendo Kinkai-gyogyo-shigen no Kagyo-
ka Sisutemu no Kaihatsu ni kansuru Sogokenkyu (Marin Rantingu
Keikaku) Puroguresu Repoto, Byogai Bojo Gijutsu [Progress Report
for Fiscal Years 1980–1982 on the Comprehensive Research Project
(Marine Launching Plan) on the Development of a Domesticat-
ing System Using Inshore Fishery Resources]. National Research
Institute of Aquaculture, Fisheries Agency of Japan, Tamaki. [In
Japanese]
Fujioka, Y. and Kido, Y. 1998. Distribution and growth of Cottus reinii
from Lake Biwa. Pp. 32–33. In: Heisei 9-nendo Shiga-ken Suisan
Shikenjo Jigyo Hokoku [Annual Report of the Shiga Prefectural
Fishery Experiment Station for Fiscal Year 1997]. Shiga Prefectural
Fishery Experiment Station, Hikone. [In Japanese]
Fujioka, Y., Kido, Y., Uenishi, M., Yoshioka, M., and Kashiwagi, M.
2014. Distribution of Cottus reinii and Cottus pollux in rivers
around Lake Biwa, Japan. Biogeography 16: 31–37.
Fujita, T. 1927. [Helminths parasitic in shes in Lake Biwa]. Dobutsu-
gaku Zasshi 39: 39–45, pl. I. [In Japanese]
Fukui, T. 1929. On some Acanthocephala found in Japan. Annotationes
Zoologicae Japonenses 12: 255–270.
Fukui, T. 1962. Acanthocephala of Japan and its vicinity. Bulletin of the
Yokohama Municipal University Society, Natural Science 13: 127–
144. [In Japanese]
Fukui, T. 1965. [General remarks on Acanthocephala]. P. 468. In:
Okada, Y., Uchida, S., and Uchida, T. (Eds), New Illustrated Ency-
clopedia of the Fauna of Japan, Volume I. Hokuryukan, Tokyo. [In
Japanese]
Fukui, T. 1973. Acanthocephala. Pp. 272–276. In: Uéno, M. (Ed.) Tam iji
Kawamura’s Freshwater Biology of Japan. Hokuryukan, Tokyo. [In
Japanese]
Fukui, T. and Morisita, T. 1936. ree new species of Acanthocephala
from Japan. Dobutsugaku Zasshi 48: 759–764. [In Japanese with
English abstract]
Fukui, T. and Morisita, T. 1937. [On some species of Acanthoceph-
ala from Japan]. Zikken Igaku Zasshi 21: 1841–1848, 1 pl. [In
80 K. Nagasawa and M. Nitta
Japanese]
Funao, T., Kanao, S., and Sawada, H. 2010. Freshwater sh fauna of the
Ezura River and inux irrigation ditch system, Shiga Prefecture,
central Japan. Biology of Inland Waters 25: 87–95. [In Japanese
with English abstract]
García-Verela, M., Anzar, F. J., Rodrígues, R. P., and Pérez-Pornce de
León, G. 2012. Genetic and morphological characterization of
Southwellina hispida Van Cleave, 1925 (Acanthocephala: Polymor-
phidae), a parasite of sh-eating birds. Comparative Parasitology
79: 192–201.
Golvan, Y. J. 1969. Systématique des acanthocéphales (Acanthocephala
Rudolphi 1801), l’ordre des Palaeacanthocephala Meyer 1931, la
super-famille des Echinorhynchidea (Cobbold 1876) Golvan et
Houin 1963. Mémoirs du Muséum National d’Histoire Naturelle,
Série A, Zoologie 47: 1–373.
Golvan, Y. J. 1994. Nomenclature of the Acanthocephala. Research and
Reviews in Parasitology 54: 135–205.
Grygier, M. J. 2004. [Clarifying the parasitofauna of Lake Biwa]. Pp.
273–284, 341–342. In: Nagasawa, K. (Ed.) Aquaparasitology in the
Field in Japan. Tokai University Press, Hadano. [In Japanese]
Harada, I. 1935. Zur Acanthocephalenfauna von Japan. Memoirs of the
Faculty of Science and Agriculture, Taihoku Imperial University
14: 7–23.
