Content uploaded by Kazuya Nagasawa
Author content
All content in this area was uploaded by Kazuya Nagasawa on Jan 29, 2023
Content may be subject to copyright.
119
Received: 27 Jul 2021. Accepted: 21 Sep 2021. Published online: 2 Nov 2021.
Crustacean Research 2021 Vol.50: 119–129
©Carcinological Society of Japan. doi: 10.18353/crustacea.50.0_119
Argulus japonicus (Branchiura: Argulidae) parasitic on largemouth
bass Micropterus salmoides in Japan, with the morphology of the adult
female of the argulid
Kazuya Nagasawa
Abstract.―Largemouth bass Micropterus salmoides (Lacepède, 1802) was intro-
duced from North America into Japan in 1925 and 1972. The fish has spread exten-
sively since the late 1960s and is now found in all prefectures of Japan. An adult fe-
male of the argulid branchiuran Argulus japonicus Thiele, 1900 was collected from
the body surface of a largemouth bass in the Kako River, Hyogo Prefecture, Japan.
This represents a new host record for A. japonicus. The morphology of the adult fe-
male collected is reported in detail. Although A. japonicus is native to Japan, the spe-
cies is not strictly host-specific and can utilize largemouth bass of the North American
origin as its host in Japan.
Key words: fish parasite, fish louse, new host record
■Introduction
Many species of freshwater fishes have been
introduced from other countries to Japan for
aquaculture, sport-fishing, and ornamental pur-
poses (Chiba et al., 1989). The largemouth
bass Micropterus salmoides (Lacepède, 1802)
(Centrarchiformes: Centrarchidae) is one such
fish: the species was introduced in 1925 and
1972 from North America into Japan, where,
since the late 1960s, it has established popula-
tions nationwide (Takamura, 2007). Nonethe-
less, little attention has been paid to the para-
site fauna of largemouth bass from Japan. In
addition to some helminth parasites and glo-
chidial larvae of unionid bivalves, only two
species of crustacean parasites are known to
infect largemouth bass in Japan (Nagasawa,
2017a), both are cyclopoid copepods: Lernaea
cyprinacea Linnaeus, 1758 (Lernaeidae)
(Kasahara, 1962) and Neoergasilus japonicus
(Harada, 1930) (Ergasilidae) (Nagasawa & In-
oue, 2012; Nagasawa & Sato, 2014).
A specimen of crustacean parasite collected
from a largemouth bass in western Japan was
received from a student at Hiroshima Universi-
ty. As described below, the specimen was iden-
tified as Argulus japonicus Thiele, 1900
(Branchiura: Argulidae). This represents a new
host record for A. japonicus and its first record
from largemouth bass in Japan. Argulus japoni-
cus was originally described by Thiele (1900)
based on a single female specimen from Tokyo
(reported as “Yeddo”), Japan, but its original
description was very short, without any figure
and host information. Thus, the species was
later redescribed by Thiele (1904) from speci-
mens collected from goldfish Carassius aura-
tus (Linnaeus, 1758) from Yokohama, Japan,
and also by Nakazawa (1914), Tokioka (1936),
and Yamaguti (1937) from specimens taken
from Japanese freshwater fishes, including
goldfish and common carp Cyprinus carpio
Linnaeus, 1758. However, as compared with
the current descriptions of Argulus spp. (e.g.,
Benz et al., 1995; Uyeno et al., 2017; Nagasa-
wa & Hirose, 2021), the redescriptions of A.
japonicus by the above authors lack detailed
KAZUYA NAGASAWA
120 Crustacean Research 50
morphological information. Moreover, as A.
japonicus has spread globally (Poly, 2008), it is
important to accurately describe the species
from Japan in order to aid in distinguishing it
from morphologically similar species in other
countries. Therefore, based on a detailed exam-
ination of the specimen collected, this paper re-
ports on the morphology of A. japonicus.
■Materials and Methods
The argulid specimen was collected from a
largemouth bass M. salmoides (body size not
measured) on 5 June 2007 in a reservoir (34°47′
38″N, 134°53′35″E) created upstream of a bar-
rage in the the lower reaches of the Kako River
at Yahata, Kakogawa, Hyogo Prefecture, west-
ern Japan. It was removed from the fishʼs body
surface, fixed, and then preserved in 70% etha-
nol. Later, at the Aquaparasitology Lobaorato-
ry, Shizuoka Prefecture, the specimen was first
examined under an Olympus SZX10 stereo mi-
croscope. It was then cleared in lactophenol
and examined under an Olympus BX51 phase-
contrast compound microscope using the
wooden slide procedure (Humes & Gooding,
1964; Benz & Otting, 1996). All drawings
were made with the aid of drawing tubes at-
tached to the microscopes. Morphological ter-
minology follows Benz et al. (1995) and Benz
& Otting (1996). The specimen was deposited
in the Crustacea (Cr) collection of the National
Museum of Nature and Science, Tsukuba,
Ibaraki Prefecture (NSMT-Cr 29117).
