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Research 2017 Vol.46: 153–159 ©Carcinological Society of Japan. doi: 10.18353/crustacea.46.0_153 Three new host records for the marine fish ectoparasite, Nerocila phaiopleura (Isopoda: Cymothoidae), with a list of its known hosts

Kazuya Nagasawa, Susumu Isozaki

Abstract.̶ The cymothoid isopod Nerocila phaiopleura Bleeker, 1857 is a skin par- asite of actinopterygian fishes in the Indo-West Pacific. The isopod is reported from three species of fishes, viz., Japanese barracuda, Sphyraena japonica Bloch & Schnei- der, 1801 (Sphyraenidae), Japanese jack , japonicus (Temminck & Schlegel, 1844) (), and round herring, (Temminck & Schlegel, 1846) (), in coastal waters of the northwest Pacific Ocean off Mie Prefecture, central Japan. These three fish species represent new host records for N. phaiopleura. Based on the literature published between 1857 and 2017, 44 nominal and some unidentified species in four orders and 14 families of fishes have been re- ported as the hosts of N. phaiopleura, and 18 nominal species of them belong to two clupeiform families (10 spp. in and 8 spp. in Engraulidae). This indicates that N. phaiopleura utilizes a wide variety of fish species as its hosts but prefers the fishes of the two families. The infected fish examined in this study had a large skin wound caused by N. phaiopleura.

Key words: fish parasite, host list, host utilization

Nerocila phaiopleura Bleeker, 1857 is a skin versity, where they were thawed and identified. parasite of actinopterygian fishes in the Indo- They were fixed and preserved in 70% ethanol. West Pacific (e.g., Bruce, 1982, 1987; Bowman The scientific and common names of fishes & Tareen, 1983; Bruce & Harrison-Nelson, used in this paper follow Froese & Pauly 1988; Trilles et al., 2011, 2013; Aneesh et al., (2017), except for Japanese , Sardinop- 2013; Nagasawa & Shirakashi, 2017). During a sis melanostictus (Temminck & Schlegel, study of cymothoid infection of fishes in coast- 1846), which follows Nakabo (2013). To make al waters of the northwest Pacific Ocean off a list of the known hosts of N. phaiopleura, Mie Prefecture, central Japan, we collected N. several local papers from were not avail- phaiopleura from three fish species, which rep- able in this study. However, citing such local resent new host records for the isopod. papers, information on the Indian known hosts Fishes were commercially caught in June was compiled by Trilles et al. (2011: table 1), 2016 and July 2017 with a set net installed in which is cited herein for the list. Kowaura Bay off Maruwa (34°13′33″N, 136° Specimens of N. phaiopleura were collected 29′00″E), Minami-Ise, Mie Prefecture. After from three species of fishes: one ovigerous fe- capture, fishes were identified and examined male from a Japanese barracuda, Sphyraena ja- macroscopically for the presence or absence of ponica Bloch & Schneider, 1801 (Sphyraeni- ectoparasites. When cymothoid isopods were dae) (Fig. 1A, 1D) on 12 July 2016; one found, infected fishes were photographed, and ovigerous female from a Japanese jack mack- the isopods were frozen with sea water and erel, Trachurus japonicus (Temminck & Schle- transported to the laboratory of Hiroshima Uni- gel, 1844) (Carangidae) (Fig. 1B, 1E, 1F) on

Received: 4 Sept 2017. Accepted: 16 Oct 2017. Published online: 14 Nov 2017. 153 KAZUYA NAGASAWA, SUSUMU ISOZAKI

Fig. 1. Fishes infected with Nerocila phaiopleura from coastal waters of the northwest Pacific Ocean off Mie Prefecture, central Japan. A, Japanese barracuda, Sphyraena japonica; B, , Trachurus japonicus; C, round herring, Etrumeus micropus; D, ovigerous female of N. phaiopleura, NSMT-Cr 25572, on S. japonica; E, ovigerous female of N. phaiopleura, NSMT- Cr 25573, on T. japonicus; F, same female of N. phaiopleura and a wound of T. japonicus. Scale bars: 40 mm in A–C; 10 mm in D–F.

