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Crustacean Research 46 Crustacean Research 46 a CYMOTHOID ISOPOD in FISH MARICULTURE

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Crustacean Research 46 Crustacean Research 46 a CYMOTHOID ISOPOD in FISH MARICULTURE Crustacean Research 2017 Vol.46: 95–101 ©Carcinological Society of Japan. doi: 10.18353/crustacea.46.0_95 Nerocila phaiopleura, a cymothoid isopod parasitic on Pacific bluefin tuna, Thunnus orientalis, cultured in Japan Kazuya Nagasawa, Sho Shirakashi Abstract.̶ Ovigerous females of Nerocila phaiopleura Bleeker, 1857 were collected from the body surface of young Pacific bluefin tuna, Thunnus orientalis (Temminck & Schlegel, 1844), cultured in Japan. This represents the first record of N. phaiopleura in finfish mariculture. The species is the third cymothoid isopod from maricultured fishes in Japan. The infected fish had a large hemorrhagic wound caused by N. phaio- pleura at the attachment site. Thunnus orientalis is a new host of the isopod. No cy- mothoid infection has so far been reported from wild individuals of T. orientalis that swims at high speeds in the oceans, and the observed occurrence of N. phaiopleura on this fish species is regarded as unusual under confined mariculture conditions. The hosts and geographical distribution records of N. phaiopleura in Japan are reviewed. Key words: fish parasite, fish mariculture, new host record Recently, Pacific bluefin tuna, Thunnus ori- mar et al., 2016). This is the first report of N. entalis (Temminck & Schlegel, 1844), is abun- phaiopleura in finfish mariculture. dantly cultured in Japanese coastal waters The isopods were collected from two (Yamamoto, 2012), with a production of 14726 individuals of six young T. orientalis (176– metric tons in 2015 (Anonymous, 2016). How- 259 mm in standard length) examined from ever, due to a short history of aquaculture of T. floating rectangular net-cages (12 m sides and orientalis in Japan, much remains poorly un- 5 m deep) in coastal waters of the north- derstood on its parasites. During a study of the western Pacific off Shirahama (33°40′45″N, crustacean parasites of T. orientalis farmed in 135°21′37″E), Nishimuro, Wakayama Prefec- Japan, two specimens of parasitic isopod were ture, central Japan, on 22 October 2009. Each collected from cage-cultured fish. Previously, fish was infected by one isopod. The isopod these specimens were preliminarily reported as specimens collected were fixed in AFA (alco- “Nerocila sp.?” (Shirakashi, 2013) or “Cy- hol-formaldehyde-acetic acid) solution and lat- mothoid isopods, possibly Nerocila sp.” (Balli er preserved in 70% ethanol. They are deposit- et al., 2016) without providing any information ed in the Crustacea (Cr) collection of the on their morphology and collection data. In National Museum of Nature and Science, this study, the specimens were re-examined Tsukuba, Ibaraki Prefecture, Japan (NSMT-Cr and identified as Nerocila phaiopleura Bleeker, 25555). The scientific and common names of 1857 (Isopoda, Cymothoidae). This species has fishes used in this paper follow Froese & Pauly been reported as a skin parasite of a variety of (2017), except for Japanese sardine, Sardinop- wild fishes in the Indo-West Pacific (e.g., sis melanostictus (Temminck & Schlegel, Bruce, 1982, 1987; Bowman & Tareen, 1983; 1846), which follows Nakabo (2013). Bruce & Harrison-Nelson, 1988; Trilles et al., The specimens were ovigerous females of N. 2011, 2013; Aneesh et al., 2013; Raja et al., phaiopleura (Fig. 1A, 1C), measuring 21.0– 2014; Nagasawa & Tensha, 2016; Rameshku- 22.0 mm in total length (with uropod rami) and Received: 9 Feb 2017; Accepted: 18 June 2017; Published online: 23 Aug 2017 95 KAZUYA NAGASAWA, SHO SHIRAKASHI Fig. 1. Caudal peduncle of a cage-cultured Thunnus orientalis infected by an ovigerous female Nerocila phaiopleura in coastal waters of the north-western Pacific off Shirahama, central Japan. A, N. phaiopleura infecting the host’s body surface; B, a hemorrhagic wound caused by N. phaiopleura; C, a specimen of N. phaiopleura, NSMT-Cr 25555, dorsal view. Scale bars: 10 mm in A and B; 5 mm in C. 9.0–9.2 mm in maximum width. They are char- lar skin wounds caused by N. phaiopleura have acterized by a broadly rounded anterior margin been reported in other fishes (Morton, 1974; of the cephalon, large eyes, weakly produced Mitani, 1982; Saito & Hayase, 2000; Ravi- ventrolateral margins of pleonites 1 and 2, a chandran et al., 2001; Raja et al., 2014; Nagas- triangular pleotelson, and straight and long awa & Tensha, 2016). A secondary bacterial in- uropod exopods. These morphological features fection is known to occur in skin lesions correspond to the descriptions of N. phaiopleu- caused by N. phaiopleura in Indian fishes ra from Kuwait (Bowman & Tareen, 1983) and (Ravichandran et al., 2001; Raja et al., 2014). Australia (Bruce, 1987). Coloration, such as At present, it is unknown when and where black