Fauna Ryukyuana ISSN 2187-6657 http://w3.u-ryukyu.ac.jp/naruse/lab/Fauna_Ryukyuana.html First record of a gill parasite, Dactylogyrus extensus (Monogenea: Dactylogyridae) co-introduced with common carp into Okinawa-jima Island, southern Japan 1 Masato Nitta1, 2 & Kazuya Nagasawa1 Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8528, Japan 2 Corresponding author ([email protected]) Abstract. Dactylogyrus extensus (Monogenea: Dactylogyridae) is described from the gills of the common carp, Cyprinus carpio, from the Hija River, Okinawa-jima Island, Okinawa Prefecture, southern Japan. This monogenean is undoubtedly an alien species introduced along with C. carpio to the island from an unknown locality. Introduction Currently, about 20 species of alien freshwater fishes have been established on Okinawa-jima Island, one of the Ryukyu Islands, southern Japan (Shimadzu 2011). Parasites have also been co-introduced along with such aliens to this island, with the following four monogenean species known to have been established: Cichlidogyrus halli (Price & Kirk, 1967), C. sclerosus Paperna & Thurston, 1969, C. tilapiae Paperna, 1960, and Heteropriapulus heterotylus (Jogunoori, Kritsky & Venkatanarasaiah, 2004) (Maneepitaksanti & Nagasawa 2012; Nitta & Nagasawa 2013). The common carp (Cyprinus carpio Linnaeus, 1758) is one species of freshwater fish introduced to Okinawa-jima Island (Kochi 2003). During a survey of freshwater fish parasites of this island, the dactylogyrid monogenean, Dactylogyrus extensus Mueller & Van Cleave, 1932, was collected from a river-caught specimen of C. carpio. The present note reports on this monogenean as a new record from Okinawa-jima Island. Material and methods One common carp (191 mm in standard length [SL]) was collected using a cast net from the Hija River at Misato, Okinawa City, Okinawa-jima Island, Okinawa Prefecture, Japan on 26 January 2013. The fish was brought alive to the laboratory of the Ryukyu University Museum (Fujukan) and examined for ectoparasites under a dissecting microscope. One dactylogyrid specimen was collected from the gill and fixed in ammonium picrate glycerin under coverslip pressure (Lim 1991). At the laboratory of Hiroshima University, this specimen’s whole-body morphology was observed, then dehydrated through a graded ethanol series, cleared in xylene, and mounted in Canada balsam. Drawings were made with the aid of a drawing tube fitted on an Olympus BX51 light microscope. Axes of measurements of sclerotized parts are presented in Fig. 1. The male copulatory organ and accessory piece lengths were measured from images taken by an Olympus DP20 microscope digital camera at a magnification of ×1,000 using ImageJ software (version 1.48i). The numbering of marginal hook pairs follows Llewellyn (1963). The voucher specimen is deposited in the Platyhelminthes collection of the National Museum of Nature and Science, Tsukuba City, Ibaraki Prefecture, Japan (NSMT-Pl). Species account Dactylogyrus extensus Mueller & Van Cleave, 1932 (Fig. 2) Host. Cyprinus carpio Linnaeus, 1758 (Cypriniformes: Cyprinidae). Locality. Hija River (26°21'11"N, 127°48'28"E), Misato, Okinawa City, Okinawa Prefecture. Material. One specimen (NSMT-Pl 6169). Site of infection. Gill. Description. Body (Fig. 2A) length 1678 µm, median width 219 µm. Three pairs of head organs. Two pairs of eye-spots with some dissociated eyes. Pharynx length 113 µm, width 105 µm. Esophagus absent, bifurcate intestine with branches confluent just posterior to testis. Testis pyriform, postovarian. Vas