59 RESEARCH NOTE NEMATODE INFESTATION IN THE INDONESIAN SHORTFIN EEL (Anguilla bicolor) (ACTINOPTERYGII: ANGUILLIFORMES: ANGUILLIDAE) HARVESTED FROM ACEH WATERS, INDONESIA Zainal A. Muchlisin, BS, MS, PhD1*, Bahtiar Lubis, BS, MS1, Agung Setia Batubara, BS, MS1, Irma Dewiyanti, BS, MS1, Muzailin Affan, BS, MS, PhD2 and Mufakkir Sidqi, BS, MS3 1Department of Aquaculture, Faculty of Marine and Fisheries; 2Faculty of Mathematics and Natural Sciences; 3Department of Integrated Coastal Zone Management, Institute of Graduate Studies, Syiah Kuala University, Banda Aceh, Indonesia ABSTRACT The study was conducted to determine the nature of infestation of nematodes on Indonesian shortfin eel (Anguilla bicolor) harvested from Aceh Province waters, Indonesia. The sampling was conducted in Aceh Singkil, Aceh Jaya and Aceh Besar Districts from August to September 2016 and January 2017. Twenty-two samples from Aceh Singkil, one sample from Aceh Jaya, and 23 samples from Aceh Besar were analyzed for gastrointestinal worms. Two species of worms were found in the gastrointestinal tract of fish samples, namely, Anisakis sp. and Procamallanus sp. Anisakis sp. was found in the stomach of the eel sample from Aceh Singkil, while Procamallanus sp. was found in the intestine of the eel samples from Aceh Jaya. No fish samples from Aceh Besar were infested with nematode. Key words: Anisakis, Indonesia, nematode, Procamallanus, shortfin eel Philipp. J. Vet. Med., 55(1): 59-64, 2018 INTRODUCTION Eels of the genus Anguilla are widely found Unfortunately, several species of eels are throughout the world (Arai and Wong, 2016). threatened by overfishing and habitat loss According to Miller and Tsukamoto (2004), resulting in decrease of glass eel production there are 19 species of eels worldwide. Thirteen (Pujolar et al., 2007; Silfvergrip, 2009). species of eels are reported in tropical regions Information on the distribution and migration (Watanabe et al., 2009); of these, seven species of tropical shortfin eels A. bicolor bicolor and are found in Indonesian waters (Sugeha et al., A. bicolor pacifica have been reported by Arai 2006). Based on biometric characteristics, two et al. (1999), Sugeha and Suhartati (2008), and species of eels have been reported from Aceh Muchlisin et al. (2016); while genetic studies waters, Indonesia: Anguilla bicolor and A. have been conducted by Tanaka et al. (2014) marmorata (Muchlisin and Siti-Azizah, 2009). and Muchlisin et al. (2017). However, no Of the two species, the Indonesian shortfin eel report on parasites, particulary on nematode A. bicolor is the most abundant and distributed infestation in Indonesian shortfin eelA. bicolor widely in Aceh waters (Muchlisin et al., 2017). from Indonesian waters, is available. Eels are catadromous fishes; they migrate The world eels market is very promising. between inland or coastal growth habitats Japan needs about 130,000 tons of eels per and spawn offshore (Arai and Wong, 2016). year, but only 21,000 tons (16.8%) can be met (KKP, 2011). In addition, the global market requires more than 268,000 tons of eels per *FOR CORRESPONDENCE: year (FAO, 2014). Presently, most of the eels (email: [email protected]) produced come from wild populations, and 60 MUCHLISIN et al. production is seasonally dependent. Therefore, on Hurst (1984), Moravec and Justine (2006) eel production has a very good potential for and Koinari et al. (2013). The prevalence and aquaculture business (Muchlisin, 2013). intensity of infection were calculated based The extensive culture of eels has been on Kabata (1985) as follows: prevalence = initiated in Indonesia, where the larvae (total infected fish/total examined fish) × 100; are collected from the wild (Affandi, 2005); intensity = total parasites/total infected fish. therefore, the eels are very susceptible to diseases and parasites harmful to humans. Tumbo et al. (2011) reported that the giant RESULTS AND DISCUSSION marbled eel A. marmorata from North Sulawesi, Indonesia, has been infested with Trichodina A total of 46 eels were examined for sp., Myxobolus sp. and Vorticella sp., while gastrointestinal nematode infestation. Anguillicola crassus is a common parasite of the Twenty-two samples were obtained from Aceh European eel A. anguilla (Evan and Matthews, Singkil, one sample from Aceh Jaya and 23 1999; Kirk, 2003; Kennedy, 2007; Muñoz et samples from Aceh Besar. The fish samples al., 2015). Grano-Maldonado et al. (2011) also from Aceh Singkil and Aceh Jaya were infected reported that the European eel was infected by nematodes with intensity of 1.74-18.0 and by Gyrodactylus anguillae. However, there is prevalence of 86.4-100 (Table 1). No fish sample no information on the parasites that infect the from Aceh Besar was infested with nematode. Indonesian shortfin eelA. bicolor in the waters Further analysis of fish samples from Aceh of Aceh, Indonesia. Thus, the present study Singkil and Aceh Jaya showed that two species was conducted to examine the gastrointestinal of nematodes were detected, namely, Anisakis