■Results
The argulid specimen collected in this study
is an adult female of A. japonicus, measuring
6.0 mm total length (from anterior tip of cara-
pace to posterior tip of abdomen) and 3.8 mm
maximum width (around midlength of cara-
pace).
Description of adult female
Body dorsoventrally flattened (Fig. 1A, B).
Carapace nearly circular, 4.0 mm long, compris-
ing 66.7% of total length, with frontal region
weakly delimited by anterolateral indentations,
and almost totally covering first to second pairs
of legs (Fig. 1A, B). Paired compound eyes dis-
tinct dorsally in frontal region of carapace (Fig.
1A). Naupliar eye located posterior to com-
pound eyes along midline of frontal region of
carapace (Fig. 1A). Dorsal surface of carapace
smooth without spines (Fig. 1A). Ventral sur-
face of frontal and lateral regions of carapace
ornamented with numerous, small sharply
pointed spines (Fig. 1B). Posterolateral lobes
of carapace 1.1 mm long, comprising 27.5% of
carapace length, ending in rounded margin,
separated by sinus nearly 1/3 length of cara-
pace (Fig. 1A). Paired respiratory areas each
consisting of small, oval anterior area and
large, reniform posterior area, located at levels
of first maxillae and second maxillae to first
legs, respectively (Fig. 1B, D). Thorax indis-
tinctly segmented (due to developed ovary
filled with eggs) (Fig. 1A, B). Abdomen bi-
lobed by anal indentation, longer than wide,
with posterior margin of each lobe rounded and
covered with tiny spines (Fig. 1A, B); anal in-
dentation 46.2% as long as abdomen. Paired
spermathecae oval in anterocentral region of ab-
domen (Fig. 1A, B). Subquadrate caudal rami
located at base of anal indentation with four
short naked setae on each ramus (Fig. 1A, C).
First antennae with four segments (Fig. 1E);
first segment sclerotized, with large projection
on posterolateral margin; second segment also
sclerotized, with large projection on anterior
margin, apically bent hook at lateral corner,
and large projection and knob-like swelling on
posterior margin; third segment longer than
wide, with two naked spiniform setae near dis-
tal margin; apical segment shorter than third
segment, with seven short naked spiniform se-
tae apically. Second antennae with five seg-
ments (Fig. 1E); first segment sclerotized, with
ARGULUS JAPONICUS FROM LARGEMOUTH BASS
121
Crustacean Research 50
Fig. 1. Argulus japonicus, adult female, 6.0 mm total length, NSMT-Cr 29117, from a largemouth bass Micropterus salmoides
in the the Kako River, Hyogo Prefecture, Japan. A, habitus, dorsal view; B, habitus, ventral view; C, caudal rami, dorsal view; D,
respiratory areas, ventral view; E, first antenna (a1), second antenna (a2), and postantenal spine (pas), ventral view; F, preoral sheath
and stylet, ventral view; G, mouth tube, ventral view; H, section of sucker membrane of first maxilla showing two supporting rods
and maginal projections, ventral view; I, second maxilla, ventral view; J, tip of terminal segment of second maxilla, ventral view; K,
two scale-like denticles on third segment of second maxilla, ventral view. Scale bars: A, B, 2 mm; C, E, F, 0.1 mm; D, 0.5 mm; G, I,
0.2 mm; H, J, K, 0.05 mm.
KAZUYA NAGASAWA
122 Crustacean Research 50
large projection and small swelling with four
naked spiniform setae on posterior margin;
second segment shorter than first segment, with
three and three naked spiniform setae, respec-
tively, near distal and on posterior margins;
third, fourth, and apical segments each longer
than wide, decreasing in length; third segment
with two and two naked spiniform setae, re-
spectively, near distal and on posterior mar-
gins; fourth segment with seven naked spini-
form setae on distal margin; apical segment
ending in six naked spiniform setae. Postanten-
nal spines large and stout, located posterior to
projections of first segments of first antennae
(Fig. 1E). Preoral sheath on ventral midline of
frontal region of carapace, with anterior tip of
stylet seen at sheath opening (Fig. 1F). Mouth
tube located posterior to preoral sheath, longer
than wide, becoming wider posteriorly, com-
posed of anterior labrum and posterior labium
furnished with scales and pair of tiny spines
(Fig. 1G).
First maxillae forming cup-like suckers (Fig.
1B, H), with 50 and 52 supporting rods each in
two sucker membranes; each rod composed of
six to seven (mostly seven, n＝10) sclerites;
basal sclerite nearly three times as long as
wide, widening distally; other sclerites trape-
zoidal or oval, decreasing in size distally; outer
margin of rim of sucker membrane with nu-
merous triangular projections. Second maxillae
with five segments (Fig. 1I–K); first segment
robust, with three basally separated, subequally
long blunt projections on posterior margin;
corpus of first segment bearing two posteriorly
directed spiniform setae and furnished with-
raised field of scale-like denticles; second seg-
ment nearly two times as long as wide, with
raised patch of serrate scale-like denticles on
anterodistal surface; third segment shorter than
second segment, with patch of serrate scale-
like denticles on anterolateral surface; fourth
Fig. 2. Argulus japonicus, adult female, 6.0 mm total length, NSMT-Cr 29117, from a largemouth bass Micropterus salmoides in
the the Kako River, Hyogo Prefecture, Japan. A, first leg, ventral view; B, second to apical segments of endopod of first leg, ventral
view; C, second leg, ventral view; D, third leg, ventral view; E, fourth leg, ventral view. Distal part of exopods and endopods and setae
projecting from these rami are not illustrated. Scale bars: A, C–E, 0.3 mm; B, 0.05 mm.