Homan, G. L. 1997. Parasites of North American Freshwater Fishes;
with a foreword by E. H. Williams, Jr., Second Edition. Cornell Uni-
versity Press, Ithaca, New York, xx + 539 pp.
Horie, S. (Ed.) 1984. Lake Biwa. Monographiae Biologicae, Vol. 54. Dr.
W. Junk Publishers, Dordrecht, xi + 654 pp.
Hosoya, K. 2013. Cyprinidae. Pp. 308–327. In: Nakabo, T. (Ed.) Fishes of
Japan with Pictorial Keys to the Species, ird Edition. Tokai Uni-
versity Press, Hadano. [In Japanese]
Ishikawa, T. and Urabe, J. 2002. Population dynamics and production of
Jesogammarus annandalei, an endemic amphipod, in Lake Biwa,
Japan. Freshwater Biology 47: 1935–1943.
Ito, I. 1959. [On some observations of an acanthocephalan (Acantho-
cepharus [sic]) parasitizing rainbow trout, rst report]. Shiga-ken
Samegai Yoshoku Shikenjo Hokoku 2: 32–33. [In Japanese]
Katahira, H. and Nagasawa, K. 2014. Helminths from the giant mottled
eel Anguilla marmorata Quoy & Gaimard in Japan, with a descrip-
tion of Acanthocephalus longiacanthus n. sp. (Acanthocephala:
Echinorhynchidae). Systematic Parasitology 88: 91–102.
Kataoka, N. and Momma, K. 1933. [Notes on parasitic helminthes of
ayu]. Pp. 257–275. In: Kataoka, N. (Ed.) Yogyo to Noen [Fish farm-
ing and agricultural farm]. Privately published by Arimatsu, M.,
Nagao, Hyogo. [In Japanese]
Kataoka, N. and Momma, K. 1934. Helminthes from the salmonoid
sh, Plecoglossus altivelis T. & S. Bulletin of the Japanese Society of
Scientic Fisheries 3: 59–64.
Kataoka, N. and Momma, K. 1937. Helminthes from the salmonoid
sh, Plecoglossus altivelis T. & S. Pp. 67–72. In: Anonymous (Ed.)
Collected Papers of the Faculty of Medicine, Osaka Imperial Uni-
versity. Faculty of Medicine, Osaka Imperial University, Osaka.
[Cited from Golvan (1969); actually, a repackaging of Kataoka and
Momma (1934)]
Kawamura, T. 1918. Tansui Seibutsugaku, Jokan [Freshwater Biology,
Vol. 1]. Shokabo, Tokyo, 362 pp. [In Japanese]
Kawanabe, H., Nishino, M., and Maehata, M. (Eds) 2012. Lake Biwa: In-
teractions between Nature and People. Springer, Dordrecht, xvii +
744 pp., 12 color pls.
Kurawaka, K. 1977. Cephalic lateral-line systems and geographical dis-
tribution in the genus Tribolodon (Cyprinidae). Japanese Journal
of Ichthyology 24: 167–175.
Kusano, H. 2009. Geographical distribution and habitats of a spring-
dwelling amphipod, Jessogammarus uvialis Morino (Amphipo-
da). Japanese Journal of Limnology 69: 223–236. [In Japanese with
English abstract]
Lisitsyna, O. I. 2011. First ndings of acanthocephalans Arhythmorhyn-
chus invaginabilis, Southwellina hispida (Acanthocephales [sic],
Polymorphidae), Plagiorhynchus (Plagiorhynchus) odhneri (Acan-
thocephales [sic], Plagiorhynchidae) in the intermediate hosts.
Vestnik Zoologii 45: e-1–e-8.
