Caligus sclerotinosus (Copepoda: Caligidae), a serious pest of cultured red seabream Pagrus major (Sparidae) in Korea

Veterinary Parasitology 188 (2012) 355–361

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Caligus sclerotinosus (Copepoda: Caligidae), a serious pest of cultured red seabream Pagrus major (Sparidae) in Korea B.A. Venmathi Maran a,∗ , Sung-Yong Oh a , Ho Young Soh b , Hee Jung Choi a , Jung-Goo Myoung a a Marine Biology and Living Resources Research Department, Korea Ocean Research and Development Institute, Ansan, P.O. Box 29, Seoul 425-600, Republic of Korea b Faculty of Marine Technology, Chonnam National University, San 96-1, Dundeog-dong, Yeosu, Jeollanamdo 550-749, Republic of Korea

a r t i c l e

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Article history: Received 30 December 2011 Received in revised form 15 March 2012 Accepted 16 March 2012 Keywords: Sea lice Copepod Infestation Prevalence Chalimus Host switching

a b s t r a c t Caligid copepods (Crustacea) known as sea lice are pests of cultured fish, causing serious diseases and economic losses in fish aquaculture worldwide. One species, Caligus sclerotinosus Roubal, Armitage & Rohde, 1983 (Caligidae), is considered a serious pest of the highly prized red seabream Pagrus major (Temminck and Schlegel, 1843) (Sparidae) cultured in Japan. Recently, in neighboring Korea, red seabream culture has intensified and almost replaced yellow tail culture. However, until now, there have been no reports on infection of this sea louse from red seabream in Korea. We surveyed 120 (20 fish per month) P. major from a sea ranched Tongyeong Marine Research Center aquaculture facility, Gyeongsangnamdo, Korea for six months in 2011 (June to November). We recorded severe infection by the sea louse C. sclerotinosus on the skin of P. major. Prevalence was 100%, mean intensity 7.06, maximum intensity 49, and minimum intensity 2. Adult females (624), males (219) and few chalimi (5) were observed and identified by their morphology. As an average of all our collections, less than 0.6% of individuals were chalimi. We suggest, therefore, that adults of C. sclerotinosus undergo ontogenetic host switching after their final moult. No infection of C. sclerotinosus was found on wild P. major collected from Tongyeong and Yeosu fish markets on the southern coast of Korea. Severe infection by this sea louse may cause secondary infections of the host. This copepod is already reported from Australia and Japan and hence, this is the first report from Korea. We expect this pest to have an impact on Korean red seabream fisheries equally serious to that being experienced in Japan. © 2012 Elsevier B.V. All rights reserved.

1. Introduction Over-exploitation and decline of wild marine fisheries (Hutchings, 2000; Worm et al., 2006) led to the rapid expansion of marine aquaculture worldwide (FAO, 2010). In commercial aquaculture, sea lice have been considered

∗ Corresponding author at: Korea Ocean Research and Development Institute, Ansan P.O. Box 29, Seoul 425-600, Republic of Korea. Tel.: +82 31 400 6281; fax: +82 31 406 2882. E-mail addresses: [email protected], [email protected] (B.A. Venmathi Maran). 0304-4017/$ – see front matter © 2012 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2012.03.023

as serious pests of marine finfish (Rosenberg, 2008) that cause significant health problems in mariculture, particularly to marine salmonid farming (Johnson et al., 2004; Nowak et al., 2011). In net cage fish farms, fish are likely to be infected by parasites from wild fishes. Since they are rather concentrated in their net cages they can become a source of parasite propagation and dispersal (Nowak, 2007). Infestation of parasites that in turn also cause secondary infections of cultured marine fishes led to economic losses in marine aquaculture (Johnson et al., 2004; Costello, 2009). In Asia, there are 90 species of Caligus and 33 species of Lepeophtheirus that have been reported from cultured and

