Trematoda: Isoparorchiidae) from Freshwater Fishes in Western Japan, with a Review of Its Host-Parasite Relationships in Japan (1915–2013

Variation of insular mice in Kyushu Biogeography 15. 11–20．Aug. 20, 2013

Isoparorchis hypselobagri (Trematoda: Isoparorchiidae) from freshwater fishes in western Japan, with a review of its host-parasite relationships in Japan (1915–2013)

Kazuya Nagasawa1*, Hirotaka Katahira1,2 and Masato Nitta1 1 Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima, Hiroshima, 739-8528 Japan 2 Present address: Graduate School of Environmental Science, Hokkaido University, N10 W5, Sapporo, Hokkaido, 060-0810 Japan

Abstract. Specimens of Isoparorchis hypselobagri (Billet, 1898) were collected from the following freshwater fishes in western Japan: Anguilla japonica (Anguillidae) from Shimane and Ehime prefectures; Silurus asotus (Siluridae) from Hiroshima and Yamaguchi prefectures; Acanthogobius flavimanus (Gobiidae) from Shimane Prefecture; Candidia temminckii (Cyprinidae), Pungtungia herzi (Cyprinidae), Rhinogobius fluviatilis (Gobiidae), and Rhinogobius sp. (Gobiidae) from Hiroshima Prefecture. The collection of I. hypselobagri from A. japonica, A. flavimanus, R. fluviatilis, and Rhinogobius sp. represents new host records, and the parasite is reported for the first time from Hiroshima, Yamaguchi, and Ehime prefectures. Host-parasite relationships of I. hypselobagri infecting Japanese freshwater fishes are reviewed based on the literature published in 1915–2013.

Key words: Isoparorchis hypselobagri, Trematoda, fish parasite, new host records

Introduction Tewari & Pandey, 1989), physiology (e.g., Adak & Manna, 2011), body composition (e.g., Srivastava & Trematodes of the digenean family Isoparorchi- Gupta, 1976), occurrence in fishes (e.g., Devaraji & idae are endoparasites of freshwater fishes in Asia Ranganathan, 1967; Bashirullah, 1972), and pathol- and Australsia (Gibson, 2002), where Isoparorchis ogy (e.g., Mahajan et al., 1979; Li et al., 2002). hypselobagri (Billet, 1898) has been reported from During a study of the parasite fauna of freshwater the Russian Far East (Bykhovskaya-Pavlovskaya fishes of western Japan, we collected specimens of & Kulakova, 1987), Japan (Shimazu et al., 2011), I. hypselobagri in Shimane, Hiroshima, Yamaguchi, China (Chen et al., 1973), Vietnam (Moravec & and Ehime prefectures. This collection includes new Sey, 1989), Indonesia (Bovien, 1927), Bangladesh host and prefecture records for the parasite. In Ja- (Chandra, 2006), India (Bhalerao, 1936), Pakistan pan, the species has been studied for its morphology (Bilquees & Khatoon, 1972), and Australia (Cribb, and ecology since 1915 when Kobayashi (1915a) 1988). Because of its large body size of adult worms first described it. However, many of those studies (up to over 40 mm) and impacts on fish hosts, much have been published in Japanese, thus it is difficult attention has been paid to various aspects of the bi- for scientists of other countries to fully understand ology of the species, such as the morphology (e.g., the knowledge of the species reported in Japan. The present paper reports on our findings and, using the *Corresponding author: [email protected] literature published between 1915 and 2013, reviews