11 June 2017; and one ovigerous female from a the Indo-West Pacific, including South , round herring, Etrumeus micropus (Temminck Kuwait, , India, Thailand, Singapore, & Schlegel, 1846) (Dussumieriidae) (Fig. 1C) , Australia, China, and Japan (Table on 7 July 2017. Isopods were all found to be 1). The three species, viz., S. japonica, T. attached to the posterior body surface of these japonicus, and E. micropus, which were found fishes. The specimens of N. phaiopleura col- to harbor N. phaiopleura in this study, are add- lected are identical with those of N. phaiopleu- ed herein as its new hosts. In Japan, in addition ra described by Bowman & Tareen (1983), to these three newly added species, the follow- Bruce (1987), and Nagasawa & Shirakashi ing seven species have been reported before as (2017), measuring 21.1–22.8 (mean 21.8) mm the hosts: dotted gizzard shad, Konosirus punc- in total length (with uropod rami) and 8.0–10.0 tatus (Temminck & Schlegel, 1846); Japanese (9.0) mm in maximum width (n＝3). Voucher sardinella, Sardinella zunasi (Bleeker, 1854); specimens of isopods are deposited in the Japanese sardine, Sardinopsis melanostictus (all Crustacea (Cr) collection of the National Mu- Clupeidae); Japanese , Engraulis seum of Nature and Science, Tsukuba, Ibaraki japonicus Temminck & Schlegel, 1846 (En- Prefecture, Japan (NSMT-Cr 25572–25573). graulidae); , japonicus Based on the literature published between Houttuyn, 1782; Japanese , 1857 and 2017, a total of 44 nominal and some niphonius (Cuvier, 1832); and unidentified species in four orders and 14 fami- Pacific bluefin , Thunnus orientalis (Tem- lies of actinopterygian fishes has so far been minck & Schlegel, 1844) (all ) (Ta- reported as the hosts of N. phaiopleura from ble 1). The first four species are listed in a re-

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Table 1. Known hosts of Nerocila phaiopleura. The orders of fishes are arranged based on their systematics. Fish species in each family are shown in alphabetical order.

Order Family Species Common Name Country Reference

Clueiformes Chirocentridae Chirocentrus dorab dorab wolf-herring South Africa Barnard (1925) Kuwait Bowan & Tareen (1983) India Ravichandran et al. (2001), Trilles et al. (2011: table 1), Trilles et al. (2013) Chirocentrus nudus whitefin wolf-herrnig Pakistan Ghani (2003) India Raja et al. (2014) Chirocentrus sp. wolf-herring Thailand Bruce & Harrison-Nelson (1988) Clupeidae sp. herring Thailand Bruce & Harrison-Nelson (1988) Konosirus punctatus dotted gizzard shad Japan Mitani (1982) Sardinella albella white sardinella India Bharadhirajin et al. (2014) China Morton (1974, as S. peforata) Sardinella brachysoma deepbody sardinella India Trilles et al. (2011: table 1) Saldinella fimbriata fringescale sardinella Thailand Bruce & Harrison-Nelson (1988) Sardinella gibbosa goldstripe sardinella China Morton (1974) India Rameshkumar et al. (2013a), Trilles et al. (2013) Sardinella longiceps Indian oil sardine India Trilles et al. (2011: table1), Trilles et al. (2013), Rameshkumar et al. (2016b) Sardinella sindensis sind sardinella India Trilles et al. (2011: table 1) Sardinella zunasi Japanese sardinella Japan Mitani (1982) China Bruce (1982, as Harengula zunasi) Sardinella sp. sardinella Thailand Bruce & Harrison-Nelson (1988, as Harengula sp.) Sardinopsis melanostictus Japanese sardine Japan Mitani (1982), Williams & Bunkley-Williams (1986), Bruce & Harrison-Nelson (1988), Hiramoto (1996), Saito & Hayase (2000), Nunomura (2011), Hata et al. (2017) Spratelle kowale* Indonesia Bleeker (1857) Spratelle tembang* Indonesia Bleeker (1857) Tenualosa ilisha hilsa shad India Trilles et al. (2013) Dussumieriidae acuta Thailand Monod (1934) Kuwait Bowan & Tareen (1983) India Trilles et al. (2011: table 1), Trilles et al. (2013), Ravichandran & Rameshkumar (2014) Dussumieria elopsoides China Morton (1974, as D. hasselti) Etrumeus micropus round herring Japan This paper Engraulidae Engraulis australis Australian anchovy Australia Bruce (1987) Engraulis japonicus Japanese anchovy Japan Mitani (1982), Bruce & Harrison-Nelson (1988) Engraulis sp. anchovy Thailand Bruce & Harrison-Nelson (1988) Stoleophorus commersonnii Commerson's anchovy India Rajkumar et al. (2006, 2007, as S. commersonii), Trilles et al. (2011: table 1) Stoleophorus indicus Indian anchovy Indonesia Bruce (1987) dussumieri Dussumier's thryssa India Trilles et al. (2011: table 1), Bharadhirajin et al. (2014) Thryssa malabarica Malabar thryssa India Aneesh et al. (2013) Thryssa mystax moustached thryssa India Trilles et al. (2011: table 1), Aneesh et al. (2013), Trilles et al. (2013) Thryssa setirostris longjaw thryssa India Aneesh et al. (2013) Pristigasteridae Illisha melastoma Indian illisha Singapore Bruce & Harrison-Nelson (1988) India Bruce & Harrison-Nelson (1988) Opisthopterus tardoore tardoore India Aneesh et al. (2013)