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Fig. 1. Map showing the localities at Tongyeong (Gyeongsangnamdo) and Yeosu (Jeollanamdo) where cultured and wild red seabream Pagrus major were collected; on the right side, enlarged map of Tongyeong city marked in red with 3 localities: (1) Tongyeong Marine Research Center; (2) Fish farm 1; (3) Fish farm 2. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

wild marine fish (Ho, 2000). These include more than 90 species of sea lice from Taiwan (Ho and Lin, 2004), India (Pillai, 1985), and Japan (Ho, 2000; Nagasawa et al., 2010). However, in Korea infections of sea lice have not been as extensively surveyed as in Japan and Taiwan. According to Kim (2008) there are 14 species of Caligus and 10 species of Lepeophtheirus and 1 species of Pseudocaligus that so far have been reported from both cultured and wild marine fin fish in Korea. In Southeast Asia floating net cage culture is extensively developed and expanding rapidly (Ho, 2000; MuhdFaizul et al., 2011). Likewise, aquaculture in East Asia, including Korea, is flourishing with the development of advanced aquaculture scientific technology for important marine finfish such as, olive flounder Paralichthys olivaceus (Temminck and Schlegel, 1846), Korean rockfish Sebastes schlegelii Hilgendorf, 1880, red seabream Pagrus major (Temminck and Schlegel, 1843), blackhead seabream Acanthopagrus schlegelii schlegelii (Bleeker, 1854), and flathead grey mullet, Mugil cephalus Linnaeus, 1758. These have been cultured since the late 1980s in Korea (Yoon, 2008). Production losses due to infections by various diseases increased in recent years (Park, 2009). Red seabream culture began in the early 1970s. Compared to yellowtail, red seabream is a slow growing fish and therefore was an ancillary culture species to yellowtail in Korea. However, recently it attracted considerable attention as a result of slow growth rate and mortality in winter affecting the culture of yellowtail (Kim, 2000). Considering its ongoing and future potential importance, we thoroughly checked for the presence of parasites on red seabream at the sea ranched area of Tongyeong Marine Research Center (TMRC), and in net cage culture facilities and in fish markets around Tongyeong and Yeosu on the southern coast of Korea. The aim of our study was to reveal infections of the sea louse Caligus sclerotinosus Roubal, Armitage & Rohde, 1983 on red

seabream, which is considered a serious pest of cultured red seabream in Japan (Ho et al., 2004; Ohtsuka et al., 2009). 2. Materials and methods Red seabream P. major (Sparidae) were sea ranched at Tongyeong Marine Research Center (TMRC) and cultured in net cage fish farms at Tongyeong, Gyeongsangnamdo, Korea (Fig. 1). At Tongyeong MRC, red seabream sampling was carried out from June to November 2011. P. major (120 individuals – over six months) of different sizes were collected randomly and screened for sea lice and other parasites. We received samples to check the infection of sea lice from two fish farms located at Tongyeong. Sea lice were located on the body surface of P. major from all three different localities. They were removed from the skin of the fish hosts using fine forceps under a dissecting microscope and preserved in 70% ethanol. Prevalence and mean intensity were calculated. To detect small and immature parasites, the fins were checked and also the gills were dissected and separated into the 4 arches and examined in petridishes containing 70% ethanol under a dissecting microscope. All sediments (scales, mucous and dissection debris) settling in preservative solutions were also retained and checked for any detached parasite or developmental stages under the microscope. The sampling of wild red seabream was carried out at Tongyeong and Yeosu (Jeollanamdo) fish markets, Korea. They were screened for the infection of the sea louse. Preserved sea lice were cleared in a drop of 85% lactic acid or lactophenol prior to examination using an Olympus CX41 (Tokyo) phase contrast microscope for identification. Selected specimens were measured intact using an ocular micrometer and/or dissected and examined according to the wooden slide procedure of Humes and Gooding (1964). Measurements are made from the body length of the copepods and given as

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Fig. 2. (A) Ranched red seabream Pagrus major found with the infection of sea lice on the body surface/skin; (B) Arrows show the severe infection of Caligus sclerotinosus; (C) Adult C. sclerotinosus female; (D) Male; (E) Chalimus III stage, male. Scale bars: (A) – 6 cm; (C) and (D) – 0.8 mm; (E) – 0.4 mm.

means followed by their range in parentheses. The common and scientific names of host fishes follow Froese and Pauly (2011). Voucher specimens are deposited at the National Institute of Biological Resources (NIBR) Museum, Incheon, Korea.