－ 11 － Isoparorchis hypselobagri from freshwater fishes Kazuya Nagasawa, Hirotaka Katahira and Masato Nitta the host-parasite relationships of the species infect- 2) Candidia temminckii (Temminck & Schlegel, ing Japanese freshwater fishes. 1846) (Cypriniformes: Cyprinidae): one immature (6.8 mm BL, site: mesentery) and one mature (9.6 Materials and Methods mm BL, site: mesentery, NSMT-Pl 6023 [N=1]) specimens from the Nukui River, a tributary of the Freshwater fishes were collected at various locali- Kurose River, Higashi-Hiroshima City, Hiroshima ties in Shimane, Hiroshima, Yamaguchi, and Ehime Prefecture, on 26 and 28 March 2012, respectively. prefectures, western Japan, in 2008–2013. Fishes 3) Pungtungia herzi Herzenstein, 1892 (Cyprini- were transported alive to the laboratory at Hiroshima formes: Cyprinidae): one mature (26.1 mm BL, site: University, where they were identified using Nakabo body muscle, NSMT-Pl 6024 [N=1, Fig. 2]) and one (2002) and examined for parasites. Trematodes were immature (11.2 mm BL, site: mesentery) specimens flattened between slide glass and cover-slip, fixed from the Nukui River, a tributary of the Kurose Riv- in 70% ethanol, stained in Heidenhain’s iron he- er, Higashi-Hiroshima City, Hiroshima Prefecture, matoxyline, dehydrated in a graded ethanol series, on 24 July 2012. cleared in xylene, and mounted in Canada balsam. 4) Silurus asotus Linnaues, 1758 (Siluriformes: They were measured for body length (BL, mm) and Siluridae): three mature (12.5–20.3 mm BL, site: air examined for maturity: worms with and without eggs bladder) and one immature (3.2 mm BL, body cav- in the uterus were recorded as mature and immature, ity) specimens from the Awano River, Shimonoseki respectively. Drawings were made with the aid of City, Yamaguchi Prefecture, on 22 February 2011; a drawing tube. Representative voucher specimens four mature (22.9–45.2 mm BL, site: air bladder, are deposited in the Platyhelminthes (Pl) collection NSMT-Pl 6025 [N=1]) and three mature (35.9–40.1 housed at the National Museum of Nature and Sci- mm BL, site: air bladder) specimens from the Fu- ence (NSMT-Pl) in Tsukuba, Ibraki Prefecture, Ja- ruko River, a tributary of the Kurose River, Higashi- pan, and the remaining specimens are retained in the Hiroshima City, Hiroshima Prefecture, on 21 Febru- senior author’s collection. The scientific and Japa- ary and 10 July 2012, respectively. nese names of fishes used in this paper are adopted from Nakabo (2013) and the English names of fishes are from Froese & Pauly (2013).

Results and Discussion

Specimens of I. hypselobagri were collected from the following fishes in western Japan: 1) Anguilla japonica Temminck & Schlegel, 1847 (Anguilliformes: Anguillidae): one immature specimen (6.4 mm BL, site: stomach wall tissue) from the Sozu River, Ainan Town, Ehime Prefecture, on 5 July 2008; four immature specimens (2.3–5.8 mm BL, sites: mesentery and outer surface of air bladder wall, NSMT-Pl 6022 [N=1, Fig. 1A]) from Lake Shinji, Izumo City, Shimane Prefecture, on 3 August Fig. 1. Isoparorchis hypselobagri: A, immature specimen, 2011; and one immature specimen (9.6 mm BL, site: NSMT-Pl 6022, from Anguilla japonica in Lake Shinji, Shimane Prefecture; B, immature specimen, NSMT-Pl mesentery) from Lake Nakaumi, Matsue City, Shi- 6026, from Acanthogobius flavimanus in Lake Shinji, mane Prefecture, on 8 November 2011. Shimane Prefecture. Scale bars: 1 mm.

－ 12 － Isoparorchis hypselobagri from freshwater fishes Kazuya Nagasawa, Hirotaka Katahira and Masato Nitta

5) Acanthogobius flavimanus (Temminck & specimen (2.5 mm BL, site: liver tissue, NSMT-Pl Schlegel, 1845) (Perciformes: Gobiidae): six imma- 6029 [N=1]) from the Furuko River, a tributary of ture specimens (2.4–5.3 mm BL, site: body cavity, the Kurose River, Higashi-Hiroshima, Hiroshima NSMT-Pl 6026 [N=1, Fig. 1B]) from Lake Shinji, Prefecture, on 13 September 2012. Matsue City, Shimane Prefecture, on 8 January 2013. Since immature and mature worms of I. 6) Rhinogobius fluviatilis Tanaka, 1925 (=Rhino- hypselobagri were well described by Yamashita & gobius sp. LD of Nakabo [2002]; LD= large-dark Nishida (1955) and Shimazu et al. (2011), respec- type [Anonymous, 1989]) (Perciformes: Gobiidae): tively, and our observation did not add new informa- one immature (4.2 mm BL, site: liver tissue, NSMT- tion on its morphology, no description of the speci- Pl 6027 [N=1]) and three immature (3.3–4.4 mm BL, mens collected is given in this paper. Four species of site: liver tissue, NSMT-Pl 6028 [N=1]) specimens fishes, A. japonica, A. flavimanus, R. fluviatilis, and from the Furuko River, a tributary of the Kurose Rhinogobius sp. (=Rhinogobius sp. OR of Nakabo River, Higashi-Hiroshima City, Hiroshima Prefec- [2002]), are new host records for I. hypselobagri. ture, on 10 January 2012 and 13 September 2012, This parasite is herein reported for the first time respectively. from Hiroshima, Yamaguchi, and Ehime prefectures 7) Rhinogobius sp. (=Rhinogobius sp. OR of in Japan. The fish hosts of I. hypselobagri in Japan is Nakabo [2002]; OR=orange type [Anonymous, listed in Table 1. 1989]) (Perciformes: Gobiidae): one immature There was a taxonomic confusion in R. fluviatilis and Rhinogobius sp. in Japan. The former species was earlier reported as“ Rhinogobius sp. LD” (Naka- bo, 2002), but Suzuki & Chen (2011) conducted a detailed taxonomic study of gobiids of the genus and concluded that both are identical with each other: thus, R. fluviatilis is a current valid name. Although Rhinogobius sp. reported in this paper was formerly regarded as“ Rhinogobius sp. OR” (Nakabo, 2002), the latter has been demonstrated to include several species (Suzuki et al., 2010) and, following Nakabo (2013), Rhinogobius sp. is herein used. Future iden- tification of Rhinogobius sp. examined in this study, a specimen preserved in 70% ethanol is kept in the junior author’s (M.N.) collection.