Maruyama, T., Fujii, K., Kijima, T., and Maeda, H. 1987. Gaikoku san
Shin Gyoshu no Donyu Keika [Progress of Introduction of New Fish
from Other Countries]. Fisheries Resources Department, Research
Division, Fisheries Agency, Tokyo, and Aquaculture Institute,
Fisheries Agency, Ise, Mie, 147 pp., 4 gs., 1 unnumbered table, 2
tables, 8 pls. [In Japanese]
Matsumoto, K. 1973. Isopoda. Pp. 473–488. In: Uéno, M. (Ed.) Tamij i
Kawamura’s Freshwater Biology of Japan. Hokuryukan, Tokyo. [In
Japanese]
Morino, H. 1985. Revisional studies on Jesogammarus–Annanogamma-
rus group (Amphipoda: Gammaroidea) with descriptions of four
new species from Japan. Publications of Itako Hydrobiological
Station 2: 9–55.
Morino H. 1994. e phylogeny of Jesogammarus species (Amphipoda:
Anisogammaridae) and life history features of two species endem-
ic to Lake Biwa, Japan. Archiv für Hydrobiologie-Beihe Ergeb-
nisse der Limnologie 44: 257–266.
Nagasawa, K. and Grygier, M. J. 2011. Acanthocephala. P. 1464. In: Ti-
moshkin, O. A. (Ed.) Index of Animal Species Inhabiting Lake Bai-
kal and its Catchment Area: Volume II. Basins and Channels in the
South of East Siberia and North Mongolia. Nauka, Novosibirsk.
[Part of Timoshkin et al. 2011]
Nagasawa, K., Ishino, K., and Egusa, S. 1982. Occurrence of Acantho-
cephalus minor (Acanthocephala) in two types of the goby, Chae-
nogobius annularis. Japanese Journal of Ichthyology 29: 229–231.
Nagasawa, K., Urawa, S., and Awakura, T. 1987. A checklist and bibliog-
raphy of parasites of salmonids of Japan. Scientic Reports of the
Hokkaido Salmon Hatchery 41: 1–75.
Nagasawa, K., Umino, T., and Grygier, M. J. 2007. A checklist of the
parasites of ayu (Plecoglossus altivelis altivelis) (Salmoniformes:
Plecoglossidae) in Japan (1912–2007). Journal of the Graduate
School of Biosphere Science, Hiroshima University 46: 59–89.
Nakabo, T. (Ed.) 2013. Fishes of Japan with Pictorial Keys to the Spe-
cies. ird Edition. Tokai University Press, Hadano. 2428 pp. [In
Japanese]
Nakajima, K. and Egusa, S. 1975a. Acanthocephalus opsariichthydis
Yamaguti, 1935, from cultured rainbow trout, Salmo gairdnerii
irideus, in Japan. Fish Pathology 10: 53–57. [In Japanese]
Nakajima, K. and Egusa, S. 1975b. Pseudorhadinorhynchus samegaien-
sis n. sp. (Acanthocephala), from cultured rainbow trout, Salmo
gairdnerii in Japan. Fish Pathology 10: 58–68. [In Japanese with
English abstract]
Nakajima, K., Oota, T., and Egusa, S. 1975. Some aspects of the para-
sitism and the susceptibility to some chemicals of the adult of
the spiny-headed worms in 2 years old rainbow trout kept at
Samegai Trout Experimental Station. Fish Pathology 10: 48–52.
[In Japanese]
Narita, T. 1976. Occurrence of two ecological forms of Anisogammarus
annandalei (Tattersall) (Crustacea: Amphipoda) in Lake Biwa.
Physiology and Ecology Japan 17: 551–556.
Natsuhara, Y. and Akiyama, Y. 2012. Comparison of sh assemblages in
drainage ditches of rice elds in Lake Biwa basin, Japan. Journal of
Environmental Information Science 40: 159–166.
Nishino, M. 2012. A list of Acanthocephala in Lake Biwa. Pp. 579–581.
In: Kawanabe, H., Nishino, M., and Maehata, M. (Eds) Lake Biwa:
Interactions between Nature and People. Springer, Dordrecht.
Nishino, M. and Watanabe, N. C. 2000. Evolution and endemism in
A sh parasite from the Lake Biwa basin 81
Lake Biwa, with special reference to its gastropod mollusc fauna.