Mugiliformes Mugilidae Chelon parsia goldspot mullet India Bharadhirajin et al. (2014, as Liza parsia) Liza argentea flat-tail mullet Indonesia Bruce (1987) Australia Bruce (1987)

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Table 1. Continued.

Order Family Species Common Name Country Reference

Siluriformes Ariidae Arius jella blackfin sea catfish India Trilles et al. (2011: table 1) Plotosidae Cnidoglanis macrocephalus cobbler Australia Bruce (1987, as Cnidoglannus macrocephalus)

Perciformes Carangidae Carangoides malabaricus Malabar trevally India Trilles et al. (2013) Carangoides sp. trevally India Rameshkumar et al. (2013b), Trilles et al. (2013), Rameshkumar et al. (2016a) Decapterus maruadsi Japanese scad China Morton (1974) Parastromateus niger black pomfret India Bruce & Harrison-Nelson (1988) Selaroides leptolepis yellowstripe scad India Trilles et al. (2013) Trachurus japonicus Japanese jack mackerel Japan This paper Istiophoridae Istiophorus platypterus** Indo-Pacific sailfish India Barnard (1936, as Histiophorus gladius) Leiognathidae Eubleekeria splendens splendid ponyfish India Trilles et al. (2013, as Leiognathus splendens) Gazza minuta toothpony India Trilles et al. (2013) Polynemidae Polynemus sp. threadfin Indonesia Trilles (1979) Scombridae kanagurta India Rameshkumar & Ravichandran (2010), Trilles et al. (2013) Scomber japonicus chub mackerel Japan Nagasawa & Nakao (2017) Scomberomorus guttatus Indo-Pacific India Trilles et al. (2011: table 1) Scomberomorus niphonius Japanese Spanish mackerel Japan Nagasawa & Tensha (2016), Hata et al. (2017) Thunnus orientalis Pacific bluefin tuna Japan Shirakashi (2013), Nagasawa & Shirakashi (2017) Sphyraenidae Sphyraena japonica Japanese barracuda Japan This paper Sphyraena jello pickhandle barracuda India Trilles et al. (2013)

* These fishes are probably species of (Bowan & Tareen, 1983: 7). ** The record from this fish was regarded as an error by Bruce (1987: 384). Both Bowman & Tareen (1983: 7) and Bruce (1987: 384) reported this fish as Xiphias gladius. view of Japanese cymothoids by Yamauchi through extensive survey. In addition, there are (2016), while the remaining three species were some differences in host species composition reported by the senior author (KN) and col- between countries. For example, six species of leagues (Nagasawa & Tensha, 2016; Nagasawa Clupeidae are known as the hosts of N. phaio- & Shirakashi, 2017; Nagasawa & Nakao, pleura in India, but only three species of the 2017). Hata et al. (2017) also collected N. family serve as its hosts in Japan (Table 1). phaiopleura from S. niphonius. This difference may be explained by a differ- Of the 44 nominal host species listed in Table ence in the clupeid fauna between both coun- 1, 19 (43.2%) belong to the order Cluepiformes tries: as many as 46 species of clupeids are dis- (Clupeidae [10 spp.], Engraulidae [8 spp.], and tributed in the (Froese & Pauly, Dussumieriidae [1 sp.]), which indicates that N. 2017), while only 16 clupeids occur in Japa- phaiopleura utilizes a wide variety of fish spe- nese waters (Nakabo, 2013). In other words, cies as its hosts but prefers the fishes of this or- the difference in host range of N. phaiopleura der, especially those of the first two families. between countries is affected by the fish fauna Since the two newly added hosts (S. japonica of individual countries. and T. japonicus) are not clupeiform fishes, The attachment site of N. phaiopleura ob- they may not serve as suitable hosts for N. served in this study was the posterior body sur- phaiopleura to maintain the parasite’s popula- face of fishes, especially an area surrounded by tion in Japanese waters. the lateral line and the anal fin (Fig. 1A–1F). As demonstrated in this study, N. phaiopleu- This location was the same in different species ra is not a host-specific parasite. It is thus like- of the fishes examined, indicating that the pos- ly that the species is found on other fish species terior body surface is the most preferred attach-