Review of the host-parasite relationships of Isoparorchis hypselobagri infecting Japanese freshwater fishes

In Japan, this parasite was originally described by Kobayashi (1915a) as Leptolecithum eurytremum using mature specimens from the air bladder of Silu- rus asotus (as Parasilurus asotus) and Tachysurus Fig. 2. Isoparorchis hypselobagri: mature specimen, NSMT- nudiceps (as Pseudobagrus aurantiacus) (see below Pl 6024, from Pungtungia herzi in the Nukui River, a tributary of the Kurose River, Hiroshima Prefecture. for the scientific name of this species) and imma- Scale bar: 4 mm. ture specimens from the body cavity of these fishes,

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Table 1. Fish hosts of Isoparorchis hypeselobagri in Japan, based on the previous and present studies. The classification scheme and scientific and Japanese names of fishes are adopted from Nakabo (2013). If present, English names of fishes are also adopted from Froese & Pauly (2013).

Order Family Scientific name Japanese name English name Prefecture Reference Anguilliformes Anguillidae Anguilla japonica nihon-unagi Japanese eel Shimane, Ehime present study Cypriniformes Cyprinidae Candidia sieboldii numamutsu ―* Shiga Shimazu et al. (2011) (as Nipponocypris sieboldii) Candidia temminckii kawamutsu dark chub Nara, Oita, Hiroshima Sawada & Osako (1969); (as Zacco temminckii) Kugi & Shiote (1979); present study Gnathopogon elongatus ta-moroko Nagano, Shiga Yamaguti (1938); Shimazu ― elongatus et al. (2011) Hemibarbus barbus nigoi Tokyo Suzuki et al. (1967); ― Kamegai et al. (1972) Opsariichthys platypus oikawa freshwater minnow Oita Okabe (1940); Kugi & (as Zacco platypus) Shiote (1979) Pseudogobio esocinus kamatsuka ― Gunma, Tokyo, Shiga Nihei et al. (1964); esocinus Suzuki et al. (1967); (as Pseudogobio esocinus) Shimazu et al. (2011) Pungtungia herzi mugitsuku ― Shiga, Hiroshima, Kifune (1978); Shimazu et Fukuoka al. (2011); present study Sarcocheilichthys vari- biwa-higai ― Ibaraki Yamaguti (1934) egatus microoculus (as Sar- cocheilichthys variegatus) Tanakia lanceolata yari-tanago ― Shiga Shimazu et al. (2011) Tribolodon hakonensis ugui big-scalled redfin Ibaraki Kobayashi (1915a, 1921); (as Richardosonius hakuen- Yamaguti (1934) sis, Leuciscus hakonensis) Siluriformes Bagridae Tachysurus nudiceps (as gigi ― Ibaraki, Chiba, Shiga, Kobayashi (1915a, 1915b, Pseudobagrus aurantiacus) Okayama 1921) Siluridae Silurus biwaensis biwako-ō-namazu Eurasian catfish Shiga Shimazu et al. (2011) Silurus asotus namazu Amur catfish Ibaraki, Gunma, Chiba, Kobayashi (1915a, 1915b, (as Parasilurus asotus) Tokyo, Nagano, Shiga, 1921); Yamaguti (1934); Kyoto, Okayama, Nihei et al. (1964); Suzuki Hiroshima, Yamaguchi, et al. (1967); Iwata et al. Miyazaki (2007); Shimazu (2007); Shimazu et al. (2011); present study Salmoniformes Osmeridae Hypomesus nipponensis wakasagi Japanese smelt Not clear** Kobayashi (1915a, 1921) (as Hypomesus olidus) Perciformes Centrarchidae Lepomis macrochirus burūgiru bluegill Shiga Shimazu et al. (2011) Micropterus salmoides burakku-basu largemouth black Shiga Grygier (2004); Shimazu et bass al. (2011) Cottidae Cottus reinii utsusemi-kajika ― Shiga Shimazu et al. (2011) Odontobutidae Odontobutis obscura donko ― Not reported Yamaguti (1934) (as Mogrunda obscura) Gobiidae Acanthogobius flavimanus mahaze yellowfin goby Shimane present study Gymnogobius urotaenia ukigori ― Nagano, Shiga Yamaguti (1938); Shimazu (as Chaenogobius macro- et al. (2011) gnathos)*** Rhinogobius fluviatilis ō-yoshinobori ― Hiroshima present study Rhinogobius sp. BW biwa-yoshinobori ― Shiga Shimazu et al. (2011) Rhinogobius sp.**** ― Hiroshima present study Tridentiger brevispinis numa-chichibu ― Shiga, Kyoto Shimazu & Urabe (2005); Shimazu et al. (2011) Channidae Channa argus kamuruchī snakehead Ibaraki, Chiba, Shiga, Yamashita & Nishida (as Ophicephalus argus) Shimane, Kochi, (1955); Komatsu & Kumamoto Matsumura (1963); Suzuki et al. (1967); Uehara (1972); Shimazu et al. (2011) *: No English name. **: Kobayashi (1915a, 1921) collected the infected fishes of four species, including H. nipponensis, in Okayama, Chiba, Ibaraki, and Shiga prefectures but did not indicate the sampling locality of the parasite. ***: See Shimazu (2007) for the scientific name of this gobiid. ****: This is identical with“ Rhinogobius sp. OR” (Nakabo, 2002).