Advances in Ecological Research 31: 151–180.
Petrochenko, V. I. 1956. Acanthocephala of Domestic and Wild Animals.
Volume I. Izdatel’stvo Akademii Nauk SSSR, Moscow. [English
translation by Israel Program for Scientic Translations, Keter
Press, Jerusalem, 1971, 465 pp.]
Sakai, H., 1995. Life-histories and genetic divergence in three species of
Tribolodon (Cyprinidae). Memoirs of the Graduate School of Fish-
eries Sciences, Hokkaido University 42: 1–98.
Shiga-Kenritsu Biwako-Bunkakan (Ed.) 1980. Kokoku Biwako no Saka-
na-tachi [Fishes of Lake Biwa]. Dai-ichi Hoki, Tokyo. 177 pp. [In
Japanese]
Shimazu, T. 1999. Acanthocephalans of freshwater shes in Japan:
a review. Journal of Nagano Prefectural College 54: 21–29. [In
Japanese with English abstract]
Timoshkin, O. A., Grygier, M. J., Wada, E., Nakai, K., Nishino, M., Gen-
kal, S. I., Biserov, V. I., Gagarin, V. G., Semernoy, V. P., Jankowski,
A. W., Stepanjants, S. D., Tsalolikhin, S. Ya., Starobogatov, Ya. I.,
Alexeev, V. R., Tuzovskij, P. V., Okuneva, G. L., Sheveleva, N. G.,
Pomazkova, G. I., Arov, I. V., Mazepova, G. F., Janz, H., Obolkina,
L. A., Chernyshev, A. V., Morino, H., Matsuda, M., Ohtsuka, T.,
Kawakatsu, M., Maehata, M., Masuda, Y., Faubel, A., Yahiro, K.,
Hirasawa, R., Tuji, A., Kusuoka, Y., Kameda, K., Ishida, T., Itoh,
T., Ichise, S., Wakabayashi, T., Okubo, I., Seki, Sh., Nagasawa, K.,
Ogawa, K., Masunaga, K., and Gamo, J. 2011. Biodiversity of Lake
Biwa: new discoveries and future potential. Pp. 1439–1513. In : Ti-
moshkin, O. A. (Ed.) Index of Animal Species Inhabiting Lake Bai-
kal and its Catchment Area: Volume II. Basins and Channels in the
South of East Siberia and North Mongolia. Nauka, Novosibirsk.
Tomikawa, K. and Morino, H. 2012. An annotated inventory with a key
of freshwater Amphipoda (Crustacea) from Japan. TAXA, Pro-
ceedings of the Japanese Society of Systematic Zoology 32: 39–51.
[In Japanese with English abstract]
Uchida, T. 1979. Aschelminthes. Pp. 147–150. In: Imajima, M. and
Takeda, M. (Eds) Illustrated Encyclopedia of the Fauna of Japan.
Newly Compiled. Hokuryukan, Tokyo. [In Japanese]
Van Cleave, H. J. 1925. Acanthocephala of Japan. Parasitology 17: 149–
156.
Van Cleave, H. J. 1931. Acanthocephala from Japan. II. Two new
species of the genus Acanthocephalus. Annotationes Zoologicae
Japonenses 13: 33–37.
Yamada, M. 1962. Acanthocephala. Pp. 243–280. In: Uchida, T. (Ed.)
Keito Dobutsugaku, Dai 4 kan. Taikei-dobutsu [Systematic Zoology,
Vol. 4. Aschelminthes]. Nakayama Shoten, Tokyo. [In Japanese]
Yamaguti, S. 1935. Studies on the helminth fauna of Japan. Part 8.
Acanthocephala, I. Japanese Journal of Zoology 6: 247–278.
Yamaguti, S. 1939. Studies on the helminth fauna of Japan. Part 29.
Acanthocephala, II. Japanese Journal of Zoology 8: 317–351, pls.
XLI–XLIX.
Yamaguti, S. 1963. Systema Helminthum. Volume IV. Acanthocephala.
Interscience Publishers, New York, viii + 423 pp.