3.1. Diagnosis of C. sclerotinosus Adult female. Body (Fig. 2C) 2.94 (2.79–3.07) mm long (n = 10) (NIBRIV0000245079). Cepahalothorax shield subcircular, slightly wider than long; fourth pediger wider than long; genital complex wider than long with broadly protruded posterolateral corners carrying seta bearing process

3. Results A total of 848 sea lice were collected from cultured red seabream (Fig. 2A and B) at sea ranched Tongyeong MRC, 22 and 13 sea lice from fish farm 1 and fish farm 2, respectively. These all belonged to the species C. sclerotinosus (Copepoda: Siphonostomatoida: Caligidae) (Fig. 2C and D). It was identified by following their most prominent characteristic features: a sclerotized body, short and broad sternal furca, and setation/armature of leg 4. The total number of C. sclerotinosus including their sexes during a period of six months from June to November, 2011 at Tongyeong MRC is elucidated (Fig. 3). More detailed information on the infestation of C. sclerotinosus as well as the presence of other parasitic copepods and monogeneans are tabulated for all stations such as: TMRC, fish farm 1, fish farm 2, and fish markets (Tongyeong and Yeosu) (Table 1).

Fig. 3. Total number of infected Caligus sclerotinosus and its sexes on the red seabream Pagrus major for the period of six months at sea ranched Tongyeong Marine Research Center in 2011.

C. sargi

C. sargi

–

0 0 0 10 Wild

N, number; T, total; F, female; M, male; C, chalimus; P, prevalence; MI, mean intensity; Max, maximum intensity; Min, minimum intensity.

0

10 Wild

308–376

June to November

0

0

0

0

0 0 0 0 0 0 284–375

June to November

0

0

0 3 (23.1) 10 (76.9) 260–343 5 Net cage

7 September

13

0 6 (27.3) 200–264 5 Net cage

Tongyeong fish farm 1 Tongyeong fish farm 2 Tongyeong fish market Yeosu fish market

7 September

22

16 (72.7)

100

2.6

6

2

Anoplodiscus sp. Benedenia sp. Anoplodiscus sp. Benedenia sp. Unidentified monogenea Unidentified monogenea 2 10 4.4

2 49 7.06 5 (0.6) 219 (25.8)

100 C M F

160–365 Sea ranched 120 Tongyeong Marine Research Center

June to November

848

624 (73.6)

100

Anoplodiscus sp. Benedenia sp. Choricotyle sp.

Fins Max Min Gills T

Sex (%)

P (%) MI

Other parasites Caligus sclerotinosus infestation Date Host-body length (mm) N Facility Locality

Table 1 Caligus sclerotinosus infestation and information on other parasites on the cultured and wild red seabream Pagrus major at southern coast of Korea in 2011.

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Clavellotis sargi Clavella sp. 1 Clavella sp. 2

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with leg 5; abdomen small, short, wider than long; caudal ramus armed with 2 long and 4 short setae in irregular length; leg 5 with 2 papillae bearing 1 and 2 setae, respectively; sternal furca short with broad tines. Adult male. Body (Fig. 2D) 2.37 (2.31–2.43) mm long (n = 10) (NIBRIV0000245079). Cephalothorax shield subcircular; fourth pedigerous somite wider than long; genital complex wider than long with prominent posterolateral processes, armed with 1 subterminal and 2 terminal setae distally; abdomen small, wider than long; caudal ramus with row of long setules subterminally on inner margin, armed with 6 plumose setae, 3 long terminally and 3 short subterminally. Chalimus. Body (Fig. 2E) 1.23 (1.22–1.24) mm long (n = 5). Attached on the host near the caudal and anal fins. Body showing development of caligid cephalothorax with incorporation of third pedigerous somite; frontal plates development visible; cephalothorax subcircular, wide, 2.5 times longer than posterior somites combined; frontal filament with three basal bulbs; genital complex slightly wider; caudal setae plumose. The sexual dimorphism of developmental stages are expressed from III stage of the chalimus, could be differentiated through the feature of antenna (Ho and Lin, 2004; Ohtsuka et al., 2009). Antenna is with rounded process distally in male, but acutely pointed in female. Body and other appendages are similar for both the sexes. 4. Discussion Until now, no parasitic copepods have been reported from the sparid, red seabream P. major, cultured in Korea, whereas a few have been recorded from wild P. major (Kim, 1998). The present study revealed the C. sclerotinosus from the body surface of P. major and some additional copepods such as: Clavellotis sargi (Kurtz, 1877), Clavella sp. 1, and Clavella sp. 2 (Lernaeopodidae) from the fins, and the monogeneans Anoplodiscus sp. (Anoplodiscidae), Benedenia sp. (Capsalidae), Choricotyle sp. (Diclidophoridae) from the gills (Table 1). Sea lice and monogeneans are considered as common pests of cultured fishes (Nowak, 2007). Of these mentioned parasites, the targeted species C. sclerotinosus has so far been reported only from two countries, viz. Australia (Roubal et al., 1983) and Japan (Ho et al., 2004; Madinabeitia, 2008) in the world (Fig. 4). Hence, this is the first study documenting infestation of C. sclerotinosus in Korea. It was first reported from Australia in 1981 from the sparid surf bream Acanthopagrus australis (Günther, 1859), but not designated a name since only one male was recorded (Roubal, 1981). In 1983, it was named as C. sclerotinosus while found from silver seabream Chrysophrys (=Pagrus) auratus (Forster, 1801) at Coffs Harbor, New South Wales and Wallaroo, South Australia (Roubal et al., 1983). In Japan, it was reported that fish farms of P. major in Oita Prefecture (Ho et al., 2004) and Ehime Prefecture (Madinabeitia, 2008) were highly infected with this species and hence recently, the species has been considered as one of the pests in fish aquaculture in Japan (Ho et al., 2004; Ohtsuka et al., 2009; Venmathi Maran et al., 2011). This sea louse is host-specific to sparid hosts (Ho et al., 2004). It is noteworthy to mention that C. sclerotinosus has not been