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ment site of N. phaiopleura. Morton (1974) Barnard, K. H., 1936. Isopods collected by the R. obtained a similar result on the location of the I. M. S. “Investigator.” Records of the Indian species in Chinese fishes. Museum, Calcutta, 38: 147–191. The fish infected by an ovigerous female of Bharadhirajan, P., Murugan, S., Sakthivel, A., & N. phaiopleura examined in this study had a Selvakumar, P., 2014. Isopods parasites in- large wound at the attachment site. The wound fection on commercial fishes of Parangipet- was as large as the parasite (Fig. 1E, 1F), and tai waters, southeast coast of India. Asian probably due to its feeding and/or the deep in- Pacific Journal of Tropical Disease, 4: sertion of the pereopod’s dactyli, the host’s skin S268–S272. disappeared (Fig. 1F). The same disease condi- Bleeker, P., 1857. Recherches sur les Crustacés de l’Inde Archipelagique. II. Sur les Isopodes tion caused by N. phaiopleura has been found Cymothoadiens de l’Archipel Indien. Ver- in China (Morton, 1974) and India (Raja et al., handelingen der Natuurkundige Vereeniging 2014; Ravichandran & Rameshkumar, 2014) as in Nederlandsch-Indië, 2: 20–40, 2 pls. well as in Japan, and the parasite is also known Bowman, T. E., & Tareen, I. U., 1983. Cymothoi- to induce secondary bacterial infections in In- dae from fishes of Kuwait (Arabian Gulf) dia (Ravichandran et al., 2001; Rajkumar et (Crustacea: Isopoda). Smithsonian Contribu- al., 2007). Based on these facts, N. phaiopleura tion to Zoology, 382: 1–30. can be regarded as an important pathogenic Bruce, N. L., 1982. On a small collection of ma- parasite of coastal marine fishes in these coun- rine Isopoda (Crustacea) from Hong Kong. tries. In addition, the infected individual of S. In: B. S. Morton & C. K. Tseng, (eds.), Pro- japonica had an abnormally shaped body ceedings of the First International Marine around the attachment site of N. phaiopleura Biological Workshop: The Marine Flora and (Fig. 1A, 1D), but it is unknown at present Fauna of Hong Kong and Southern China, whether the parasite’s infection can cause such Vol. 1, Hong Kong University Press, Hong a condition. Kong, pp. 315–324. Bruce, N. L., 1987. Australian species of Nerocila ■ Acknowledgments Leach, 1818, and Creniola n. gen. (Isopoda: Cymothoidae), crustacean parasites of ma- We thank the captain and crews of the fishing rine fishes. Records of the Australian Muse- vessel Ryosyo-maru for their assistance during um, 39: 355–412. fish sampling. Bruce, N. L., & Harrison-Nelson, E. B., 1988. New records of fish parasitic marine isopod ■ Literature Cited (Cymothoidae, subfamily Anilo- crinae) from the Indo-West Pacific. Proceed- Aneesh, P.-T., Sudha, K., Arshad, K., Anilkumar, ings of the Biological Society of Washing- G., & Trilles, J.-P., 2013. Seasonal fluctua- ton, 101: 585–602. tion of the prevalence of cymothoids repre- Froese, R., & Pauly, D., (eds.), 2017. FishBase. senting the genus Nerocila (Crustacea, Isop- (URL: http://www.fishbase.org/) (accessed oda), parasitizing commercially exploited 15 July 2017) marine fishes from the Malabar Coast, India. Ghani, N. A. S. E. E. M., 2003. Isopod parasites Acta Parasitologica, 58: 80–90. of marine fishes of Pakistan. Proceedings of Barnard, K. H., 1925. Contributions to the crusta- Pakistan Congress of Zoology, 23: 217–221. cean fauna of South Africa. No. 9. Further Hata, H., Sogabe, A., Tada, S., Nishimoto, R., addition to the list of Isopoda. Annals of the Nakano, R., Kohya, N., Takeshima, H., & South African Museum, 20: 381–412. Kawanishi, R., 2017. Molecular phylogeny

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