ARGULUS JAPONICUS FROM LARGEMOUTH BASS
123
Crustacean Research 50
segment subquadrate, with small denticles an-
teriorly; terminal segment smallest, ending in
one club-like and two spiniform projections.
Accessory spines near first segments of second
maxillae (Fig. 1B). Postmaxillary spines locat-
ed posterior to accessory spines (Fig. 1B).
First to fourth pairs of legs biramous; sym-
pods two-segmented, consisting of coxa and
basis, with small scale-like projections on ven-
tral surface; rami each consisting of exopod
and endopod, with two rows of plumose setae,
respectively, near ventro- and dorsoposterior
margins (Figs. 1, 2). First and second pairs of
legs each with dorsal flagellum projecting from
extreme proximal part of exopod (flagella usu-
ally not seen in ventral view, but flagellum
bearing 13 plumose setae ventrally visible on
second leg of specimen examined, Fig. 2C).
First pair of legs each with single plumose seta
on posterior margin of coxa and three-segment-
ed endopod ending in three short spines (Fig.
2A, B). Sympods of second and third pairs of
legs without setae (Fig. 2C, D). Endopods of
third and fourth pairs of legs two-segmented
(Fig. 2D, E). Fourth pair of legs each with coxa
forming natatory lobe bearing 12 plumose and
three short naked setae, respectively, on poste-
rior and distal margins, and basis bearing seven
plumose setae on posterior margin (Fig. 2E).
Color in ethanol-preserved specimen: Cara-
pace, abdomen, and legs white; thorax pale
yellow with irregularly shaped black spots un-
evenly scattered on dorsal surface; respiratory
areas fringed by continuous black pigment
(Fig. 3).
Remarks
Although the carapace of A. japonicus from
Japan has been reported to cover the first to
third or fourth pairs of legs (Nakazawa, 1914;
Tokioka, 1936; Yamaguti, 1937), the argulid
specimen collected in this study has a shorter
carapace that does not reach the third pair of
legs (Fig. 1A, B). In spite of this difference,
other morphological characters of the specimen
correspond to those of A. japonicus reported by
the above authors, and the specimen is identi-
fied as A. japonicus.
Only one adult female of A. japonicus was
examined in this study, but several morphologi-
cal differences are known between both sexes
of the species (Nakazawa, 1914; Tokioka,
1936; Yamaguti, 1937). The male of A. japoni-
cus has two posteriorly directed finger-like
projections on the posteroventral margin of the
coxa of the second leg, a swelling (＝socket)
on the posterior margin of the basis of the third
leg, and a peg on the anterior margin of the ba-
sis of the fourth leg. A knob-like projection is
also found at the anteroventral side of the third
segment of the thorax of the male. These struc-
tures are not found on the sympods and thorax
of the female (Figs. 1B, 2C, D, E).
Argulus japonicus has been introduced to
other continents from east/southeast Asia (Poly,
Fig. 3. Argulus japonicus, adult female, 6.0 mm total
length, NSMT-Cr 29117, from a largemouth bass Micropterus
salmoides in the the Kako River, Hyogo Prefecture, Japan.
Ethanol-preserved specimen, habitus, ventral view. Scale bar:
2 mm.
KAZUYA NAGASAWA
124 Crustacean Research 50
2008), in which it has been reported from Ja-
pan, Russian Far East (Gusev, 1987), Korea
(Choi & Yang, 1998; Han et al., 1998; De Zoy-
sa et al., 2017), China (e.g., Tokioka, 1939;
Hsiao, 1950; Wang, 1958; Institute of Hydrobi-
ology, Hubei Province, 1973; Kuang & Qian,
1991; Wadeh et al., 2008; Yang, 2009), Viet-
nam (Arthur & Te, 2006; Ky & Te, 2007), Ma-
laysia (Leong, 1986), Philippines (Cruz-Laci-
erda & Nagasawa, 2017), and Indonesia (e.g.,
Inaya et al., 2015; Idris et al., 2020). The spe-
cies has been identified using a traditional mi-
croscopic technique (Tokioka, 1939; Hsiao,
1950; Wang, 1958; Institute of Hydrobiology,
Hubei Province, 1973; Leong, 1986; Kuang &
Qian, 1991; Choi & Yang, 1998; Ky & Te,
2007; Yang, 2009; Cruz-Lacierda & Nagasawa,
2017) and a scanning electron microscope
(Wadeh et al., 2008; De Zoysa et al., 2017).
