Occurrence of Parasitic Isopods Norileca indica on Some Carangid Fishes from the Upper Gulf of Thailand Jittikan Intamong 1 and Smarn Kaewviyudth 1

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Occurrence of Parasitic Isopods Norileca indica on Some Carangid Fishes from the Upper Gulf of Thailand Jittikan Intamong 1 and Smarn Kaewviyudth 1 1 Department of Zoology, Faculty of Science, Kasetsart University Corresponding author s email: i.jittikan@gmail.com Abstract: This study was to identify and describe parasitic isopod infestation on some carangid fishes collected from the upper gulf of Thailand. A total of 155 carangid fish specimens from 7 species, Alepes djedaba, Atule mate, Liza subviridis, Parastromateus niger, Selar crumenophthalmus, Selaroides leptolepis and Sillago sihama were collected from Chanthaburi and Trat provinces in November 2013 to February 2014. Only one species of isopod, Norileca indica, was found in the branchial cavity of S. crumenopthalmus. The prevalence and intensity of this species infestation were 31.7% and 2.4, respectively. Keywords: Parasitic Isopods, Norileca indica, Carangid Fishes, The upper gulf of Thailand Introduction More than 450 species of parasitic isopods are great problems in the culture and captive maintenance of marine fishes (Moller and Anders, 1986). Due to they can cause significant economic losses to fisheries by killing, stunting, or damaging these fishes (Papapanagiotou et al., 2001, Ravichandran et al., 2010, Rameshkumar et al., 2011). Isopods of the genus Norileca (Isopod: Cymothoidae), consist of three species; N. borealis (Javed and Yasmeen), 1999, N. indica (Milne Edwards, 1840) and N. triangulata (Richardson, 1910) that found in marine, estuarine and freshwater. They are ectoparasites habit in the mouth, branchial cavity, fins of fishes, they fed on blood and macerated tissues that several species (Hoffman, 1998; Trilles and Bariche, 2006). Most of N. indica infected the branchial cavities of the pelagic fishes such as Alepes apercna, Atule malam, S. crumenophthalmus, Rastelliger kanagurta, and Herklotichthyes sp. from Southeast Asia and off Mozambique (Trilles, 1976; Avdeev, 1978; Rokicki, 1982; Bruce, 1990; Yu and Li, 2003). Currently, the studies on parasitic isopods particularly in cymothoids are less available in South Africa, South America and Asia (Trilles, 1994). In Thailand, the examination of Nerolica depressa parasitizing Sadinella albella from Eastern coast and Norileca indica parasitizing S. crumenophthalmus from the Southern coast were recorded (Nagasawa and Petchsupa, 2009; Printrakoon and Purivirojkul, 2011). The fishes in family Carangidae, known as scad or jack, represent the most important species in the small pelagic catches of the Gulf of Thailand, approximately twenty three species occur in Thailand (Roos et al., 1998). They act as an important protein sources and have a valuable fishery. In this study, therefore, was to determine the rates and distribution of parasitic isopod infestation in some carangid fishes from the upper gulf of Thailand. 265 10-

