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The Epidemiology of the Trichodinid Ciliate Trichodina Truttae on Hatchery-Reared and Wild Salmonid Fish in Hokkaido

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The Epidemiology of the Trichodinid Ciliate Trichodina Truttae on Hatchery-Reared and Wild Salmonid Fish in Hokkaido 魚病研究 Fish Pathology, 51 (4), 199–209, 2016. 12 © 2016 The Japanese Society of Fish Pathology Research article The Epidemiology of the Trichodinid Ciliate Trichodina truttae on Hatchery-reared and Wild Salmonid Fish in Hokkaido Shinya Mizuno1*, Shigehiko Urawa2, Mahito Miyamoto1, Makoto Hatakeyama1, Hayato Saneyoshi1, Yoshitaka Sasaki1, Nobuhisa Koide1 and Hiroshi Ueda3 1Salmon and Freshwater Fisheries Research Institute, Hokkaido Research Organization, Hokkaido 061-1433, Japan 2Hokkaido National Fisheries Research Institute, Japan Fisheries Research and Education Agency, Hokkaido 062-0922, Japan 3Field Science Center for Northern Biosphere, Graduate School of Environmental Science, Hokkaido University, Hokkaido 060-0809, Japan (Received September 27, 2016) ABSTRACT―Trichodinids are ectoparasitic ciliates that infect the body surface of salmonid fish and occasionally cause high mortality in juvenile chum salmon Oncorhynchus keta reared at hatcheries in northern Japan. The present study examined the occurrence of trichodinid ciliates on wild fish and hatchery-reared juvenile chum salmon in Hokkaido to determine the epidemiology of these parasites. Trichodinids were observed on juvenile chum salmon reared at 28 out of the 87 examined hatcheries and on wild fish, including masu salmon O. masou, rainbow trout O. mykiss, adult chum salmon, white-spot- ted char Salvelinus leucomaenis, and Dolly Varden S. malma in rivers. All isolates of trichodinid ciliates had the same nucleotide sequences of small subunit ribosomal RNA gene and were identified morpho- logically as T. truttae. A transmission experiment showed that T. truttae was transmitted horizontally from wild masu salmon to hatchery-reared juvenile chum salmon. Our results demonstrate that a domi- nant species of trichodinid ciliate infecting salmonid fish in Hokkaido is T. truttae and that wild salmonids can be an infection source of hatchery-reared juvenile chum salmon. Key words: Trichodina truttae, Oncorhynchus keta, Oncorhynchus mykiss, Salvelinus leucomaenis, Salvelinus malma, hatchery, Hokkaido, Epidemiology Trichodina species are ectoparasitic ciliates that 1991) and Japan (Urawa, 1992a, b). Infections of the infect the skin and/or gills of fish. These parasites are parasite are widely observed on hatchery-reared juvenile common and occasionally cause trichodinosis, which chum salmon in the regions of Hokkaido and Tohoku, can be lethal for cultured freshwater and marine fish northern Japan, but have not been reported on hatchery- (Lom and Hoffman, 1964; Hoffman, 1976; Lom and reared pink salmon O. gorbuscha, masu salmon O. Dyková, 1992; Urawa, 1992a; Khan, 2004). The identi- masou, or sockeye salmon O. nerka (Urawa, 1992b). fication of Trichodina species in Japanese fish has been Results of a transmission experiment revealed that a limited; T. reticulata has been detected on goldfish heavy T. truttae infection causes epidermal hyperplasia Carassius auratus auratus, silver crucian carp Carassius on the skin of juvenile chum salmon and cumulative auratus langsdorfii, and common carp Cyprinus carpio mortality of 56%, with intensive flashing and jumping out (Ahmed, 1977); T. truttae has been observed on chum of the water (Urawa, 1992a). In fact, high mortalities salmon Oncorhynchus keta (Urawa and Arthur, 1991); due to trichodinid infections occurred in chum salmon fry T. japonica, T. jadranica, and T. acuta have been found reared in a Hokkaido hatchery in 1968 (Takeda et al., on Japanese eel Anguilla japonica (Imai et al., 1991); 1969). It is important for hatchery managers to control and T. fugu has been identified on tiger puffer Takifugu the parasite using seawater baths (Khan, 1991) and to rubripes (Imai et al., 1997). intercept the infection routes of the parasite to prevent Epidemiological information on T. truttae, which was mortality of juvenile chum salmon due to trichodinosis. originally identified on hatchery-reared cutthroat trout O. It is presumed that wild fish inhabiting rivers are the clarki in Oregon, USA (Mueller, 1937), has been source of T. truttae infection because these infections reported in Canada (Arthur and Margolis, 1984; Khan, are often found in hatcheries that utilize river water to culture juveniles (Urawa, 1992b). However, this * Corresponding author hypothesis has not been proven because little informa- E-mail: [email protected] tion is available on T. truttae infections in wild fish. 200 S. Mizuno, S. Urawa, M. Miyamoto, M. Hatakeyama, H. Saneyoshi, Y. Sasaki, N. Koide