Although no morphological information exists
on A. japonicus from Far East Russia and In-
donesia, there is no significant difference in the
morphology of the species from Japan, China,
Korea, Philippines, and Malaysia (see the
above literature).
Argulus japonicus is morphologically similar
to Argulus coregoni Thorell, 1864, which also
occurs in east/southeast Asia, including Japan
(e.g., Tokioka, 1936; Yamaguti, 1937; Hoshina,
1950; Nagasawa & Yuasa, 2020; Nagasawa &
Taniguchi, 2021), Russian Far East (e.g., Do-
giel & Akhmerov, 1952; Smirnova, 1971; Gu-
sev, 1987; Ermolenko, 2004; Sokolov et al.,
2012), China (e.g., Wang, 1958; Institute of
Hydrobiology, Hubei Province, 1973; Kuang &
Qian, 1991; Yang, 2009), and Malaysia (Everts
& Avenant-Oldewage, 2009). Argulus japoni-
cus is distinguished from A. coregoni by hav-
ing an apically rounded abdomen (Fig. 1A, B)
(vs. apically pointed abdomen in A. coregoni),
about 50 supporting rods in the sucker mem-
brane of the first maxilla (vs. 60 or more sup-
porting rods in A. coregoni), and a single plu-
mose seta on the posterior margin of the coxa
of the first leg (Fig. 2A) (vs. four to eight plu-
mose setae in A. coregoni). The morphological
characters of A. coregoni have been reported
from Japan, China, and Malaysia (see the
above literature).
No information is available on the native
hosts of A. japonicus in the Kako River, where
the specimen was collected in this study. Previ-
ously, two specimens of A. japonicus were col-
lected from the river, but one specimen was
found on an unknown host and another speci-
men was a detached, free-swimming individual
(Nagasawa et al., 2009). In this study, the in-
fected largemouth bass was collected in the
lower reaches of the river, where 18 species of
cyprinids are found (Nishiguchi, 2007) and
likely to serve as native hosts for A. japonicus.
■Discussion
Largemouth bass is native to North America,
where the species is known as the hosts of sev-
eral Argulus species (A. appendiculosus C. B.
Wilson, 1907, A. flavescens C. B. Wilson,
1916, A. mississippiensis C. B. Wilson, 1916,
and an unidentified species) (Hoffman, 1999;
McAllister et al., 2016). Although A. japonicus
was introduced from Asia including Japan into
the U.S.A. (Meehean, 1940; Wilson, 1944;
Cressey, 1978), it has not been reported from
largemouth bass (e.g., Amin, 1981; Poly, 1998;
Hoffman, 1999). For sport fishing, largemouth
bass has been transplanted from North America
into other regions, such as South America, Eu-
rope, South Africa, and Far East Asia (Pereira
& Vitule, 2019) but, to date, A. japonicus has
not been recorded from the fish in these re-
gions. Thus, the collection of A. japonicus in
this study represents the first record of the spe-
cies from largemouth bass worldwide.
In Japan, various species of cyprinids (Cypri-
niformes) serve as the hosts for A. japonicus
(e.g., Nagasawa et al., 2012, 2013, 2018, 2021;
Yamauchi & Shimizu, 2013; Nagasawa, 2017b,
2018; Nagasawa & Miyajima, 2018; Nagasawa
& Ishiyama, 2019; see Nagasawa, 2009, 2011
ARGULUS JAPONICUS FROM LARGEMOUTH BASS
125
Crustacean Research 50
for the earlier literature), and a non-cyprinid
fish, i.e., Amur catfish Silurus asotus Linnaeus,
1758 (Siluriformes: Siluridae) is also known as
a host for the parasite (Nagasawa et al., 2010;
Yamauchi et al., 2011). Largemouth bass is the
second species of non-cyprinid host of A. ja-
ponicus in Japan. Moreover, two species of
parasitic copepods, L. cyprinacea and N. ja-
ponicus, have been reported from largemouth
bass in Japan (Kasahara, 1962; Nagasawa &
Inoue, 2012; Nagasawa & Sato, 2015), and A.
japonicus is the third crustacean parasite from
this fish species. Like A. japonicus, both L.
cyprinacea and N. japonicus show no strict
host specificity (Nagasawa et al., 2007; Nagas-
awa & Uyeno, 2012), and these three crusta-
cean parasites can utilize largemouth bass of
the North American origin as their host in Ja-
pan.
Recently, using GenBank, molecular identifi-
cation has been applied to A. japonicus and its
populations (Wadeh et al., 2010; Tandel et al.,
2021) but considerable variation is found be-
tween populations within the same country and
those in different countries (Wadeh et al.,
2010). There is, however, the possibility that
molecular data of misidentified congeneric
species have been registered at GenBank as
those of A. japonicus. Thus, for better under-
standing such variations, accurate morphologi-
cal identification of A. japonicus from each
collection locality is essential in submitting its
sequence data to GenBank.