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Hypomesus nipponensis (as H. olidus) and Tri- and 5 orders are known as its hosts (Table 1), which bolodon hakonensis (as Richardosonius hakuensis) indicates that the host specificity of the parasite is not collected in Okayama Chiba, Ibaraki, and Shiga pre- strict for fishes. Kobayashi (1915a) used“ gigi” as the fectures. Kobayashi (1915a) did not designate a type Japanese name for P. aurantiacus, but these names locality nor a type host for this parasite. As the origi- were a problematic use, because P. aurantiacus nal description was published in Japanese, its Eng- indicates a different species of bagrid called“ giba- lish version was later published (Kobayashi, 1921). chi” in Japanese. Thus, Kifune (1978) suggested the In a series of papers on the endoparasitic worms fish reported as“ gigi” by Kobayashi (1915a) might from Japan, Kobayashi (1915b, 1915c, 1915d) re- have been“ Pelteobagrus nudiceps.” Shimazu et al. ported anatomical features of the species (as L. eury- (2011) also made a similar suggestion. As no Kobayashi’s tremum) using adult specimens from S. asotus and (1915a) specimen of“ gigi” or P. aurantiacus re- T. nudiceps. The same scientific name of the parasite mains, it is impossible at present to clarify what was also used by Odhner (1927) for the Japanese species was examined by him. Therefore, following specimens provided by Kobayashi. Subsequently, the the original Japanese name of the fish, we adopt species was reported as Isoparorchis trisimiltubis “gigi” and its most current scientific name, T. nudi- Southwell, 1913 (Yamaguti, 1934, 1938; Yamashita ceps, is used in this paper instead of P. aurantiacus. & Nishida, 1955; Uehara, 1972), but both L. eury- Okabe (1940) collected“ Isoparorchis sp.” from an tremum and I. trisimiltubis have been regarded as unspecified host but, according to Kifune (1978), it a junior synonym of I. hypselobagri in Japan (see was I. hypselobagri from Opsariichthys platypus (as Shimazu, 1999, 2002; Shimazu et al., 2011). Re- Zacco platypus). Also, Iwata et al. (2007) reported cently, Shimazu et al. (2011) redescribed the species “Isoparorchis sp.” from S. astotus, and their speci- based on specimens from fishes in the Lake Biwa mens are herein regarded as I. hypselobagri based basin, central Honshu, Japan, and made a detailed on the pictures (figs. 1–2 in Iwata et al., 2007). On historical review of the synonymy of the species. the other hand, Shimazu (2007) found a specimen No molecular work using materials from Japan and of Isoparorchis from Tandanus tandanus in Satyu other countries has so far been conducted. Yamaguti’s Collection deposited at the Meguro Para- sitological Museum, Tokyo, but this host record is Geographical distribution not included in Table 1, because he suggests that the The species has been found in the following 18 specimen was collected in Australia. prefectures in Japan (Table 1): Gunma, Ibaraki, Chi- ba, Tokyo, Nagano, Shiga, Kyoto, Nara, Okayama, Prevalence and intensity of infection Shimane, Hiroshima, Yamaguchi, Ehime, Kochi, Fu- Infection levels of I. hypselobagri vary between kuoka, Oita, Miyazaki, and Kumamoto. These pre- fish species, fish sizes, or sampling localities. For ex- fectures are located in central and western Honshu, ample, 70.0% of 10 Channa argus (as Ophicephalus Shikoku, and Kyushu islands, all of which belong to argus) from Lake Shinji, Shimane Prefecture, were the temperate portion of Japan. So far, the species infected with a mean intensity of 3.1 worms (intensity has not been reported from the subarctic (e.g., north- range: 0–5) (Yamashita & Nishida, 1955), while only ern Honshu and Hokkaido) and subtropical (e.g., 3.2% of 2,061 Candidia temminckii (as Zacco tem- Okinawa) portions of Japan. mickii) from the Shirazuna River, Nara Prefecture, harbored up to 3 worms (mean intensity: 1.1 worms) Fish hosts (Sawada & Osako, 1969). In the latter fish sample, The species parasitizes various freshwater fishes no worm was found in small fish (≤44 mm BL) but in Japan. Based on the previous and present studies, prevalence of infection steadily increased with an 24 nominal and 2 unnamed species in 10 families increase in fish size: 2.3, 8.1, and 14.5% for fish

