Crustacean Research 49: 15-21 (2020)
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Crustacean Research 2020 Vol.49: 15–21 ©Carcinological Society of Japan. doi: 10.18353/crustacea.49.0_15 Areolate grouper, Epinephelus areolatus (Perciformes: Serranidae), a new host record for Lernaeenicus ramosus (Copepoda: Pennellidae), with comments on the known hosts and distribution records of the copepod in the Indo-West Pacific region Kazuya Nagasawa, Kenyu Suzuki, Fumihito Muto Abstract.̶ An ovigerous female of Lernaeenicus ramosus Kirtisinghe, 1956 was collected from an areolate grouper, Epinephelus areolatus (Forsskål, 1775), in coastal waters of Suruga Bay (western North Pacific Ocean), Shizuoka Prefecture, central Ja- pan. This represents a new host and the easternmost distribution records for L. ramo- sus. Based on the literature published between 1956 and 2019, this paper tabulates the known hosts and distribution records of the species in the Indo-West Pacific region. The recent collections of L. ramosus from Japan further support a previous suggestion that the geographical distribution of the species in Japanese waters is affected by two warm currents, the Kuroshio, and its branch, the Tsushima Current. Key words: fish parasite, geographical distribution, host range, pennellid, Serranidae The pennellid copepod Lernaeenicus ramo- ramosus from an areolate grouper, Epinephelus sus Kirtisinghe, 1956 is a mesoparasite of per- areolatus (Forsskål, 1775), in Suruga Bay ciform fishes in the Indo-West Pacific region (western North Pacific Ocean), Shizuoka Pre- (Nagasawa & Uyeno, 2014). The species was fecture, central Japan. This represents a new originally described using females from comet host and the easternmost distribution records grouper, Epinephelus morrhua (Valenciennes, for L. ramosus. The species has been well re- 1833), in the Indian Ocean off Ceylon (now Sri described by Shiino (1958) and Izawa (2019) Lanka) (Kirtisinghe, 1956) and since has been using specimens from Japan. Thus, this paper reported from groupers in India (Pillai, 1985) briefly reports on the morphology of L. ramo- and Japan (see below) and from bluestriped sus from the bay and, based on the literature fangblenny, Plagiotremus rhinorhynchos published between 1956 and 2019, gives a list (Bleeker, 1852) (as Runula rhinorhynchus) in of the known hosts and collection localities of Australia (Boxshall, 1986). the species. Much information has been accumulated on An areolate grouper was caught using rod various aspects of the biology, such as taxono- and line in coastal waters of Suruga Bay off my, geographical distribution, host range, lar- Miho, Shimizu (35°02′02.1″N,138°52′45.5″E), val development, and pathogenicity, of L. ra- Shizuoka Prefecture, on 19 September 2019. mosus in Japan, where the groupers are known The fish was transported alive to the laboratory to serve as hosts of the species (Shiino, 1958, of the School of Marine Science and Technolo- 1964; Anonymous, 2004; Doi, 2007; Doi et al., gy, Tokai University, Shimizu, where it was 2008; Nagasawa et al., 2010, 2011, 2014; Oka- measured for standard length (SL, mm) and ex- moto, 2011; Nitta et al., 2017; Izawa, 2019). amined for ecto- and endoparasites. One cope- Recently, we collected an adult female of L. pod was found, removed carefully, and fixed in Received: 20 Oct 2019. Accepted: 25 Dec 2019. Published online: 13 Feb 2020. 15 KAZUYA NAGASAWA ET AL. 70% ethanol. Later, at the Aquaparasitology well developed, nearly elongated, and ends Laboratory, Shimizu, the copepod was exam- bluntly without caudal rami (Fig. 2A). ined for its morphology and identified as L. ra- Lernaeenicus ramosus was described from mosus. A drawing was made with the aid of a Sri Lanka (Kirtisinghe, 1956). Later, the spe- drawing tube fitted on an Olympus SZX10 ste- cies was redescribed by Shiino (1958) and, reo microscope. The specimen preserved in again, by Izawa (2019) based on the material 70% ethanol is deposited in the Crustacea (Cr) from Japan. Pillai (1985) and Boxshall (1986) collection of the National Museum of Nature also described the species using specimens and Science, Tsukuba, Ibaraki Prefecture from Indian and Australia, respectively. All (NSMT-Cr 26743). The scientific and common these authors examined metamorphosed fe- names of fishes mentioned in this paper follow males. Izawa (2019) stated that the females Froese & Pauly (2019). from Sri Lanka, Japan, and Australia are mor- An ovigerous female of L. ramosus inserted phologically identical to each other. No mor- the anterior part of its body into the host phological difference is observed between the (132 mm SL) near the base of the dorsal fin. specimen examined in this study and those re- This anterior part was embedded in the host ported by Shiino (1958) and Izawa (2019). musculature. The posterior part of the female However, it is desirable to identify the species, protruded externally and was deep purple in using molecular data as well, from these three color