■Acknowledgments
I thank the student of the Faculty of Applied
Biological Science, Hiroshima University, Hi-
gashi-Hiroshima, for providing me with the
speciemen of A. japonicus reported in this pa-
per. I am grateful to Daisuke Uyeno, Kagoshi-
ma University, Kagoshima, for his help with
literature. I also gratefully acknowledge two
anonymous reviewers for their comments to
improve the manuscript.
■Literature Cited
Amin, O., 1981. On the crustacean ectoparasites
of fishes from Southeast Wisconsin. Trans-
actions of the American Microscopical Soci-
ety, 100: 142–150.
Arthur, J. R., & Te, B. Q., 2006. Checklist of the
Parasites of Fishes of Viet Nam. FAO Fish-
eries Technical Paper. No. 369/2. vi＋133
pp. FAO, Rome
Benz, G. W., & Otting, R. L., 1996. Morphology
of the fish louse (Argulus: Branchiura).
Drum and Croaker, 27: 15–22.
Benz, G. W., Otting, R. L., & Case, A., 1995. Re-
description of Argulus melanostictus
(Branchiura: Argulidae), a parasite of Cali-
fornia grunion (Leuresthes tenuis: Atherini-
dae), with notes regarding chemical control
of A. melanostictus in a captive host popula-
tion. Journal of Parasitology, 81: 754–761.
Chiba, K., Taki, Y., Sakai, K., & Oozeki, Y.,
1989. Present status of aquatic organisms in-
troduced into Japan. In: S. S. De Silva, (ed.),
Exotic Aquatic Organisms in Asia. Proceed-
ings of the Workshop on Introduction of Ex-
otic Aquatic Organisms in Asia. Asian Fish-
eries Society Special Publications Vol. 3.
Asian Fisheries Society, Manila, pp. 63–70.
Choi, S. D., & Yang, H. C., 1998. Prevalence and
extermination of Argulus japonicus (Branchi-
ura) parasitic on farmed carp (Cyprinus car-
pio). Bulletin of the Yosu National University,
13: 949–958. (In Korean with English ab-
stract)
Cressey, R. F., 1978. Marine flora and fauna of
the Northeastern United States. Crustacea:
Branchiura. NOAA Technical Report NMFS
Circular, 413: 1–10.
Cruz-Lacierda, E. R., & Nagasawa, K., 2017.
Morphology of Argulus japonicus Thiele
(Crustacea, Branchiura, Argulidae) from koi
carp (Cyprinus carpio) and goldfish (Caras-
sius auratus) (Cypriniformes, Cyprinidae) in
Iloilo, Philippines. Philippine Agricultural
Scientist, 100: 431–436.
De Zoysa, M., Ryu, S.-Y., Kim, H.-C., & Park, B.
KAZUYA NAGASAWA
126 Crustacean Research 50
K., 2017. A scanning electron microscopic
study of Argulus japonicus (Crustacea:
Branchiura) isolated from goldfish (Caras-
sius auratus) in Korea. Pakistan Journal of
Zoology, 49: 727–732.
Dogiel, V. A., & Akhmerov, A. K., 1952. Parasitic
Crustacea of Amur River fishes. Uchenye
Zapiski Leningradskogo Ordena Gosu-
darstevennogo Universiteta, 141, Seria Bio-
logia Nauka 28: 268–294. (In Russian)
Ermolenko, A. V., 2004. Parasite fauna from
loaches (Cobitidae) of water basins in the
Primorsk Territory. Parazitologiya, 38: 53–
67. (In Russian with English abstract)
Everts, L., & Avenant-Oldewage, A. 2009. First
record of Argulus coregoni: a fish ectopara-
sitic crustacean from Malaysia and addition-
al notes on the morphology. Malaysian Ap-
plied Biology, 38: 61–71.
Gusev, A.V., 1987. Phylum Arthropoda. In: O. N.
Bauer, (ed.), Key to the Parasites of Fresh-
water Fishes of the Fauna of the USSR. Part
3. Nauka, Leningrad, pp. 378–524. (In Rus-
sian)
Han, K.-S., Jung, Y.-M., Park, T.-W., Lim, C.-W.,
Song, H.-J., & Do, H.-K., 1998. Experimen-
tal infection of Argulus japonicus in fresh-
water fishes. Korean Journal of Veterinary
Service, 21: 431–437. (In Korean with Eng-
lish abstract)
Hoffman, G. L., 1999. Parasites of North American
Freshwater Fishes. Second Edition. xx＋539
pp. Comstock Publishing Associates, Cornell
University Press, Ithaca and London.
Hoshina, T., 1950. Über eine Argulus-Art im Sal-
monidenteiche. Bulletin of the Japanese So-
ciety of Scientific Fisheries, 16: 239–243.
Hsiao, S. C., 1950. Copepods from Lake Erh Hai,
China. Proceedings of the United States Na-
tional Museum, 100: 161–299.
Humes, A. G., & Gooding, R. U., 1964. A method
for studying the external anatomy of cope-
pods. Crustaceana, 6: 238–240.