－ 15 － Isoparorchis hypselobagri from freshwater fishes Kazuya Nagasawa, Hirotaka Katahira and Masato Nitta of 45–70, 71–110, and ≥111 mm BL, respectively in the air bladder of S. asotus (Kobayashi, 1915a, (Sawada & Osako, 1969). 1921; Yamaguti, 1934; Sawada & Osako, 1969; Prevalence of infection by I. hypselobagri fluctu- Shimazu, 2007; Iwata et al., 2007; Shimazu et al., ated seasonally in C. temminckii from the Shirazuna 2011; this paper) but also occur in various body parts River (Sawada & Osako, 1969). Although it was of some other fishes, i.e., the body cavity of Silurus high in late winter and spring (February to May), it biwaensis (Shimazu et al., 2011), the air bladder decreased in early and mid-summer (June and July) of T. nudiceps (Kobayashi, 1915a, 1921), the body and reached the lowest value in late summer (Au- muscles of C. temminckii (Sawada & Osako, 1969; gust). It, however, increased in fall (September to Kugi & Shiote, 1979; this paper), O. platypus (Kugi November) and showed high values in early and mid- & Shiote, 1979), Lepomis macrochirus (Shimazu et winter (December and January). For the observed al., 2011) and Micropterus salmoides (Shimazu et high prevalence in winter, Sawada & Osako (1969) al., 2011), the hypodermal tissues and body muscles suggested that cercariae of this parasite may invade of P. herzi (Kifune, 1978: this paper), and around the the fish in fall after they develop in and emerge from air bladder and in the body cavity of C. argus (Suzuki snail intermediate hosts during summer, but since et al., 1967; Shimazu et al., 2011). Mature worms the parasite is known to use three hosts (i.e., snail from the air bladder of S. asotus were constantly first intermediate hosts, arthropod second intermedi- large (up to 45.2 mm BL, see below), which suggests ate hosts, and fish final hosts) to complete its life that this fish and the air bladder are quite suitable for cycle (Besprozvannykh & Ermolenko, 1989), it may the parasite as its final host and infection site. be reasonable to consider that C. temminckii gets Immature worms (with no eggs in the uterus) infected by feeding on the second intermediate hosts also occur in various body parts of various fish spe- in fall. On the other hand, Sawada & Osako (1969) cies: the body cavity of S. asotus, Odontobutis obscura gave no explanation for the decline in prevalence in (as Mogrunda obscura), C. temminckii, Gnathopogon summer, but it is likely that this summer decline in elongatus elongates, H. barbus, O. platypus, Acantho- prevalence was caused by mortality of infected hosts gobius flavimanus, Gymogobius urotaenia (as after their spawning, because C. temminckii spawns Chaenogobius macrognathus), and C. argus (Ko- in May to August and reduces its adult density in the bayashi, 1915a, 1921; Yamaguti, 1934, 1938; Okabe, population during summer and fall (Katano, 1989). 1940; Yamashita & Nishida, 1955; Sawada & Osako, 1969; Kamegai et al., 1972; this paper), hypodermal Distribution and maturation in fish (as subcutaneous) tissues of Tribolodon hakonensis When worms parasitize the body muscles of C. (as Leuciscus hakonensis) and Sarcocheilichthys temminckii, they occur in the tunnel-like tubes built variegatus microoculus (as S. variegatus) (Yama- by themselves (Sawada & Osako, 1969). The color- guti, 1934), body muscles and flesh of T. hako- ation of the tissues surrounding the tubes changes to nensis, S. variegatus microoculus, H. barbus and blackish brown, and the skin near the infection site is C. argus (Yamaguti, 1934; Yamashita & Nishida, swollen (see fig. 1 in Sawada & Osako, 1969). Simi- 1955; Suzuki et al., 1967; Kamegai et al., 1972), air lar tube formation and blackish pigmentation also bladder and air bladder wall of Anguilla japonica have been reported from other Japanese fishes, such and O. obscura (Yamaguti, 1934; this study), gut of as C. argus (Yamashita & Nishida, 1955), Hemibar- Rhinogobius sp. BW (Shimazu et al., 2011), stom- bus barbus (Kamegai et al., 1972), and Pungtungia ach wall of A. japonica and Cottus reini (Shimazu et herzi (Kifune, 1978). It is not yet known how much al., 2011; this paper), intestine of S. asotus (Shimazu the parasite affects the physiology and behavior of et al., 2011), intestinal wall of C. argus (Suzuki et those infected fishes in Japan. al., 1967), liver and liver wall of C. reini, R. fluvia- Mature worms (with eggs in the uterus) are found tilis, Rhinogobius sp. and C. argus (Yamashita &