Methods A total of one hundred fifty-five specimens belonged to seven species of carangid fishes (Alepes djedaba, Atule mate, Liza subviridis, Parastromateus niger, Selar crumenophthalmus, Selaroides leptolepis and Sillago sihama) were collected from landing center or local markets of the Laem Ngob Pier, Trat province, Thailand, located at 12 10'14.86N and 102 23'33.65E and Laem Sing fishery village, Chanthaburi province, Thailand, located 12 28'54.89N and 102 3'44.43E during November 2013 to February 2014. Fish samples were brought to the laboratory for isopod collection. The total length and weight of the fishes were measured and examined for the isopod infestation, site of attachment, orientation of parasites on the host and the numbers of parasites in each fish were recorded. Isopod were removed and preserved immediately in 70% ethanol. All the total length of fish hosts and isopods were measured in millimeters. The prevalence (number of infested hosts/number of examined hosts) and the mean intensity (total number of parasites/number of infested hosts) were calculated according to Bush et al. (1997). The taxonomic identification of all fish specimens will be characteristically based on the reports of Food and Agriculture Organization of the United Nations (FAO, 2010) and Yoshida et al. (2013). Voucher specimens of isopod parasites are deposited at the Department of Zoology, Faculty of Science, Kasetsart University, Thailand. Results During the investigation of isopod parasites on collected carangid fish samples, only one species, Selar crumenopthalmus was infested with isopods in the branchial cavity (Figure 1). Total of 117 parasitic isopods, Norileca indica observed from 49 infested specimens of S. crumenopthalmus with the prevalence and mean intensity as 31.7 % and 2.4, respectively. The host fish length ranges from 188 to 230 mm. It is further confirmed that the parasites were specific in the selection the hosts of S. crumenopthalmus. A B Figure 1 (A) S. crumenopthalmus, (B) The presence of N.indica in the brachial cavity of S. crumenopthalmus 266

The morphology description of N. indica base on nine females and eleven males. The details are shown in Figures 2. Female isopods (Figure 2A, B, E): have creamy white color and mean size 31 mm long by 25 mm wide. The body twisted to one side and had the widest at pereonite 4. Pereonite 1 with posterolateral angles weakly produced. Coxae of pereonite 2 as long as segment and coxae of pereonite 3-7 all as long as respective segment. Posterior margin pereonite 7 weakly concave. Male isopod (Figure 2C, D, F): have a color similar to female with 22 mm long by 13 mm wide. All male parasites are much smaller and narrower than females. The body of male does not twisted, lateral margin sub-parallel. Coxae are longer than in female. A B C Figure 2 N. indica, (A, E) Dorsal view and (B) Ventral view of adult female. (C, F) Dorsal view and (D) Ventral view of adult male. (Scale bar= 10 mm). 267 10-

Discussion The investigation of parasitic isopods in this study found only one species of N. indica infested on S. crumenophthalmus from the host branchial cavity. The prevalence and mean intensity were 31.7 % and 2.4, respectively. The first report of this isopod species recovered from Pattani Bay, a small bay in the Southmost of Thailand (Nagasawa and Petchsupa, 2009). Rokicki (1982) found N. indica in branchial cavity of all bigeye scad specimens (N=70) examined from off Mozambique. Neeraja et al. (2014) also reported N. indica in S. crumenophthalmus from the south-west coast of India (the prevalence and intensity equal to 37.94% and 1.38, respectively). Similar results of N. indica infestation were reported by Rameshkumar et al. (2014), in a study about Rastrelliger kanagurta from the west coast of India. Many carangid fish species were parasitized by N. indica as bigeye scad S. crumenophthalmus, blackfin scad Atule malam (Avdeev, 1978), smallmouth scad Alepes apercna (Trilles, 1976) and Indian scad Decapterus Russelli (Ghani, 2003). Moreover, N. indica is known to be widely distributed in Sumatra, Indonesia, Philippines and New Guinea (Trilles, 1976), north-western Australia (Avdeev, 1978), off Mozambique (Rokicki, 1982), eastern Australia (Bruce, 1990), Pakistan (Ghani, 2003), China (Yu and Li, 2003), the Philippines (Yamauchi et al., 2005) and south-eastern India (Rameshkumar et al., 2011). From the result of this infestation able to further confirms its wide geographic distribution. The specimens of the cymothoid isopod N. indica in present study were collected from the host branchial cavity. This attachment site similar to Neeraja et al. (2014) that the female isopods were found inner surface of the operculum and dorsal side deeply plunged in the first gill arch with the gill filaments showing considerable atrophy and necrosis. This species belonged to the head to the anterior, and the abdomen facing outwards, pressed against the gill operculum, positioned ventrally in the gill cavity (Bruce, 1990). According to isopods habit on the gill chambers of their host, they may be produce pressure on the gill surface and thus affecting the efficiency of respiration. Moreover, they will affected to the growth of the host fishes especially degeneration of sexual organs (Ravichandran et al., 2010). According to this results, the species N. indica parasitizing S. crumenophthalmus is the first record of their infestation from Chanthaburi province and Trat province that located in eastern coast of Thailand. For further investigations of N. indica infestation from the different coasts of Thailand waters would be useful for better understanding of environmental and host effects on distribution of host-parasitic specificity and biogeographic distribution of this cymothoid isopod. Conclusion Occurrence of parasitic isopods in present study was done in the upper gulf of Thailand. Only one species of N. indica infested in the on branchial cavity of S. crumenophthalmus. The prevalence and mean intensity of N. indica on S. crumenophthalmus were 31.7 % and 2.4 respectively. 268