Idris, F., Kismiyati, & Mahasri, G., 2020. Differ-
ent concentration influence of Moringa ole-
ifera leaf aqueous extract immersion against
Argulus japonicus egg damage. IOP Confer-
ence Series: Earth and Environmental Sci-
ence, 441: 012131. doi:10.1088/1755-1315/
441/1/012131
Inaya, A. F. N., Kismiyati, & Subekti, S., 2015.
The influence of paraya seedʼs [sic] (Carica
papaya) toward the damage Argulus japoni-
cusʼs [sic] eggs. Jurnal Ilmiah Perikanan dan
Kelautan, 7: 159–164. (In Indonesian with
English abstract)
Institute of Hydrobiology, Hubei Province, (ed.),
1973. [An Illustrated Guide to the Fish Dis-
ease and Causative Pathogenic Fauna and
Flora in the Hubei Province]. 456 pp. Sci-
ence Press, Beijing. (In Chinese)
Kasahara, S., 1962. Studies on the biology of the
parasitic copepod Lernaea cyprinacea Lin-
naeus and the methods for controlling this
parasite in fish-culture ponds. Contributions
of the Fisheries Laboratory, Faculty of Agri-
culture, University of Tokyo, 3: 103–196. (In
Japanese with English abstract)
Kuang, P., & Qian, J., 1991. Parasitic Crustacea
of Freshwater Fishes. In: Editorial Commit-
tee of Fauna Sinica, Academia Sinica, (ed.),
Economic Fauna of China. iv＋199 pp. Sci-
ence Press, Beijing. (In Chinese)
Ky, H., & Te, B. Q., 2007. [Parasites of Freshwa-
ter Fishes of Vietnam]. 360 pp. Scientific
and Technical Publishing House, Hanoi. (In
Vietnamese)
Leong, T. S., 1986. Two ectoparasitic crustaceans
belonging to the family Argulidae (Crustacea:
Branchiura) in Malaysian freshwater fishes.
Malayan Nature Journal, 39: 157–164.
McAllister, C. T., Poly, W. J., Cloutman, D. G., Ro-
bison, H. W., & Hill, M. K., 2016. Argulus
spp. (Crustacea: Branchiura) on fishes from
Arkansas and Oklahoma: new geographic dis-
tribution records. Proceedings of the Oklaho-
ma Academy of Science, 96: 70–72.
Meehean, O. L., 1940. A review of the parasitic
Crustacea of the genus Argulus in the collec-
tions of the United States National Museum.
Proceedings of the United States National
Museum, 88: 459–522.
ARGULUS JAPONICUS FROM LARGEMOUTH BASS
127
Crustacean Research 50
Nagasawa, K., 2009. Synopsis of branchiurans of
the genus Argulus (Crustacea, Argulidae),
ectoparasites of freshwater and marine fishes
in Japan (1900–2009). Bulletin of the Bio-
geographical Society of Japan, 64: 135–148.
(In Japanese with English abstract)
Nagasawa, K., 2011. The biology of Argulus spp.
(Branchiura, Argulidae) in Japan: a review.
In: A. Asakura, R. T. Bauer, A. H. Hines, M.
Thiel, C. Held, C. Schubart, J. M. Furse, J.
Coughran, A. Baeza, K. Wada, T. Yamagu-
chi, T. Kawai, S. Ohtsuka, M. V. Archdale,
& M. Moriyasu, (eds.), New Frontiers in
Crustacean Biology, Proceedings of the TCS
Summer Meeting, Tokyo, 20–24 September
2009. Crustacean Monographs, 15: 15–21.
Nagasawa, K., 2017a. A checklist of the parasites
of three species of centrarchids (bluegill,
largemouth bass, and smallmouth bass) in
Japan (1962–2017). Biosphere Science, 56:
105–120. (In Japanese with English abstract)
Nagasawa, K., 2017b. Argulus japonicus
(Branchiura: Argulidae) parasitic on a fresh-
water minnow, Opsariichthys platypus (Cy-
prinidae): the second record from Shikoku,
western Japan. Biogeography, 19: 150–152.
Nagasawa, K., 2018. Argulus japonicus (Branchi-
ura: Argulidae) parasitic on a koi carp, Cyp-
rinus carpio, reared in Hokkaido, northern
Japan. Bulletin of the Biogeographical Soci-
ety of Japan, 73: 201–204. (In Japanese with
English abstract)
Nagasawa, K., & Hirose, M., 2021 Marine fish
parasite Argulus caecus (Crustacea: Branchi-
ura: Argulidae) accidentally collected from a
fixed net caught squid in northern Japan. Spe-
cies Diversity, 26: 289–296.
Nagasawa, K., & Inoue, A., 2012. Variations in
the infection level of Neoergasilus japonicus
(Copepoda: Ergasilidae) between freshwater
fishes at different sites in the Ashida River
system, western Japan. Zoosymposia, 8:
106–116.
