Seasonal occurrence and habitat of two pennellids (Copepoda, Siphonostomatoida) infecting marine ranched black scraper and Korean rockfish in Korea

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1 Tropical Biomedicine 31(2): (2014) Seasonal occurrence and habitat of two pennellids (Copepoda, Siphonostomatoida) infecting marine ranched black scraper and Korean rockfish in Korea Venmathi Maran, B.A. *, Oh, S-Y., Choi, H-J. and Myoung, J-G. Marine Ecosystem Research Division, Korea Institute of Ocean Science & Technology, 787, Haean lo, Ansan , Seoul, Korea * Corresponding author bavmaran@gmail.com; bavmaran@kiost.ac Received 16 November 2013; received in revised form 8 January 2014; accepted 10 January 2014 Abstract. The seasonal occurrence and habitat of two parasitic copepods, Peniculus minuticaudae (Shiino, 1956) and Peniculus truncatus (Shiino, 1956) (Siphonostomatoida, Pennellidae) infecting the fins of black scraper Thamnaconus modestus and Korean rockfish Sebastes schlegelii, respectively were investigated. The fishes were collected from Tongyeong marine living resources research and conservation center, southern coast of Korea as five per month for two years from July 2011 to June In total, 391 copepods of P. minuticaudae were collected in two years, in contrast to P. truncatus. Prevalence was 85%, mean intensity was 3.25, and maximum intensity was 33. Season wise, the infestation was observed as the highest in autumn (September-November) season, and the lowest in winter (December- February). It was infested only on fins of black scrapers. Abundance of P. minuticaudae was found on the pectoral fin (43.5%), followed by anal (22.5%), second dorsal (20.5%) and caudal fins (13.5%). Statistically significant interactions were observed between season, infestation and infected regions (P<0.001). It is also reported for the first time in Korea from the fins of wild threadsail filefish Stephanolepis cirrhifer from Busan, Jeju, Tongyeong and Yeosu fish markets. It can be a new record on its host and localities. A total of 51 P. truncatus were collected with the prevalence of 37.5%, mean intensity of 0.37 and maximum intensity of 6. Season wise, infestation was observed as the highest in summer (June-August), and the lowest in winter. Attachment site was the dorsal fin and not found from any other fins of rockfish. Statistically significant interaction was observed between season and infestation (P<0.05). This is the first report on the ecology of these two pennellids. INTRODUCTION The genus Peniculus (von Nordmann, 1832) (Siphonostomatoida: Pennellidae) is one of the parasitic copepods frequently reported from Korea and Japan and it consists of 14 valid species (Venmathi Maran et al., 2012a). In Korea, two species of Peniculus have recently been reported with their complete redescription such as Peniculus minuticaudae (Shiino, 1956) from black scraper Thamnaconus modestus (Günther, 1877) and Peniculus truncatus (Shiino, 1956) from Korean rockfish Sebastes schlegelii (Hilgendorf, 1880) (Venmathi- Maran et al., 2012a). Those two species were originally described by Shiino (1956) from wild fishes of Japan, but recently P. minuticaudae was reported from farmed T. modestus and threadsail filefish Stephanolepis cirrhifer (Yamaguti, 1963; Fukuda, 1999; Nagasawa et al., 2011; Ismail et al., 2013), aquarium fishes, unicorn leatherjacket filefish Aluterus monoceros (Linnaeus, 1758), hairfinned leatherjacket Paramonacanthus japonicus (Tilesius, 1809) and brown-banded butterflyfish Roa modesta (Temminck & Schlegel, 1844) in Japan (Okawachi et al., 2012). The severity of P. minuticaudae infection is high in both Korea (Venmathi Maran et al., 2012a) and Japan (Nagasawa et al., 2011) and it has so 362