Acknowledgement Authors are gratefully to the Department of Zoology, Faculty of Science, Kasetsert University for providing facilities and Science Kasetsart University Postgraduate Studentship, ScKUPGS for funding support. We thank to Miss Kamonchanok Wongissarakul for illustration in this research work. Finally, we would like to express our honest appreciation to the anonymous reviewers who helped improve this paper. References Avdeev, V. V., 1978. Notes on the distribution of the marine Cymothoidae (Isopoda, Crustacea) in the Australian New Zealand region. Folia Parasit. 25: 281 283. Bruce, N. L., 1990. The genera Catoessa, Elthusa, Enispa, Ichthyoxenus, Idusa, Livoneca and Norileca n. gen. (Isopoda, Cymothoidae), Crustacean Parasites of Marine Fishes, with descriptions of Eastern Australian Species. Rec. Aust. Muse. 42: 247-300. Bush, A. O., Lafferty, K. D., Lotz, J. M., and Shostak, A. W., 1997. Parasiology meets ecology on its own terms: Margolis et al. revisited. J Parasitol. 83: 575 583. Food and Agriculture Organization: FAO. 2010. Avaiable Source: http://www.fao.org, September 10, 2010. Ghani, N., 2003. Isopod parasites of marine fishes of Pakistan. Proc. Pakistan Con. Zool. 23: 217-221. Hoffman, G. L., 1998. Parasites of North American Freshwater fishes. 2 nd ed. New York, USA: Cornell University Press, p. 325. Moller, H., and Anders, K., 1986. Diseases and parasites of marine fishes. German Federal Republic: Verlag Moller. p 365. Nagasawa, K., and Petchsupa, N., 2009. Norileca indica (Isopod, Cymothoidae) Parasitic on Bigeye Scad Selar crumenophthalmus in Thailand. Biogeography. 11: 131-133. Neeraja, T., Tripathi, G., and Shameem, U., 2014. Occurrence of the isopod, Norileca indica (Isopoda: Cymothoidae) on bigeye scad, Selar crumenophthalmus (Bloch) off Mumbai coast, India. Indian J. Fish. 61(1): 49-56. Papapanagiotou, E. P., and Trilles, J. P., 2001. Cymothoid parasite Ceratothoa parallela inflicts great losses on cultured gilthead sea bream Sparus aurata in Greece. Dis Aqua Org. 45: 237-239. Printrakoon, C., and Purivirojkul, W., 2011. Prevalence of Nerocila depressa (Isopoda, Cymothoidae) on Sardinella albella from a Thai estuary. Journal of Sea Research. 65. 322 326. Rameshkumar, G., Ramesh, M., Ravichandran, S., Trilles, P. J., and Subbiah, S., 2014. New record of Norileca indica from the west coast of India. J Parasit Dis. 1-4 Rameshkumar, G., Ravichandran, S., and Trilles, J. P., 2011. Cymothoidae: (Crustacea: Isopoda) from Indian fishes. Acta Parasitol. 56(1): 78-91. Ravichandran, S., Rameshkumar, G., and Balasubramanian, T., 2010. Infestation of isopod parasites in commercial marine fishes. J Parasit Dis. 34(2): 97-98. 269 10-

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