Nagasawa, K., & Ishiyama, N., 2019. First record
of Argulus japonicus (Branchiura: Arguli-
dae) from Ishikawa Prefecture, central Ja-
pan, with a note on its infection on common
carp and koi carp. Nature of Kagoshima, 46:
197–201. (In Japanese with English abstract)
Nagasawa, K., & Miyajima, N., 2018. Argulus
japonicus (Branchiura: Argulidae), a fresh-
water fish ectoparasite, from Oita Prefecture,
Kyushu, Japan. Nature of Kagoshima, 45:
59–62. (In Japanese with English abstract)
Nagasawa, K., & Sato, H., 2015. Neoergasilus
japonicus (Copepoda: Ergasilidae) parasitic
on two alien freshwater fishes (Lepomis
macrochirus and Micropterus salmoides) in
central Japan, with its new record from Gun-
ma Prefecture. Bulletin of Gunma Museum
of Natural History, 19: 1–4.
Nagasawa, K., & Taniguchi, R., 2021. Second re-
cord of Argulus coregoni (Branchiura: Argu-
lidae) from acheilognathine fish (Cyprini-
dae): its infection of an oily bitterling
Tanakia limbata in central Japan. Taxa, 51:
29–37. (In Japanese with English abstract)
Nagasawa, K., & Uyeno, D., 2012. Utilization of
alien freshwater fishes by the parasitic cope-
pod Neoergasilus japonicus (Ergasilidae) on
Okinawa-jima Island, Japan, with a list of
the known hosts. Zoosymposia, 8: 82–97.
Nagasawa, K., & Yuasa, A., 2020. The fish louse
Argulus coregoni from Oncorhynchus masou
ishikawae (Salmonidae) cultured in Shikoku,
western Japan, with a list of occurrence re-
cords of A. coregoni from fishes reared in Ja-
pan. Crustacean Research, 49: 1–8.
Nagasawa, K., Miyat, S., Inoue, A., & Umino, T.,
2007. New host records for Lernaea cypri-
nacea (Copepoda), a parasite of freshwater
fishes, with a checklist of the Lernaeidae in
Japan (1915–2007). Journal of the Graduate
School of Biosphere Science, Hiroshima
University, 46: 21–33.
Nagasawa, K., Uyeno, D., & Tochimoto, T.,
2009. Argulus japonicus Thiele and A. core-
goni Thorell (Crustacea: Branchiura) from
western Honshu, Japan. Journal of the Grad-
uate School of Biosphere Science, Hiroshi-
ma University, 48: 43–47. (In Japanese with
English abstract)
KAZUYA NAGASAWA
128 Crustacean Research 50
Nagasawa, K., Katahira, H., & Mizuno, K., 2010.
New host and locality of the fish ectoparasite
Argulus japonicus (Crustacea, Branchiura,
Argulidae) in Japan, with a note on its heavy
infection. Biogeography, 12: 17–20.
Nagasawa, K., Murase, T., Yanagi, S., & Maeno,
K., 2012. Argulus japonicus Thiele (Crustacea:
Branchiura) from Kyushu, western Japan,
with a note on its heavy infection of koi carp
(Cyprinus carpio) and Japanese crucian carp
(Carassius cuvieri). Biosphere Science, 51:
15–20. (In Japanese with English abstract)
Nagasawa, K., Hanazaki, K., & Morimoto, S.,
2013. Two branchiuran crustaceans (Argulus
coregoni Thorell and A. japonicus Thiele)
from Kyoto and Osaka prefectures, central
Japan. Biosphere Science, 52: 59–64. (In
Japanese with English abstract)
Nagasawa, K., Nitta, M., & Kawai, K., 2018. Ar-
gulus japonicus (Branchiura: Argulidae)
parasitic on a lakeweed chub, Ischikauia
steenackeri (Cyprinidae), in northern Ky-
ushu, Japan. Biogeography, 20: 122–124.
Nagasawa, K., Fujino, Y., & Nakano, H., 2021.
The three-lips, Opsariichthys uncirostris un-
cirostris (Cyprinidae), a new host of Argulus
japonicus (Branchiura: Argulidae), with its
first host record from Lake Biwa, Japan. Na-
ture of Kagoshima, 48: 37–39.
Nakazawa, K., 1914. [A study on Argulus japoni-
cus, a louse of goldfish]. Journal of the Im-
perial Fisheries Institute, 9: 306–316. (In
Japanese)
Nishiguchi, R., 2007. [A survey at the Kako River].
Hyogo Biology, 13: 151–154. (In Japanese)
Pereira, F. W., & Vitule, J. R. S., 2019. The large-
mouth bass Micropterus salmoides (Lace-
pède, 1802): impacts of a powerful freshwa-
ter fish predator outside of its native range.
Reviews in Fish Biology and Fisheries, 29:
639–652.
Poly, W. J., 1998. New state, host, and distribu-
tion records of the fish ectoparasite, Argulus
(Branchiura), from Illinois (U.S.A.). Crusta-
ceana, 71: 1–8.
Poly, W. J., 2008. Global diversity of fishlice
(Crustacea: Branchiura: Argulidae) in fresh-
water. Hydrobiologia, 595: 209–212.