－ 16 － Isoparorchis hypselobagri from freshwater fishes Kazuya Nagasawa, Hirotaka Katahira and Masato Nitta

Nishida, 1955; Suzuki et al., 1967; Shimazu et al., two pathways through prey-predator relationships: 2011; this paper), mesentery of A. japonica, C. tem- one is feeding by fish final hosts on arthropod second minckii and P. herzi (this paper), gonad wall of C. intermediate hosts and the other is predation by large argus (Suzuki et al., 1967), and gills of T. nudiceps piscivorus fishes on small fishes. In these pathways, (Kobayashi, 1915a, 1921). It is interesting to note metacercariae and immature worms may be trans- that the percentage of occurrence of mature worms ferred, respectively, from the second intermediate differs between body parts in the same host species: hosts to the final hosts and from the prey fishes to the in C. temminckii, about 50% of the worms from the predators. Yamaguti (1934) experimentally succeed- body muscles were mature, while the worms from ed in transferring immature worms (as larvae) from the body cavity were all immature (Sawada & Osa- O. obscura to S. asotus and regarded O. obscura as ko, 1969). a reservoir host. The previous works in Japan on I. Worms of various sizes are found in fish hosts. hypselobagri focused on its morphology and occur- Mature and immature worms from S. asotus mea- rence in freshwater fishes, and our knowledge on sured 20–40 mm BL and 8 mm BL, respectively the life cycle of the species is still limited: nothing (Shimazu et al., 2011). A similarly large mature is known, for example, about its second intermedi- specimen (45.2 mm BL) was also collected from S. ate hosts in Japan. We need more work on various asotus in this study. However, mature worms from aspects of the life cycle of the parasite. other fish species do not reach such a large size (e.g., 7.8–9.3 mm BL and 26.1 mm BL from P. herzi Acknowledgments [Kifune, 1978; this study]; 9.6 mm BL from C. temminckii [this study]: 11 mm BL from C. temminckii We thank Kouki Mizuno (Ehime Prefectural or O. platypus [Kugi & Shiote, 1979]), suggest- Uwajima Fishery High School), Tsunehiro Miura ing that, even if those fishes harbor mature worms, (Shimane Prefectural Fisheries Technology Center), they are less suitable for the parasite than S. asotus. Toshihiro Hatama (Yamaguchi Prefectural Fisher- Sawada & Osako (1969) reported a close positive ies Research Center), and Hidekatsu Yamaguchi relationship between body sizes of worms and their (Hoshizaki Green Foundation) for their assistance hosts (C. temminckii): larger worms occurred in in fish collection. We are also grateful to Yuzo Ota larger fish, which implies that the worms have no (Hiroshima University) for his help in fish examina- short-life and grow with fish growth and age. tion. This study was supported by Grants-in-Aid for JSPS Fellows (No. 22-08025 to H.K.) and Scientific Life cycle Research (C) (No. 24580267 to K.N.), both of which The life cycle of I. hypselobagri is poorly known were from the Japan Society for the Promotion of in Japan. Kobayashi (1915a, 1922) suggested that Science (JSPS), and the Hoshizaki Green Foundation the cercaria infecting freshwater snails Semisulco- to K.N. spira libertina (as Melania libertina) was identifi- able as the species, but his suggestion was denied by References Shimazu (1999, 2003). According to Shimazu (1999, 2003) and Shimazu et al. (2011), the morphology of Adak, S. & Manna, B., 2011. Amino acid excretion Cercaria introverta Faust, 1924 from Semisulcospira of Isoparorchis hypselobagri (Billet, 1898). Proc. spp. in Japan (Ito, 1964; Urabe, 2003) is similar to Zool. Soc., 64: 128–131. that of the cercaria of I. hypselobagri which was de- Anonymous, 1989. The genus Rhinogobius. In scribed in the Russian Far East (Besprozvannykh & Kawanabe, H. & Mizuno, N. (Eds), Freshwater Ermolenko, 1989). On the other hand, we consider fishes of Japan: 584. Yama-kei Publ., Tokyo. (In that wild fishes become infected with the parasite in Japanese).