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Fig. 4. Map showing the countries such as Australia (1983), Japan (2004, 2008) and Korea (2011), where the infection of Caligus sclerotinosus was found on the sparid hosts.

detected from red seabream caught in the wild. However, infection of C. sargi has been reported from wild P. major (Kim, 1998). Two Clavella species are reported from cultured red seabream in this study from Korea for the first time that is considered new to science. A detailed ecological study on reported monogeneans is in progress. Adults of C. sclerotinosus heavily infected cultured red seabream in western Japan, but no chalimus stage has been found on this host (Ho et al., 2004; Madinabeitia, 2008; Ohtsuka et al., 2010). Adults of this species were also found in plankton samples near cage culture facilities at Uwajima, Ehime Prefecture, Japan (Venmathi Maran and Ohtsuka, 2008), whereas no intermediate host for the chalimi has yet been found, despite intensive search efforts in Japan (Ohtsuka et al., 2010) and Korea (present ongoing project) were made. We predict that C. sclerotinosus expands its host range during its ontogeny, as is known for C. chiastos Lin and Ho, 2003 (see Hayward et al., 2011). The ontogenetic host-switching on these two species of Caligus has hitherto been observed only in fish farms. Hayward et al. (2008) have found a unique life cycle of C. chiastos on farmed southern bluefin tuna Thunnus maccoyii (Castelnau, 1872) off southern Australia with high level of adult