deferens arising from anterior region of testis, looped around left intestinal caeca dorsoventrally. Seminal vesicle expanded before entering into male copulatory organ. Two prostatic reservoirs both saccate. Vesicle reported in Ogawa & Egusa (1979) not observed. Male copulatory organ (Fig. 2K) tubelike, slender, length 86 µm. Sclerotized accessory piece (Fig. 2K) rod-shaped, top brash-shaped, length 54 µm. Ovary in mid-body. Vaginal armament unsclerotized; vaginal pore located on right body surface, vaginal duct connected right side of oviduct. 1 2 Fauna Ryukyuana, 26: 1–4. Oviduct arising from anterior side of ovary, continuous to oötype and uterus. Mehlis’ gland connected to top of oviduct. Vitelline system coextensive with intestinal caeca. Haptor length 178 µm, width 193 µm. Single pair of anchors (Fig. 2B), total length 84 µm, length to notch 73 µm, outer root length 16 µm, inner root length 27 µm, point length 19 µm. Dorsal bar (Fig. 2C), total length 47 µm, total width 14 µm, median width 10 µm. Ventral bar absent. Marginal hooks 7 pairs; hook lengths: pair I (Fig. 2D) 32 µm; pair II (Fig. 2E) 34 µm; pair III (Fig. 2F) 36 µm; pair IV (Fig. 2G) 34 µm; pair V (Fig. 2H) 35 µm, pair VI (Fig. 2I) 33 µm; pair VII (Fig. 2J) 34 µm. Pair of needles (Fig. 2L) located near tip of second hook, length 10 µm. Remarks. The morphology and measurements of sclerotized structures of the present specimen agree with the original and subsequent descriptions of D. extensus Mueller & Van Cleave, 1932 (e.g. Mueller & Van Cleave 1932, Ogawa & Egusa 1979, Long 2000, Gussev et al. 2010). The vesicle reported by Ogawa & Egusa (1979) could not be observed because the specimen was not stained. Dactylogyrus extensus is a gill parasite of C. carpio, being widely distributed in Europe, Asia, and North America (Gussev et al. 2010). In Japan, this monogenean is known to occur in 10 prefectures including Hokkaidō, Nīgata, Nagano, Gunma, Ibaraki, Chiba, Shizuoka, Tōkyō, Shiga, and Hiroshima (Imada et al. 1976, Nakatsugawa & Muroga 1977, Ogawa & Egusa 1979, 1982, Ogawa 1994), and this paper represents the first record of the monogenean from Okinawa Prefecture. Eight species of Dactylogyrus, i.e., D. anchoratus (Dujardin, 1845), D. biwaensis Ogawa & Egusa 1982, D. extensus, D. falciformis Achmerow, 1952, D. minutus Kulwieć, 1927, D. mrazeki Ergens & Dulmaa, 1969, D. sahuensis Ling, 1973, and D. takahashii Ogawa & Egusa 1982, have been recorded from common carp in Japan (Imada et al. 1976, Nakatsugawa & Muroga 1977, Ogawa & Egusa 1977, 1979, 1982, Ogawa 1994). Only one specimen of D. extensus was collected from the common carp examined in this study. Cyprinus carpio is not native to Okinawa-jima Island but is believed to have been introduced before the 19th century (Kochi 2003). Recently, common carp including koi carp are widely distributed on Okinawa-jima Island (Shimadzu 2011). The origin of the introduced carp is unknown, but since the native host of D. extensus is C. carpio (Gussev et al. 2010), this monogenean is undoubtedly an introduced species on Okinawa-jima Island. Acknowledgments We thank Daisuke Uyeno, Kagoshima University, for help with fish sampling. We are also grateful to Takeshi Sasaki, University Museum Fujukan, University of the Ryukyus (UR), for providing laboratory facilities. This study was partially supported by JSPS KAKENHI grants (no. 15J05777 to M. N. and no. 15K07527 to K. N.). Thanks are due to Pavel I. Gerasev, Russian Academy of Sciences, Kazuo Ogawa, Meguro Parasitological Museum, and Tohru