Yokoyama, H. and Nagasawa, K. 2014. Synopsis of Japanese names of
the parasites from cultured shes and shellshes in Japan. Bio-
sphere Science 53: 73–97. [In Japanese with English abstract]
... The specimens collected in this study fit the morphology of A. longiacanthus described by Katahira and Nagasawa (2014). This acanthocephalan was recently described from Anguilla marmorata (type host) [Japanese name: ō-unagi] in the Renjōji River, Ehime Prefecture, and this fish is the only known host (Katahira and Nagasawa, 2014 Acanthocephalus minor Yamaguti, 1935 ( Female (based on 2 specimens with ovarian balls with a list of the known parasites of Rhinogobius spp. of Japan (1935Japan ( -2018 広島大学総合博物館研究報告Bulletin of the Hiroshima University (Nagasawa et al., 1982); and O. obscura in an irrigation canal, Shiga Prefecture (Nagasawa and Nitta, 2015). The present collection of A. minor from Rhinogobius flumineus from Hiroshima Prefecture represents a new host and a new prefectural record for the acanthocephalan. ...
... All the specimens of A. minor reported herein were found in the rectum of the fish. Such site specificity by the species has been noticed by Nagasawa et al. (1982) and Nagasawa and Nitta (2015). (Schmidt and Kunz, 1967;Schmidt, 1985;Lisitsyna, 2011 (Perciformes: Cottidae) in Lake Biwa, Shiga Prefecture (Nagasawa and Grygier, 2011); Anguilla marmorata [ō-unagi] in the Renjōji River, Ehime Prefecture (Katahira and Nagasawa, 2014); and A. marmorata on Okinoerabu-jima Island in Kagoshima Prefecture (Nagasawa and Kan, 2017 (Podicipediformes: Podicipedidae), in the latter p r e f e c t u r e ( Ya m a g u t i , 1 9 3 5 , 1 9 3 9 a ) . ...
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Four species of acanthocephalans are reported from gobies of the genus Rhinogobius in western and central Japan: Acanthocephalus gotoi Van Cleave, 1925 from Rhinogobius similis in the Kamo River (Hiroshima Prefecture) and Rhinogobius sp. OR (=orange type) in the Sōja River (Ehime Prefecture) and the Hiwatashi River (Kōchi Prefecture); Acanthocephalus longiacanthus Katahira and Nagasawa, 2014 from Rhinogobius nagoyae and Rhinogobius sp. OR in the Tenchi River (Hiroshima Prefecture), Rhinogobius fluviatilis in the Kamo River, and Rhinogobius sp. OR in the Sōja and Hiwatashi rivers; Acanthocephalus minor Yamaguti, 1935 from Rhinogobius flumineus in the Aruji River (Hiroshima Prefecture); and Southwellina hispida (Van Cleave, 1925) from Rhinogobius flumineus in the Aruji River and the Shika River (Kyōto Prefecture). All these collections represent new host records for the acanthocephalans. New prefecture records are A. gotoi and A. longiacanthus from Hiroshima and Kochi prefectures, and A. minor and S. hispida from Hiroshima Prefecture. Based on the previous and present papers published between the years 1935 and 2018, 48 nominal and some unidentified species of the parasites have been reported from the Japanese Rhinogobius spp. The nominal species include: 3 species in the Myxozoa (Cnidaria); 1 species in the Monogenea; 16 species in the Trematoda; 4 species in the Cestoda (all Platyhelminthes); 3 species in the Nematoda; 5 species in the Acanthocephala; 15 species in the Bivalvia (Mollusca); and 1 species in the Copepoda (Arthropoda).
... The former species was originally described by Nakajima and Egusa (1975b) based on specimens from rainbow trout Oncorhynchus mykiss (Walbaum, 1729) (as Salmo gairdnerii irideus Gibbons, 1885) (Salmoniformes: Salmonidae) at the Samegai Trout Experimental Station, Shiga Prefecture, west-central Japan. This station is located on the Nyuu River within the watershed of Lake Biwa, which is the largest (640 km 2 ) and oldest (over four million years old) lake in Japan (Horie 1984), and the acanthocephalan has so far been reported only from Lake Biwa and its watershed (Grygier 2004(Grygier , 2013Amin et al. 2007;Nagasawa and Nitta 2015). ...