2 far not been reported from elsewhere. The complete life cycle of P. minuticaudae was revealed recently in Japan (Ismail et al., 2013), but the ecological studies on both pennellids are lacking in either countries. Hence, in this study, we report the ecology of both pennellids and a new host and localities records on P. minuticaudae. Black scrapers have been cultured at a few localities of the southern coastal regions of Korea. At Tongyeong marine living resources research and conservation center (TMRC), several commercially important fishes were ranched under the marine ranching program (MOMAF, 2007). Recently, we studied the symbiotic organisms associated with ranched fishes and their life cycle at TMRC (Venmathi Maran et al., 2012a; b; 2013). Threadsail filefish culture is uncommon in Korea, because of the small size and low growth rate of this fish, in contrast to Japan (Fukuda, 1999). Korean rockfish is cultured at several localities around the southern coastal region of Korea due to its high commercial value (Froese & Pauly, 2013). In order to control the increasing threat of parasites in aquaculture, the ecology of these two pennellids P. minuticaudae and P. truncatus are studied. MATERIALS AND METHODS The collection of ranched (TMRC, Gyeongsangnamdo, Korea) fish hosts T. modestus (T= cm) (Figure 1A) and S. schlegelii (T= cm) (Figure 2A) (five per month) were carried out for two years from July 2011 to June The seasonal study of both parasitic copepods was carried out. In addition, their habitats (infested site), prevalence, mean intensity were carefully analysed and investigated. Infested sites were microphotographed (Figure 1B, 2B). One-way and Two-way ANOVA analyses were applied for the statistical interpretation for season and infestation and also with infected regions. The common and scientific names of host fishes follow Froese & Pauly (2013). The infection of pennellids was also studied in the wild fish S. cirrhifer collected at fish markets located at Jeju (Jejudo), Busan, Tongyeong (Gyeongsangnamdo), Yeosu (Jeollanamdo) in Korea. Few specimens were used for scanning electron microscope analysis to show some general features. The copepods were transferred to 70% ethanol and then dehydrated through a graded series of ethanol (90%, 99.5% and 100%) and finally by isoamyl alcohol. The samples were critical point-dried using CO 2 gas and ion-sputtered for observation with a scanning electron microscope (Hitachi S-4700, Tokyo). RESULTS Peniculus minuticaudae (Figure 1B, C) A total of 391 pennellids of P. minuticaudae was collected from the soft fin rays of T. modestus for two years. Prevalence was 85%, mean intensity was 3.25, and maximum intensity was 33. Seasonwise, the infestation was observed as highest in autumn (September-November), and lowest in winter (December-February) (Figure 3). In two years period, infestation was found as high in September, followed by October, however, in December it was low. The habitats of infestation were only fins of black scrapers, not on body surface, gills and they were severely damaged. Abundance of pennellids was found on the pectoral fin (43.5%), followed by anal (22.5%), second dorsal (20.5%) and caudal fins (13.5%). Significant interactions were observed between season and infected regions (P<0.001), season and infestation (P<0.001). The same pennellid was also found for the first time in Korea from the fins of wild threadsail filefish Stephanolepis cirrhifer (Monocanthidae) from Busan, Jeju, Tongyeong and Yeosu fish markets. It can be considered as a new record on its host and localities in Korea. Peniculus truncatus (Figure 2B) A total of 51 P. truncatus was collected from the dorsal fin of S. schlegelii for two years (Figure 4). Prevalence was 37.5%, mean intensity was 0.37 and maximum intensity was 6. Season wise, infestation was observed as highest in July 2012 (summer), and lowest in winter. In 2011, summer and autumn 363

3 Figure 1. A. Marine ranched host black scraper Thamnaconus modestus; B. Severe infestation of pennellids on the fin (arrowed); C. Adult female Peniculus minuticaudae Shiino, 1956 with eggs Figure 2. A. Marine ranched host Korean rockfish Sebastes schlegelii; B. Infestation of adult female Peniculus truncatus Shiino, 1956 with eggs (arrowed) 364

4 Figure 3. Seasonal occurrence of Peniculus minuticaudae Shiino, 1956 infesting the all fins of Thamnaconus modestus from July 2011 to June 2013 at Tongyeong, Korea Figure 4. Seasonal occurrence of Peniculus truncatus Shiino, 1956 infesting the dorsal fin of Sebastes schlegelii from July 2011 to June 2013 at Tongyeong, Korea 365

5 Figure 5. Scanning electron micrographs of a pennellid showing: A. oral region with maxilla (arrowed); B. enlarged oral cone (arrowed); C. legs (arrowed) seasons were found with more number of pennellids than The infestation decreased (Aug-Oct) after July in 2012 (Figure 4). Attachment site was the dorsal fin (100%) and not found from any other fins, body surface or gills of rockfish. Significant interaction was observed between season and infestation (P<0.05). Scanning electron microscope The oral region (Figure 5A) of pennellid was observed with the enlarged oral cone (Figure 5B). Around the oral region, maxilla (arrowed Figure 5A) was located. The legs (Figure 5C) have been found located near the end of the neck and the beginning of cylindrical body. DISCUSSION A total of 391 P. minuticaudae and 51 P. truncatus were collected for two years from July 2011 to June 2013 from sea ranched locality. Both pennellids were collected only from the soft fin rays of fish hosts. In general, pennellids are having host specificity in both wild and farmed fishes (Ho, 1966; Boxshall & Halsey, 2004). While, fish live in aquarium, the infestation of pennellids can become in extensive range to many fish hosts due to conserved and restricted areas (Okawachi et al., 2012). However, in the ranched locality at Tongyeong (TMRC), seven different fish hosts are ranched, the infestation of P. minuticaudae was restricted only to black scraper and P. truncatus only to Korean rockfish. It shows the high host specificity of Peniculus in farming areas. However, one pennellid species, Haemobaphes disphaerocephalus (Grabda, 1976), was reported as an accidental infection from farmed Atlantic salmon Salmo salar (Linnaeus, 1758) in Canada (Kent et al., 1997; Johnson et al., 2004). Thus, our finding from Korea of P. minuticaudae and P. truncatus is only the second country record after Japan. We have also revealed a new record on localities in Korea such as Busan, Jeju, 366