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infestation, in contrast to chalimi. It was further elucidated by Hayward et al. (2010) that from over 5400 individuals of C. chiastos collected from southern bluefin tuna, only three (0.06%) represented larval stages. We, therefore, agree that all adult copepods transfer from other host fish through the water column to cultured southern bluefin tuna (Hayward et al., 2011) by active swimming after moulting from the fourth chalimus stage. On this prediction, the same group in Australia started to search for the presence of chalimi from wild fish occurring around the ranched cages and succeeded in finding the chalimi infection on the Degen’s leatherjacket Thamnaconus degeni (Regan, 1903), but was not detected on some other wild fishes such as the scad Trachurus sp., and other elasmobranchs and benthic teleosts (Hayward et al., 2011). The percentage of chalimi on the wild T. degeni occurring around the ranched cages increased over time and reached over 93%; confirmation of the species was carried out through molecular studies (Hayward et al., 2011). A similar situation has been observed with C. sclerotinosus on red seabream ranched in Korea. In the present study, a high prevalence of 100%, a mean intensity of 7.06 and a maximum intensity of 49 individuals per host were observed. But, only few developmental stages (5) of chalimi III female and male were found. Of a total 848 individuals collected, only 0.6% was identified as chalimi by their morphology. The life cycle of caligids mainly infecting marine fishes has been documented, consisting of naupliar, copepodid, chalimus and adult stages (Ho and Lin, 2004; Ohtsuka et al., 2009). The infective stages are copepodids followed by chalimus stages, which are firmly attached to the host with a frontal filament, and finally adults which freely move around the body of hosts for feeding and mating (Ohtsuka et al., 2009). Therefore, chalimi between these infective copepodid and adult stages were apparently lacking for C. sclerotinosus, similar to the case for C. chiastos on southern bluefin tuna (Hayward et al., 2008). Hostswitching has been shown to be dependent on active swimming of the adults in the water column. For instance, an adult female of C. sclerotinosus from the Ehime Prefecture, Japan (Venmathi Maran and Ohtsuka, 2008) and an adult male of C. chiastos from the western part of the Gulf of Thailand were found in plankton samples (Venmathi Maran et al., 2012) and possibly in its search for a new host that could have led to host-switching. Caligus chiastos has also been reported from other cultured fish hosts such as mulloway Argyrosomus japonicus (Temminck and Schlegel, 1843) and yellowtail kingfish Seriola lalandi Valenciennes, 1833 in Australia (Hayward et al., 2007), John’s snapper Lutjanus johni Bloch, 1792 (Venmathi Maran et al., 2009), and Asian seabass Lates calcarifer Bloch, 1790 in Malaysia (Muhd-Faizul et al., 2011). This data, and the exceptional rarity of chalimi on southern bluefin tuna, implies that the species is not host specific to southern bluefin tuna. The sparid host, red seabream is distributed in the coastal waters of Korea and is a valuable aquaculture species, replacing more and more the culture of yellow tail (Kim, 2000). However, in winter, due to cold conditions, some red seabream farms in Yeosu, Jeollanamdo (Ho Young

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Soh discussed this issue with local aquaculture sectors) experienced mortalities. A variety of parasites, bacteria and viruses are recognized as serious pathogens of cultured fishes in Korea (Syasina et al., 2004; Park, 2009). The sea louse C. sclerotinosus was introduced to Japan from Hong Kong in brood stock shipments of the host P. major, which are imported fresh for the sashimi markets (Miyazaki et al., 1986; Ho et al., 2004); however, it may well have already been present in the waters of Japan, given that it occurs widely in the Western Pacific from Australia to Asia. We suggest on its dispersal may be a result of natural migrations of some unpredictable hosts (host-switching) across the narrow and shallow water body of Tsushima Island and the Korea Strait separating the Korean peninsula from western Japan. Regarding the export of fishes, Korea exports olive flounders to both China and Japan (Kim, 2000), but red seabream is not as established as were olive flounders. Now, this sea louse might have become abundant in Korean fish farms other than Tongyeong area already. Support for the natural occurrence in, or dispersal of C. sclerotinosus to Korea would be strengthened if samples of wild red seabream in Korea or in Japan were found to be heavily infected, but so far no infection from wild red seabream has been reported in either countries. In addition, the identity of the host of the chalimi remains unknown. Within the past six years, this sea louse has been collected widely throughout Japan (Ho et al., 2004; Madinabeitia, 2008; Venmathi Maran and Ohtsuka, 2008). Ho et al. (2004) reported that in Taiwan, a thorough study on the infection of sea lice on food fishes was carried out for the last 2 decades, but sparid hosts have never been found with the infection of C. sclerotinosus. This indicates that infected wild fishes that were attracted to red seabream net cages must be the source of infections by mobile, adult C. sclerotinosus which are not found in Taiwanese waters. Hayward et al. (2011) reported that Degen’s leatherjacket was found to be infected with chalimus stages, in three months period it was increased from 0 to 93%. Hence, they suspect and confirm this could be a candidate for the main host of developmental stages of C. chiastos. Likewise, a thorough study of those species that are likely the main hosts of chalimus stages around the ranched red seabream and confirmation of chalimi through molecular studies are within our future research aims.