Smirnova, T. S., 1971. Parasitic Crustacea from
the fishes of the river Amurʼs basin. Parasi-
tology Paper, 25: 177–195. (In Russian)
Sokolov, S. G., Shedko, M. B., Protasov, E. N., &
Frolov, E. V., 2012. Parasites of the inland
water fishes of Sakhalin Island. In: V. V. Bo-
gatov, V. Yu. Barkalov, A. S. Lelej, E. A.
Makarchenko, & S. Yu. Storozhenko, (eds.),
Flora and Fauna of North-West Pacific Is-
lands (Materials of International Kuril Island
and International Sakhalin Island Projects).
Dalnauka, Vladivostok, pp. 179–216. (In
Russian with English abstract)
Takamura, K., 2007. Performance as a fish preda-
tor of largemouth bass [Micropterus salmoi-
des (Lacepède)] invading Japanese freshwa-
ters: a review. Ecological Research, 22:
940–946.
Tandel, R. S., Chanu, K. V., Hussain Bhat, R. A.,
Dash, P., Shah, T. K., & Thakuria, D., 2021.
Morphometric and molecular identification
of Argulus japonicus (Thiele, 1900) in vul-
nerable Himalayan snow trout, Schizothorax
richardsonii (Gray 1832). Aquaculture Re-
search, 52. https://doi.org/10.1111/are.15486
Thiele, J., 1900. Diagnosen neuer Arguiden-
Arten. Zoologischer Anzeiger, 23: 46–48.
Thiele, J., 1904. Beiträge zur Morphologie der
Arguliden. Mitteilungen aus dem Zoolo-
gischen Museum in Berlin II, 4: 1–51, 4 pls.
Tokioka, T., 1936. Preliminary report on Arguli-
dae in Japan. Annotationes Zoologicae Japo-
nenses, 15: 334–343.
Tokioka, T., 1939. Argulus of Manchukuo. Anno-
tationes Zoologicae Japonenses, 18: 42–47.
Uyeno, D., Miyazaki, W., & Nagasawa, K., 2017.
First record of the fish louse Argulus quad-
ristriatus (Branchiura: Arguloida: Argulidae)
from Japanese waters, with three new host
records. Species Diversity, 22: 37–44.
Wadeh, H., Yang, J. W., & Li, G. Q., 2008. Ultra-
structure of Argulus japonicus Thiele, 1900
(Crustacea: Branchiura) collected from
Guangdong, China. Parasitology Research,
ARGULUS JAPONICUS FROM LARGEMOUTH BASS
129
Crustacean Research 50
102: 765–770.
Wadeh, H., Alsarakibi, M., & Li, G., 2010. Anal-
ysis of genetic variability within Argulus ja-
ponicus from representatives of Africa, Mid-
dle East, and Asia revealed by sequences of
three mitochondrial DNA genes. Parasitolo-
gy Research, 107: 547–553.
Wang, K.-N., 1958. Preliminary studies on four
species of Argulus parasitic on fresh-water
fishes taken from the area between Nanking
and Shanghai, with notes on the early larval
development of Argulus chinensis. Acta
Zoologica Sinica, 10: 322–335. (In Chinese
with English abstract)
Wilson, C. B., 1944. Parasitic copepods in the
United States National Museum. Proceed-
ings of the United States National Museum,
94: 529–582, pls. 20–34.
Yamaguti, S., 1937. On two species of Argulus
from Japan. In: R.-E. S. Schulz, & M. P.
Gnyedina, (eds.), Papers on Helminthology
Published in Commemoration of the 30 Year
Jubileum of the Scientific, Educational and
Social Activities of the Honoured Worker of
Science K. J. Skrjabin, M. Ac. Sci. and of
15th Anniversary of All-Union Institute of
Helminthology. Lenin All-Union Academy of
Agricultural Science, Moscow, pp. 781–784.
Yamauchi, T., & Shimizu, M., 2013. New host
and distribution records for the freshwater
fish ectoparasite Argulus japonicus (Crusta-
cea: Branchiura: Argulidae). Comparative
Parasitology, 80: 136–137.
Yamauchi, T., Nakano, H., & Nagasawa, K.,
2011. Infection with Argulus japonicus on
Amur catfish Silurus asotus in an aquarium.
Japanese Journal of Limnology, 72: 211–
214. (In Japanese with English abstract)
Yang, S., 2009. Branchiura. In: D. Song, & S.
Yang, (eds.), The Fauna of Hebei, China.
Crustacea. Hebei Science and Technology
Publishing House, Shijiazhuang, pp. 178–
184. (In Chinese)
Addresses
(KN) Graduate School of Integrated Sciences for
Life, Hiroshima University, 1–4–4 Kagamiyama,
Higashi-Hiroshima, Hiroshima 739–8528, Japan
(KNʼs present address) Aquaparasitology
Laboratory, 365–61 Kusanagi, Shizuoka 424–0886
,
Japan
E-mail address of corresponding author
ornatus@hiroshima-u.ac.jp