Naruse, UR, for useful comments on the manuscript. References Gussev, A.V., P.I. Gerasev, & O. N. Pugachev, 2010. Order Dactylogyridea. In: P. Galli, O.N. Pugachev & D.C. Kritsky (Eds.), Guide to Monogenoidea of Freshwater Fish of Palaearctic and Amur Regions. Pp. 15–337, Ledizioni, Milano. Imada, R., K. Muroga, & S. Hirabayashi, 1976. Dactylogyrus extensus (Monogenoidea) from cultured carp in Japan. Bulletin of the Japanese Society of Scientific Fisheries, 42: 153–158. [In Japanese with English abstract]. Fig. 1. Dactylogyrus extensus Mueller & Van Cleave, 1932. NSMT-Pl 6169. A, whole mount (dorsal view); B, anchor; C, dorsal bar; D, marginal hook of pair I; E, marginal hook of pair II; F, marginal hook of pair III; G, marginal hook of pair IV; H, marginal hook of pair V; I, marginal hook of pair VI; J, marginal hook of pair VII; K, male copulatory organ; L, needle. Scale bars: A, 200 µm; B–L, 20 µm. Abbreviations: apl, accessory piece length; atl, anchor total length; bmw, bar median width; btl, bar total length; btw, bar total width; cl, copulatory organ length; hl, marginal hook length; irl, inner root length; ltn, length to notch; nl, needle length; orl, outer root length; pl, point length. 1. Dactylogyrus extensus Mueller & Van Cleave, 1932. NSMT-Pl 6169. A, ( ); B, ; C, ; D, 1 ; E, 2 ; F, 3 ; G, 4 ; H, 5 ; I, 6 ; J, 7 ; K, ; L, . : apl, ; atl, ; bmw, ; btl, ; btw, ; cl, ; hl, ; irl, ; ltn, ; nl, ; orl, ; pl, . [Report] Nitta & Nagasawa: Dactylogyrus extensus from Okinawa-jima Island 3 Kochi, R., 2003. Fishes of ponds, lakes, reservoirs and rivers. In: S. Nishijima, M. Nishida, N Shikatani & S. Shokita (Eds.), Inland Water Animals of the Ryukyu Archipelago. Pp. 482– 487, Tokai University Press, Tokyo. [In Japanese]. Llewellyn, J., 1963. Larvae and larval development of monogeneans. Advances in Parasitology, 1: 287–326. Lim, L.H.S., 1991. 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[In Japanese with English abstract]. Nitta, M. & K. Nagasawa, 2013. First Japanese record of Heteropriapulus heterotylus (Monogenea: Dactylogyridae), from the alien catfish Pterygoplichthys disjunctivus (Siluriformes: Loricariidae) in Okinawa. Species Diversity, 18: 281–284. Ogawa, K., 1994. Monogenean parasites of freshwater fishes of Hokkaido, Japan. Scientific Reports of the Hokkaido Fish Hatchery, 48: 59– 67. Ogawa, K. & S. Egusa, 1977. The first record of Dactylogyrus minutus Kulwieć, 1927 (Monogenea: Dactylogyridae) from the reared carp (Cyprinus carpio) in Japan. Bulletin of the Japanese Society of Scientific Fisheries, 43: 1029–1034. Ogawa, K. & S. Egusa, 1979. Redescription of Dactylogyrus extensus (Monogenea: Dactylogyridae) with a special reference to its 4 male terminalia. Japanese Journal of Parasitology, 28: 121–124. Ogawa, K. & S. Egusa, 1982. Eight species of Dactylogyrus (Monogenea, Dactylogyridae) from carp Cyprinus carpio in Japan with a proposal of two new species. Parazitologiya, 16: 95–101. [In Russian with English abstract]. Shimadzu, N., 2011. A distribution record of alien aquatic organisms and native fishes in 300 water systems on Okinawa Island in the summer of 2010. Japanese Journal of Conservation Ecology, 16: 99–110. [In Japanese with English abstract]. 比謝川で採集された外来魚コイに寄生してい た外来単生類コイユビガタムシ (単生類: ユビ ガタムシ科): 沖縄県初記録 新田理人 1, 2 ·長澤和也 1 〒739-8528 広島県東広島市鏡山1-4-4 広島大学 大学院生物圏科学研究科 2 通信著者 ([email protected]) 1 . carpio Linnaeus, 1758 Cyprinus 2 ( Dactylogyrus extensus Mueller & Van Cleave, 1932 ) 2 ( . : 2014 4 : 2015 8 : 2015 12 3 24 13
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