6 Tongyeong and Yeosu. Although some pennellids life cycles are well documented, the host location remains unknown. Brooker et al. (2013) suggested that some kind of specific mechanisms are employed initially to locate a host and then to ensure that it is suitable for the host specificity. Through SEM analysis, we could reveal its bulged oral cone and maxilla which are important for feeding after firm attachment on fins without any movement for adult pennellids. Legs are used in developmental stages with several setae, but in adult are functionless (Ismail et al., 2013). In two years period, infestation of P. minuticaudae was found as high in September (end of summer), followed by October, however, infestation was high in July (summer) for P. truncatus and in December (winter) it was low for both pennellids. The high temperature manipulates the prevalence of parasite by increasing its life cycle completion rates (Macnab & Barber, 2012). The low infestation might be due to prevailing low temperatures (5-10ºC) in the winter season, sometimes mortality of fish occurs due to severe cold (personal observation). Prevalence of P. minuticaudae was 85%, but it is 37.5% for P. truncatus. The maximum number of individuals per host was 33 for former and 6 for latter. However, the maximum intensity of P. minuticaudae was reported as 121 in Japan and heavily infected on the pectoral fin followed by the second dorsal fin (Nagasawa et al., 2011). It agrees with our study as P. minuticaudae was abundant on the pectoral fin (43.5%), but followed by anal fin (22.5%). In the case of P. truncatus, only dorsal fin (100%) was infested. The membranes of the soft fin rays of black scrapers are heavily infested with P. minuticaudae, and fins were highly damaged, but no damage in Korean rock fish. In the family Pennellidae, adult females are deeply inserted into the body of their host (Boxshall & Halsey, 2004). Pennellids target different specific organs during infection, such as the eye [Phrixocephalus cincinnatus (Wilson, 1908) and Lernaeenicus sprattae (Sowerby, 1906)], the gill arch [Lernaeocera lusci (Bassett-Smith, 1896)], the bulbus arteriosus and the heart [L. branchialis (Linneaus, 1761), Haemobaphes diceraus (Wilson, 1917), and Cardiodectes medusaeus (Wilson, 1917)], the kidney, [either occasionally Lernaeenicus hemirhamphi (Kirtisinghe, 1932) or more permanently Peroderma cylindricum (Heller, 1865)], the liver [Ophiolernaea longiceps (Shiino, 1958)] (Ho, 1966; Pillai, 1985; Boxshall, 1986; Becheikh et al., 1997; Brooker et al., 2007) and the fins [P. minuticaudae and P. truncatus] in the present study. Pennellids have a unique life cycle (Kabata, 1981; Brooker et al., 2007). It usually needs two hosts as intermediate and definitive to complete its life cycle. Three pennellids such as Cardiodectes medusaeus (Wilson, 1908), Lernaeocera branchialis (Linnaeus, 1767) and Lernaeenicus sprattae (Sowerby, 1806) have so far been reported with their life cycles on two different hosts (Sproston, 1942; Schram, 1979; Perkins, 1983; Brooker et al., 2007). However, the life cycle of P. minuticaudae is completed in a single host (Ismail et al., 2013). Peniculus minuticaudae has so far been reported from five species of teleost fish hosts in Korean (Venmathi Maran et al., 2012a) and Japanese waters (Shiino, 1956; Yamaguti, 1963; Nagasawa et al., 2011; Okawachi et al., 2012; Ismail et al., 2013). However, P. truncatus reported from two different fish hosts S. oblongus (Shiino, 1956) from Japan and S. schlegelii (present study) (cf. Venmathi Maran et al., 2012a). More attention needs to be paid on P. truncatus to study its complete life cycle. This is the first report on the ecology of these two pennellids, although more new species are recently reported from Korea (Kim & Moon, 2013). Acknowledgment. We thank TMRC-KIOST colleagues for their generous assistance in the field and for access to samples and also to Dr. SY Moon for helping us to take SEM pictures. This work was formed part of KIOST Projects (PO01110, PE99202, PG48470). 367

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