nematode infestation in Indonesian shortfin sp. and Procamallanus sp. Anisakis sp. was eel A. bicolor harvested from Aceh waters, found in the stomach while Procamallanus Indonesia. sp. was observed in the intestines (Table 2). Anisakis sp. was found in 84% the fish samples from Aceh Singkil, while Procamallanus sp. MATERIALS AND METHODS infested only one fish sample from Aceh Jaya. Eighteen Procamallanus sp. worms were Sampling was conducted from September reported in the fish sample from Aceh Jaya, 2016 to March 2017 in Singkil peat swamp, Aceh while 33 Anisakis sp. worms were found in 19 Singkil District (2o 16’ 32.55” N; 97o 50’ 39.47” fish samples (average of 1.74 worms per fish). E), the Lamno River, Aceh Jaya District (5o 3’ Procamallanus sp. is brown-orange with a 3.79” N; 95o 20’ 26.26” E) and Tibang Reservoir length of 22.35-26.22 mm, with buccal capsule Aceh, Besar District (5o 36’ 4.46” N; 95o 23’ 3.46” in the mouth, esophagus, nerve ring and E). Parasite identification was conducted at intestine. There are alae at the rearmost parts the Laboratory of Fish Quarantine, Aceh Besar of the posterior (Figs. 1 and 2). The length District. Fish samples were captured using of Anisakis sp. ranges from 10.3-12.02 mm. line hooks; they were kept alive individually in It has a mouth with no lip, with ventriculus plastic bags and transported to the laboratory and intestine and a mucron at the end of the for further analysis. All procedures involving posterior part (Figs. 3 and 4). animals were conducted in compliance with the Anisakis sp. was found in the stomach, and Syiah Kuala University Research and Ethics Procamallanus sp. was detected in the intestine. Guidelines, Section of Animal Care and Use in This indicates that the gastrointestinal tract Research (Ethics Code No: 958/2015). is the most frequently infested organ by these The fishes were measured for total length worms because this organ is rich in nutrients. and body weight and then anesthetized using According to McClelland (2005) Procamallanus MS2222 overdose. Each fish was dissected sp. is not only found in freshwater but also in abdominally, and the gastrointestinal tract marine fishes, and they are commonly detected was removed, placed in a jar, then perforated in the stomach, intestine and pylorus cecum. with a needle, and the gastrointestinal contents This is the first report on the nematode were placed in a petri dish and observed for infection in Indonesian shortfin eel A. bicolor worms with a stereo microscope (Olympus CX- from Aceh Region, Indonesia. The previous 31, Japan) at 100x magnification (Muchlisin et report by Jabal et al. (2015) shows that the al., 2015). Identification of the worm was based eel Anguilla spp. from Lindu lake, Central NEMATODE INFESTATION IN INDONESIAN SHORTFIN EEL 61 Table 1. Prevalence and intensity of nematodes in Indonesian shortfin eel (Anguilla bicolor) according to sampling locations. Intensity No. of fish No. of Prevalence Location ∑Parasites (parasite/fish samples infested fish (%) sample) Aceh Singkil 22 19 33 1.74 86.4 Aceh Jaya 1 1 18 18 100 Aceh Besar 23 0 - 0 0 Total 46 20 Table 2. Prevalence and intensity of nematodes in Indonesian shortfin eel (Anguilla bicolor) according to host organs. Parasite No. of No. of Organ Procamallanus Anisakis infected Parasites Intensity Prevalence sp. sp. fish Operculum - - - - - - Gill - - - - - - Scales - - - - - - Pectoral - - - - - - fins Annal fins - - - - - - Stomach - 33 19 33 1.74 86.4 Intestine 18 - 1 18 18 100 Total 18 33 Sulawesi, Indonesia, were infected by several Carangidae) in New Caledonia (Moravec et al., species of protozoa, e.g. Myxidium sp., 2016). Besides infesting the fish, camallanids Myxobolus sp., Chilodonella sp., Ceratomyxa also infested amphibians in Chennai, India sp., Balantidium sp., Henneguya sp. and (Jeyathilakan et al., 2013) and Lombok Island, Glugea sp., while Gyrodactylus anguillae and Indonesia (Purwaningsih et al., 2016). Anguillicoloides crassus were the common The Anisakis sp. can be identified based on parasites found in the European eel A. anguilla the presence of mucron, boring tooth, and the (Evan and Matthews, 1999; Grano-Maldonado appearance of the esophagus and ventriculus et al., 2011; Kirk, 2003; Kennedy, 2007; Muñoz (Messina et al., 2016), but the boring tooth was et al., 2015). not observed in this study, probably due to low Procamallanus sp. is a brown nematode quality sample appearance. The first report that has a cuticle layer; it has a buccal capsule on Anisakis sp. infection on marine fishes shaped like a barrel and is not split into two (Rastrelliger kanagurta, Decapterus russelli valves (Kabata, 1985). Infestation of worms and Sardinella sirm) in Indonesia was reported in other waters include Camallanus sp., which by Hutomo et al. (1978). Besides infesting infested Awaous stamineus in Hawaii waters the Indonesian eel samples as shown in this (Gagne et al., 2015), Awaous guamensis and study, Anisakis sp. also infested Rastrelliger Kuhlia marginata in New Caledonia (Moravec sp.