... Recently, Nagasawa and Nitta (2015) suggested that P. samegaiensis is not endemic to the Lake Biwa basin but also occurs in other areas of Japan, under the assumption that a widely distributed cyprinid, the big-scaled redfin Tribolodon hakonensis (Günther, 1877), is its usual definitive host, as Amin et al.'s (2007) The prevalence and mean abundance of larval P. samegaiensis were significantly higher in the amphipods from the upstream part than in those from the farther down-stream of the stream flowing through the Samegai Trout Experimental Station (Table 1). This is probably due to the fact that adult rainbow trout Oncorhynchus mykiss were abundantly cultured near the former site. ...
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Cystacanths and acanthellae of the illiosentid acanthocephalan Pseudorhadinorhynchus samegaiensis Nakajima and Egusa, 1975 are described from the anisogammarid amphipod Jesogammarus (Annanogammarus) fluvialis Morino, 1985 in a stream at the Samegai Trout Experimental Station, the type locality of the acanthocephalan, in the Lake Biwa basin, Shiga Prefecture, west-central Japan. This amphipod is herein regarded as an intermediate host of P. samegaiensis. This is the first description of developmental stages of any member of the genus Pseudorhadinorhynchus Achmerov and Dombrovskaja-Achmerova, 1941. Since J. (A.) fluvialis does not occur in the Lake Biwa proper but two other congeners, J. (A.) annandalei (Tattersall, 1922) and J. (A.) naritai Morino, 1985 , inhabit the lake, it is suggested that P. samegaiensis uses one or both of the latter two amphipods as its intermediate host(s) in the lake.
Book
Although, the first edition had a similar focus, more than five years have passed since its publication and the biological and social circumstances of the lake have drastically changed due to, for example, the further expansion of alien species, the decrease of indigenous species, the progress of integrated watershed management by the Union of the Kansai Government which was established in 2010, the legislation of the Conservation and Restoration Act of Lake Biwa in 2015 and more. The new edition will therefore feature updated and new information on the above and more topics as well as updated and revised data based on the latest research. Inventories of respective taxa, especially those of small animals, are also revised based on the latest studies. Furthermore, this volume covers the characteristics of the biota of this ancient lake, but at the same time, it will also approach it as a ‘culture ancient lake’. Other topics also include water pollution, lakeshore development, the effects of global warming in the past and present, the influence of people, and countermeasures by local and national governments. Moreover, the volume also provides a comprehensive view on the future of Lake Biwa and that of its residents. Miraculously enough, this ancient lake has kept its water quality clear even until today despite the fact of more than 1.4 million people living on its shores. Finally, the book also gives indispensable information to those engaged in improving and conserving water regimes of lakes and other water bodies all over the world and to those interested in the culture and history of Japan. Lake Biwa is not only one of the rarest ancient lakes of the world, but the people’s involvement with the lake also goes back a long way. This is shown in the diverse culture developed in this area and in the various archaeological finds that date back as early as the Jomon Period, nearly 10.000 years ago. Today Lake Biwa fulfills an important role as a water resource by providing domestic, commercial, industrial, and agricultural water for over 14 million residents living around the Lake Biwa-Yodo River drainage basin. This updated volume focuses on the geological and biological features of the lake as well as on the long-term interactions between the people and the lake.
Article
A new species of acanthocephalan, Pseudorhadinorhynchus samegaiensis (Echinorhynchidea, Illosentidae), was found from the intestine of 2 years old rainbow trout cultured at Samegai Trout Experimental Station, Shiga Prefecture, in May, 1974. Sixty-seven males and 101 females were collected from 29 of 35 fishes examined. Acanthocephalans were fixed in 70% ethanol under pressure, stained with Heidenhain's hematoxylin and mounted in balsam. Type specimens are deposited in the collection of the National Science Museum, Tokyo. © 1975, The Japanese Society of Fish Pathology. All rights reserved.