－ 17 － Isoparorchis hypselobagri from freshwater fishes Kazuya Nagasawa, Hirotaka Katahira and Masato Nitta

Bashirullah, A. K. M., 1972. On the occurrence of http//:www.fishbase.org, version (02/2013). the trematode, Isoparorchis hypselobagri (Billet, Gibson, D. I., 2002. Family Isoparorchiidae Travas- 1898), in fishes and notes on its life history. Nor- sos, 1922. In Gibson, D. I., Jones, A. & Bray, R. A. wegian J. Zool., 20: 209–212. (Eds), Keys to the Trematoda, Vol. 1: 379–380. Besprozvannykh, V. V. & Ermolenko, A. V., 1989. CABI Publ., Oxon. Life cycle of Isoparorchis hypselobagri (Trema- Grygier, M. J., 2004. [Clarifying the parasitofauna of toda, Isoparorchidae [sic]) – catfish parasite. Lake Biwa]. In Nagasawa, K. (Ed), Aquaparasi- Zool. Zhur., 68: 136–139. (In Russian with Eng- tology in the field in Japan: 273–284, 341–342. lish abstract). Tokai Univ. Press, Hadano. (In Japanese). Bhalerao, G. D., 1936. Studies on the helminths of Ito, J., 1964. A monograph of cercariae in Japan and India. Trematoda III. J. Helminthol., 14: 207–228. adjacent territories. In Morishita, K., Komiya, Y. Bilquees, F. M. & Khatoon, A., 1972. Fresh water & Matsubayashi, H. (Eds), Progress of medical fish trematodes of West Pakistan. Histological parasitology in Japan, Vol. 1: 395–550. Meguro study of Isoparorchis pakistani sp. n. In Bilquees, Parasitol. Mus., Tokyo. F. M., Saeed, R., Rehana, R., Khatoon, A. & Iwata, K., Kaneta, M. & Taguchi, T., 2007. [A trema- Kaikabad, S. H. (Eds), Helminth parasites of tode parasitic in the air bladder of wild Amur cat- some vertebrates chiefly from fishes of West Paki- fish]. Ann. Rep. Miyazaki Pref. Fish. Exp. Stat. stan: 48–59. Agric. Res. Council, Govt. Pakistan, Fiscal Year 2006: 296–297. Miyazaki Pref. Fish. Karachi. Exp. Stat., Miyazaki. (In Japanese). Bovien, P., 1927. On Isoparorchis eurytremum (Ko- Kamegai, Sh., Kamegai, S. & Kihara, M., 1972. On bayashi) from Java. Vidensk. Medd. Naturhist. the occurrence of Isoparorchis hypselobagri Bil- Foren. Kobenhavn, 84: 281–289. let, 1898 [sic] in the muscle of Hemibarbus bar- Bykhovskaya-Pavlovskaya, I. E. & Kulakova, A. P., bus (Temminck & Schlegel) in the River Tama. 1987. Class Trematoda. In Bauer, O. N. (Ed), Key Monthl. Rep. Meguro Parasitol., Mus., (35): 3–5. to the parasites of the freshwater fish fauna of (In Japanese). the USSR, Vol. 3: 77–198. Nauka, Leningrad. (In Katano, O., 1989. Zacco temmincki. In Kawanabe, Russian). H. & Mizuno, N. (Eds), Freshwater fishes of Ja- Chandra, K. J., 2006. Fish parasitological studies pan: 718. Yama-kei Publ., Tokyo. (In Japanese). in Bangladesh: a review. J. Agric. Rural Dev., 4: Kifune, T., 1978. Discovery of Isoparorchis 9–18. hypselobagri (Billet, 1898) from Pungtungia Chen, C.