stripes on the uropod exopods and the the young individuals of T. orientalis acquired lateral sides of the pleon and the posterior pe- infection by N. phaiopleura in the cages. These reonites, and back spots widely scattered on fish were produced at a hatchery from the eggs the dorsal side of the pereonites, the pleon and hatched on 23–24 June 2009. When sampled, the anterior pleotelson, is also identical with they had been held for 52 days in the cages, that shown in the photographs of N. phaiopleu- into which they were transported on 31 August ra from Japan (Saito & Hayase, 2000; Naga- 2009 from other cages set at Kushimoto, ap- sawa & Tensha, 2016). proximately 65 km distant from our sampling Both specimens of N. phaiopleura were at- site. Since the specimens of N. phaiopleura tached to the skin of the caudal peduncle of T. were ovigerous females and the skin wounds orientalis. Each infected fish had a large hem- found were large, it is unlikely that the isopods orrhagic wound caused by N. phaiopleura at infected the fish immediately before our sam- the attachment site (Fig. 1B). The wounds were pling. In other words, the isopod infection may shield-shaped (ca. 18 mm long and 10 mm have occurred before or slightly after the fish wide). No fish skin was present on the wounds, were transported to the cages sampled. where the muscle was exposed to the water. Two species of cymothoids other than N. While the specimens of N. phaiopleura collect- phaiopleura are known to infect marine fishes ed in this study were previously reported to “do cultured in Japan: Mothocya parvostis Bruce, not appear to cause serious harm to the fish” 1986 from Japanese amberjack, Seriola quin- (Bali et al., 2016: 262), their infection actually queradiata Temminck & Schlegel, 1845 and resulted in the large hemorrhagic wound. Simi- mejina, Girella punctata Gray, 1835 (Hatai & 96 Crustacean Research 46 Crustacean Research 46 A CYMOTHOID ISOPOD IN FISH MARICULTURE Yasumoto, 1980, 1981, 1982; Bruce, 1986), conditions. and Ceratothoa verrucosa (Schioedte & Mein- In Far East Asia, N. phaiopleura has been re- ert, 1883) from red seabream, Pagrus major ported from China as well (Morton, 1974; (Temminck & Schlegel, 1843) (Hatai, 1989, Bruce, 1982; Yu & Li, 2003). In Japan, in addi- 2006). Nerocila phaiopleura is the third cy- tion to T. orientalis and S. niphonius, four more mothoid species in Japanese finfish maricul- fish species are known as the hosts of N. phaio- ture. Cymothoids have been reported to infect pleura (Yamauchi, 2016): Japanese sardine, maricultured fishes in other countries as well Sardinopsis melanostictus (Clupeidae) (Mitani, (see Horton & Okamura, 2001): Ceratothoa 1982; Williams & Bunkley-Williams, 1986; gaudichaudii (H. Milne Edwards, 1840) in Bruce & Harrison-Nelson, 1988; Hiramoto, Chile (Sievers et al., 1996); Ceratothoa oes- 1996; Saito & Hayase, 2000; Nunomura, 2011; troides (Risso, 1826) in Croatia (Šarušic, 1999; Hata et al., 2017), Japanese anchovy, Engraulis Mladineo et al., 2009) and Turkey (Horton & japonicus Temminck & Schlegel, 1846 (En- Okamura, 2001, 2003); Emetha audouini (H. graulidae) (Mitani, 1982; Bruce & Harrison- Milne Edwards, 1840) and Ceratothoa paralle- Nelson, 1988), Japanese sardinella, Sardinella la (Otto, 1828) in Greece (Papapanagiotou et zunasi (Bleeker, 1854) (Clupeidae) (Mitani, al., 1999; Papapanagiotou & Trilles, 2001); 1982), and dotted gizzard shad, Konosirus and Cymothoa indica Schioedte & Meinert, punctatus (Temminck & Schlegel, 1846) (Clu- 1884 in India (Rajkumar et al., 2005a, 2005b). peidae) (Mitani, 1982). Infected individuals of The major hosts of N. phaiopleura are clupe- these fishes were caught in the coastal Pacific iform fishes, especially those of two families, waters of central and western Japan (localities Engraulidae and Clupeidae (Bruce, 1987; An- 1–7 and 11 in Fig. 2) and the Seto Inland Sea eesh et al., 2013). Marine fishes of other fami- including Hiroshima Bay (localities 8–10 in lies also serve as hosts for N. phaiopleura (e.g., Fig. 2), and most of these localities are affected Bowman & Tareen, 1983; Bruce & Harrison- by the warm current, Kuroshio (see Nagasawa Nelson, 1988; Trilles et al., 2011, 2013). Thun- & Tensha, 2016). While the species has also nus orientalis belongs to the Scombridae, and been suggested to occur in the southern Sea of three species of the family have hitherto been Japan (Toyama Bay, locality 12 in Fig. 2) (Saito reported to harbor N. phaiopleura: Indian & Hayase, 2000), no information is yet avail- mackerel, Rastrelliger kanagurta (Cuvier, able on the morphology of specimens from the 1816) (Rameshkumar & Ravichandran, 2010), bay. In addition, two species of the known Indo-Pacific king mackerel, Scomberomorus hosts, S. melanostictus and E. japonicus, occur guttatus (Bloch & Schneider, 1801) (Trilles et in the waters around our sampling site, and in- al., 2011), both from
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