when fresh (arrowhead in Fig. 1). countries and India, because Japan and Austra- Description of female: The anterior part of lia are far separated from Sri Lanka and India the body consists of the head, 2.0 mm long, and it parasitizes groupers in Sri Lanka, India, with three pairs of branching holdfasts and a and Japan but does not in Australia. Nitta et al. slender, cylindrical neck, 2.6 mm long (Fig. 2). (2017) successfully obtained molecular data of The anterior and the middle pairs arise, respec- L. ramosus from Hong Kong grouper, Epi- tively, from the dorsolateral and the ventrolat- nephelus akaara (Temminck & Schlegel, eral corners in the anterior portion of the head, 1842), in Japan. while the posterior pair does from the lateral Excluding the blenniid fish from Australia surface in the posterior portion of the head (Boxshall, 1986), the other known hosts are all (Fig. 2B, C). Each holdfast is swollen near its groupers (Serranidae). The areolate grouper is base and possesses slender branches. The pos- added herein as a new host of L. ramosus, and terior part of the body comprises the trunk and a total of eight species of groupers is now the abdomen: the former is longer (7.0 mm known as its hosts (Table 1, seven species from long) than the latter (4.8 mm long), which is Japan; one species from Sri Lanka and India). It is evident that L. ramosus almost exclusively uses groupers as its hosts, and Nagasawa et al. (2014) have suggested that the species will be discovered from other species of groupers in Japan, where they (subfamily Epinephelinae) consist of 65 species in 10 genera (42 spp. in Epinephelus, 12 spp. in Cephalopholis, 3 spp. in Plectropomus, 2 spp. in Variola, 1 sp. each Fig. 1. Areolate grouper, Epinephelus areolatus, infected by in Aethaloperca, Anyperodon, Chromileptes, Lernaeenicus ramosus (arrowhead) near the base of the dorsal Gracila, Saloptia, and Triso) (Senou, 2013). fin, fresh specimen. The fish was caught in coastal waters of Suruga Bay off Miho, Shizuoka Prefecture, central Japan, on We need to explain that E. morrhua is listed 19 September 2019. Scale bar: 10 mm. in Table 1 as the host of L. ramosus from India. 16 Crustacean Research 49 NEW HOST RECORD FOR A PARASITIC COPEPOD Fig. 2. Lernaeenicus ramosus, ovigerous female, NSMT-Cr 26743, from Epinephelus areolatus, caught in coastal waters of Suruga Bay off Miho, Shizuoka Prefecture, Japan. A, habitus, ventrolateral view; B, head and neck, ventrolateral view; C, head and anterior part of neck, dorsolateral view. The photographs were taken immediately after the specimen was fixed in 70% ethanol. Abbreviations: ap, anterior pair of holdfast; h, head; mp, middle pair of holdfast; n, neck; pp, posterior pair of holdfast. Scale bars: A, 4 mm; B–C, 2 mm. In his monograph of the parasitic copepods of and India (Pillai, 1985) should have been list- India, Pillai (1985: 721) reported three species ed. Moreover, Raja et al. (2016: table 3) in- of groupers (E. morrhua, E. akaara, E. tsirime- cluded the Japanese threadfin bream, “Nemip- naria) as the hosts of L. ramosus from Sri Lan- terus japonicus (Block, 1791)” (Nemipteridae) ka, India, and Japan but did not specify the In- among Indian hosts of L. ramosus. This fish dian host. However, the latter two species are species (as “red snapper, Synagris japonica the Japanese hosts (Shiino, 1958), thus the re- Day”) was reported by Rangnekar (1961) to maining species, E. morrhua, can be regarded harbor “L. ramosus” off Bombay (now Mum- as the Indian host, as earlier reported from Sri bai), but the copepod collected was not L. ra- Lanka (Kirtisinghe, 1956). mosus but Lernaeenicus nemipteri Gnana- Raja et al. (2016: table 3) listed the red grou- muthu, 1953 (see Pillai, 1985: 721–722). The per “Epinephelus morio (Valenciennes in Cuvi- Japanese threadfin bream is apparently not the er & Valenciennes, 1826)” as one of the hosts host of L. ramosus. of L. ramosus but it is wrong: E. morio is a Lernaeenicus ramosus has been reported species found only in the western Atlantic from off Sri Lanka, India, Australia, and Japan Ocean (Froese & Pauly, 2019) and E. morrhua (Table 1). While no detailed information on the reported from Sri Lanka (Kirtisinghe, 1956) collection locality of the species in India is Crustacean Research 49 17 18 KAZUYA NAGASAWA ET AL. ET NAGASAWA KAZUYA Table 1. Known hosts and collection localities of Lernaeenicus ramosus. The scientifc and common names of the fishes listed follow Froese & Pauly (2019). Crustacean Research 49 Crustacean Research Host Collection locality Number Reference Family Genus and species Common name Country Locality in Fig. 2 Serranidae Epinephelus morrhua (type host) Comet grouper Sri Lanka Wadge Bank (type locality) Kirtisinghe (1956) Epinephelus morrhua Comet grouper India Not reported Pillai (1985)* Epinephelus akaara Hong Kong grouper Japan Momotori, Mie 2 Shiino (1958, as E. tsirimenaria [sic]) Kobe, Hyogo 6 Doi (2007), Doi et al. (2008) Amakusa-nada Sea, Kumamoto 8 Nitta et al.