-L. et al. (Eds), 1973. An illustrative guide herzi (Herzenstein) collected in Yabe River, Kyu- to the fish disease and causative pathogenic shu. Med. Bull. Fukuoka Univ., 5: 107–110. (In fauna of Hupei Province. 456 pp. Science Press, Japanese with English abstract). Beijing. (In Chinese). Kobayashi, H., 1915a. [Studies of endoparasitic Cribb, T. H., 1998. Two new digenetic trematodes trematodes from Japan (2)]. Dobutsugaku Zasshi from Australian freshwater fishes with notes on (Zool. Mag.), 27: 50–57, 1 pl. (In Japanese). previously described species. J. Nat. Hist., 22: Kobayashi, H., 1915b. [Studies of endoparasitic 27–43. trematodes from Japan (5)]. Dobutsugaku Zasshi Devaraji, M. & Ranganathan, V., 1967. Incidence of (Zool. Mag.), 27: 258–272, 1 pl. (In Japanese). Isoparorchis hypselobagri (Billet, 1898) (Trema- Kobayashi, H., 1915c. [Studies of endoparasitic toda, Hemiuridae) among the catfishes of Bha- trematodes from Japan (6)]. Dobutsugaku Zasshi vanisagar Reservoir. Indian J. Fish., 14: 232–250. (Zool. Mag.), 27: 299–311, 1 pl. (In Japanese). Froese, R. & Pauly, D. (Eds), 2013. FishBase. World Kobayashi, H., 1915d. [Studies of endoparasitic Wide Web electronic publication. Available from trematodes from Japan (7)]. Dobutsugaku Zasshi

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in eastern Japan. Res. Bull. Meguro Parasitol. Urabe, M., 2003. Trematode fauna of prosobranch Mus., (1): 15–19. (In Japanese with English ab- snails of the genus Semisulcospira in Lake Biwa stract). and the connected drainage system. Parasitol. Suzuki, T., Mukai, T., Yoshigou, H., Oseko, N. & Int., 52: 21–34. Chen, I.-S., 2010. Redefinition and proposal of Yamaguti, S., 1934. Studies on the helminth fauna of the new standard name for Rhinogobius sp. mor- Japan. Part 2. Trematodes of fishes, I. Japan. J. photype“ Shimahire” (Perciformes, Gobiidae). Zool., 5: 249–541. Bull. Osaka Mus. Nat. Hist., (64): 1–14. (In Japa- Yamaguti, S., 1938. Studies on the helminth fauna of nese with English abstract). Japan. Part 21. Trematodes of fishes, IV. 139 pp., Tewari, S. K. & Pandey, K. C., 1989. Scanning elec- 1 pl. Author’s publication, Kyoto. tron microscopic observations on surface topol- Yamashita, J. & Nishida, H., 1955. On the occur- ogy of Isoparorchis hypselobagri (Billet, 1898) rence of Isoparorchis trisimilitubis Southwell Odhner, 1927. Proc. Indian Acad. Sci. (Anim. in the muscle of Ophicephalus argus (Cantor). Sci.), 98: 373–377. Mem. Fac. Agri., Hokkaido Univ., 2: 160–163. (In Uehara, Y., 1972. Isoparorchis trisimilitubis South- Japanese with English abstract). well, 1913, discovered from Ophicephalus argus in Kumamoto Prefecture. Japan. J. Parasitol., 21 (1, suppl.): 27. (In Japanese). (Received May 30, 2013; Accepted June 26, 2013)

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