5. Conclusion In Korea, C. sclerotinosus severely infected cultured red seabream P. major, but was not, however, detected on wild red seabream. The prevalence, the mean and the maximum intensities were high. As mostly only adults were found, the host identity for the developmental stages is still unknown. Chalimi of the sea louse C. sclerotinosus were rarely found on red seabream cultured in Korea. This finding suggests that almost all chalimi of C. sclerotinosus spend their life on other favored hosts and that some or all adults simultaneously transfer from the reservoir hosts to P. major. We further suggest that C. sclerotinosus may undergo ontogenetic host switching. Hence, it is imperative to study the sea

lice infections of wild fishes near ranched red seabream to reveal the reservoir host of the chalimus stages. Conflict of interest statement All authors declare that, they do not have any conflict of interest. Acknowledgments We thank the following for assistance in the field and access to samples: Young Wook Lee, Suk Il Jang, and Il Young Jeong. Thanks are due to Dr. Hans-Uwe Dahms (Sangmyung University) for critically reading an early draft. We also thank the reviewers for their critical suggestions to improve the manuscript. This work was supported by the National Institute of Biological Resources, Korean project on the survey and exaction of Korean indigenous species. Senior author is thankful to Korea Research Council of Fundamental Science and Technology and this work formed part of Korea Ocean Research and Development Institute Projects (PK07920, PE98811, PE98747). References Costello, M.J., 2009. The global economic cost of sea lice to the salmon farming industry. J. Fish Dis. 32, 115–118. FAO (Food and Agriculture Organization of the United Nations), 2010. State of world aquaculture. Fish. Tech. Pap., 500/1. Froese, R., Pauly, D., 2011. FishBase. World Wide Web electronic publication. (accessed 29.11.11). Hayward, C.J., Bott, N.J., Itoh, N., Iwashita, M., Okihiro, M., Nowak, B.F., 2007. Three species of parasites emerging on the gills of mulloway Argyrosomus japonicus (Temminck and Schlegel, 1843), cultured in Australia. Aquaculture 265, 27–40. Hayward, C.J., Aiken, H.M., Nowak, B.F., 2008. An epizootic of Caligus chiastos on farmed southern bluefin tuna Thunnus maccoyii off South Australia. Dis. Aquat. Organ. 79, 57–63. Hayward, C.J., Ellis, D., Foote, D., Wilknison, R.J., Crosbie, P.B.B., Bott, N.J., Nowak, B.F., 2010. Concurrent epizootic hyperinfections of sea lice (predominantly Caligus chiastos) and blood flukes (Cardicola forsteri) in ranched Southern Bluefin tuna. Vet. Parasitol. 173, 107–115. Hayward, C.J., Svane, I., Lachimpadi, S.K., Itoh, N., Bott, N.J., Nowak, B.F., 2011. Sea lice infections of wild fishes near ranched southern bluefin tuna (Thunnaus maccoyi) in South Australia. Aquaculture 320, 178–182. Ho, J-s., 2000. The major problem of cage aquaculture in Asia relating to sea lice. In: Liao, I.C., Lin, C.K. (Eds.), Cage Aquaculture in Asia. Proceedings of the First International Symposium on Cage Aquaculture in Asia. Asian Fisheries Society/World Aquaculture Society – Southeast Asian Chapter, Manila/Bangkok, pp. 13–19. Ho, J.-S., Lin, C.L., 2004. Sea Lice of Taiwan (Copepoda: Siphonostomatoida: Caligidae). The Sueichan Press, Taiwan, 388 pp. Ho, J.-S., Gómez, S., Ogawa, K., Aritaki, M., 2004. Two species of parasitic copepods (Caligidae) new to Japan. Syst. Parasitol. 57, 19–34. Humes, A.G., Gooding, R.U., 1964. A method for studying the external anatomy of copepods. Crustaceana 6, 238–240. Hutchings, J.A., 2000. Collapse and recovery of marine fishes. Nature 406, 882–885. Johnson, S.C., Treasurer, J.W., Bravo, S., Nagasawa, K., Kabata, Z., 2004. A review of the impact of parasitic copepods on marine aquaculture. Zool. Stud. 43, 8–19. Kim, I.-H., 1998. Cirripedia, symbiotic Copepoda Pycnogonida. Illustrated Encyclopedia of Fauna and Flora of Korea, vol. 38. Ministry of Education, Korea, 1038 pp. Kim, I.B., 2000. Cage aquaculture in Korea. In: Liao, I.C., Lin, C.K. (Eds.), Cage Aquaculture in Asia. Proceedings of the First International Symposium on Cage Aquaculture in Asia. Asian Fisheries Society/World Aquaculture Society – Southeast Asian Chapter, Manila/Bangkok, pp. 59–73. Kim, I.-H., 2008. Invertebrate Fauna of Korea. Flora and Fauna of Korea series, NIBR, 21. Ministry of Environment, Korea, pp. 1–66.

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