and H. Ueda Taxonomic studies of T. truttae have been per- Materials and Methods formed by morphological observations using light and scanning electron microscopy (Arthur and Margolis, Fish 1984; Urawa and Arthur, 1991; Ferguson et al., 2011) Juvenile chum salmon (weight, 0.83–1.20 g) were but no study has used a molecular approach to investi- collected from 87 hatcheries in Hokkaido from April to gate the epidemiology of the parasite. The complete May 2013. The hatcheries were designated nos. 1–87. and partial nucleotide sequences of the small subunit The name and location of each hatchery was de-identi- ribosomal RNA gene (SSUrDNA) have been elucidated fied to prevent any harm caused by a fish disease rumor. to identify and classify several Trichodina species (Zhan Wild fish composed of masu salmon, rainbow trout O. et al., 2009; Gong et al., 2010; Tang et al., 2013), but mykiss, white-spotted char Salvelinus leucomaenis, that of T. truttae have not been reported. Dolly Varden S. malma, sculpin Cottus nozawae, and To determine the epidemiological characteristics of goby Gymnogobius urotaenia were captured 50–200 m T. truttae including the infection sources of hatchery fish, upstream from the water intake point of each river where the present study examined the occurrence of trichodinid hatchery nos. 42, 43, 60, 66, 67, 69–71, and 77 were ciliates on juvenile chum salmon reared at 87 hatcheries located by electrofishing (LR-24 Backpack Electrofisher; and wild fish captured from rivers in Hokkaido. The cili- Smith-Root, Vancouver, WA, USA) from May to ates were identified morphologically and their SSUrDNA November 2013 (Table 1). In addition, 10 wild adult sequences were compared between isolates. A trans- chum salmon migrating upstream to spawn were caught mission experiment of trichodinid ciliates was performed using fixed cages in the river of the hatchery no. 43 on between wild masu salmon and hatchery-reared juvenile October 8 and in the river of hatchery no. 66 on chum salmon. November 4, 2013 (Table 1). The captured fish were held individually until sampling to prevent horizontal infection of trichodinid ciliates. Hatchery-reared juve- niles and wild fishes excepting adult chum salmon were Table 1. Wild fish collected in this study and infection status of trichodinid ciliates on the fish Sampling Fish Infection status of trichodinid ciliates The parasite- The parasite number Date River Species Number Body weight (g) positive rate of (individual/g body weight) fish (%) May 8, 2013 No. 42 Masu salmon 10 0.35–13.0 0 0 *(0/10) May 9, 2013 No. 43 Masu salmon 21 18.3–47.4 0.846 ± 2.21 62.5 *(5/8) Rainbow trout 34 18.5–77.1 0.00404 ± 0.0106 14.2 *(1/7) White-spotted char 3 167.3–457.2 0.00259 ± 0.00519 33.3 *(1/3) Sculpin 5 0.62–18.1 0 0 *(0/5) July 7, 2013 No. 60 Masu salmon 40 1.94–29.9 0.0951 ± 0.190 14.2 *(1/7) White-spotted char 29 3.30–91.2 0.0684 ± 0.0931 40.0 *(0/10) No. 66 Masu salmon 51 1.33–13.9 0.135 ± 0.419 10.5 *(2/19) Dolly Varden 38 1.01–25.5 0.123 ± 0.350 12.5 *(1/8) October 8, 2013 No. 43 Chum salmon (Adult) 10 2,000–3,500 †No data †No data November 4, 2013 No. 60 Masu salmon 10 2.71–34.3 0.107 ± 0.232 30.0 *(3/10) White-spotted char 16 2.30–5.56 0.0240 ± 0.0657 12.5 *(2/16) No. 66 Chum salmon (Adult) 10 1,800–3,200 †No data †No data Masu salmon 22 2.92–10.9 0.408 ± 0.997 50.0 *(11/22) Dolly Varden 8 1.23–26.8 0.541 ± 0.992 37.5 *(3/8) No. 67 Masu salmon 7 11.8–27.9 0 0 *(0/3) Dolly Varden 7 3.48–30.8 0.0392 ± 0.110 14.2 *(1/7) No. 69 Masu salmon 5 10.7–14.22 0 0 *(0/5) Dolly Varden 6 3.45–27.7 0 0 *(0/6) Goby 6 0.60–9.31 0 0 *(0/6) No. 70 Masu salmon 3 7.34–25.7 0 0 *(0/3) Dolly Varden 7 1.48–11.2 0.0828 ± 0.168 28.5 *(2/7) No. 71 Dolly Varden 6 4.39–51.0 0 0 *(0/6) No. 77 Rainbow trout 7 18.4–44.1 0 0 *(0/7) Dolly Varden 7 4.09–19.9 0.0667 ± 0.176 14.2 *(1/7) * Asterisks showed number of the parasite-positive fish/total number of fish analyzed infection status of the parasite. † Infection status of trichodinid ciliates on adult chum salmon was not examined in this study. The parasite numver was expressed as mean ± standard deviation. Epidemiology of trichodinid ciliates on salmonids 201 used for analyses on infection status, morphology and denticle; the width of the border membrane; and the SSUrDNA of trichodinid ciliates, while adult chum adoral ciliary spiral. These parameters were measured salmon were done for only analyses on the morphology using a three-dimensional high-resolution image analy- and rDNA. For the transmission experiment, a total of sis system (Apotome 2 and Axio Imager System; Carl 1,160 chum salmon were cultured artificially from mid- Zeiss), according to methods reported by Lom (1958) November 2012 until May 10, 2013 without becoming and Gong et al.
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