Salmincola Markewitschi (Copepoda: Lernaeopodidae) Parasitic on Whitespotted Char, Salvelinus Leucomaenis, in a Mountain Stream of Honshu Island, Central Japan

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Salmincola Markewitschi (Copepoda: Lernaeopodidae) Parasitic on Whitespotted Char, Salvelinus Leucomaenis, in a Mountain Stream of Honshu Island, Central Japan Species Diversity 25: 369–375 Published online 17 November 2020 DOI: 10.12782/specdiv.25.369 Salmincola markewitschi (Copepoda: Lernaeopodidae) Parasitic on Whitespotted Char, Salvelinus leucomaenis, in a Mountain Stream of Honshu Island, Central Japan Kazuya Nagasawa1,2 1 Graduate School of Integrated Sciences for Life, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8528, Japan E-mail: [email protected] 2 Present address: Aquaparasitology Laboratory; 365-61 Kusanagi, Shizuoka 424-0886, Japan (Received 13 August 2020; Accepted 14 October 2020) Females of the lernaeopodid copepod Salmincola markewitschi Shedko and Shedko, 2002 were collected from the buc- cal cavity of whitespotted char, Salvelinus leucomaenis (Pallas, 1814), in a mountain stream of Nagano Prefecture, Honshu Island, the largest main island of Japan. The females are described as the first record of S. markewitschi from Honshu Island, because the species has so far been reported from the Russian Far East and the southern Kuril Islands east of Hokkaido Is- land, Japan. The copepod previously reported as Salmincola californiensis (Dana, 1852) from the same host species from the same stream and a nearby hatchery is herein regarded as S. markewitschi. As the species closely resembles Salmincola carpio- nis (Krøyer, 1837), it is desirable to re-identify the copepod specimens reported before as S. carpionis from Japanese salmo- nids, especially Salvelinus spp. Contraction of the formalin-fixed and preserved specimens, especially their second maxillae, of S. markewitschi is discussed. Information on the known hosts and distribution records of S. markewitschi is also compiled. Key Words: Parasitic copepod, freshwater fish parasite, new locality record. Nagasawa et al. 2018); rainbow trout, Oncorhynchus mykiss Introduction (Walbaum, 1792) (Shedko 2005); and chinook salmon, On- corhynchus tschawytscha (Walbaum, 1792) (Shedko 2005). Copepods of the lernaeopodid genus Salmincola C. B. Nonetheless, there are two reports of “Salmincola californ- Wilson, 1915 are parasites of freshwater fishes, mainly mem- iensis” from whitespotted char, Salvelinus leucomaenis (Pal- bers of the family Salmonidae and related families, in the las, 1814), from central Honshu Island, Japan (Nishimura Northern Hemisphere (Kabata 1969, 1979). Currently, the and Hoshina 1977; Denda and Ogawa 2011). Nishimura and genus contains 22 valid species (Walter and Boxshall 2018). Hoshina (1977) collected “S. californiensis” from whitespot- Of these species, Salmincola californiensis (Dana, 1852) ted char [reported as Salvelinus leucomaenis pluvius (Hil- parasitizes mainly Pacific salmon (the genus Oncorhyn- gendorf, 1876)] reared at a hatchery in Nagano Prefecture. chus Suckley, 1861) in the U.S.A. (e.g., Kabata 1969; Hoff- The infected fish had been transported live from a nearby man 1999; Ruiz et al. 2017), Canada (Kabata 1969, 1988), mountain stream, the Zako River, a tributary of the upper the Russian Far East [Gussev 1951, reported as Salmincola Nakatsu River, to the hatchery. Later, Denda and Ogawa falculata (C. B. Wilson, 1908); Shedko et al. 2005b; Soko- (2011) actually collected “S. californiensis” from whitespot- lov et al. 2012] and Japan (Hoshina and Suenaga 1954, re- ted char in the Zako River and adjacent streams. Although ported as Salmincola yamame Hoshina and Suenaga, 1954; S. californiensis was rarely recorded from chars (the genus Kabata 1969; Hoshina and Nishimura 1976; Nagasawa and Salvelinus Richardson, 1836) (Gussev 1951; Kabata 1988; Urawa 2002; Nagasawa et al. 2018). The host species of On- Hoffman 1999), this parasite almost exclusively infects On- corhynchus reported from Far East Asia (Russia and Japan) corhynchus spp. (Kabata 1969). Thus, the records of “S. cali- are: pink salmon, Oncorhynchus gorbuscha (Walbaum, forniensis” from whitespotted char in central Honshu Island 1792) (Gussev 1951; Shedko et al. 2005b); coho salmon, are regarded as unusual. Oncorhynchus kisutch (Walbaum, 1792) (Shedko 2005); I had the opportunity to examine specimens of the co- sockeye salmon, Oncorhynchus nerka (Walbaum, 1792) pepod collected from whitespotted char in the Zako River (Gussev 1951); masu salmon, Oncorhynchus masou masou and identified them not as S. californiensis but as Salmin- (Brevoort, 1856) (Gussev 1951, reported as O. masu; Hoshi- cola markewitschi Shedko and Shedko, 2002. The latter spe- na and Nishimura 1976, reported as O. masou; Nagasawa cies has so far been reported from the Russian Far East and and Urawa 2002, reported as O. masou; Shedko et al. 2005b, the southern Kuril Islands east of Hokkaido Island, Japan reported as O. masou; Sokolov et al. 2012); amago salmon, (Shedko and Shedko 2002; Shedko et al. 2005a, b; Sokolov Oncorhynchus masou ishikawae Jordan and McGregor, et al. 2012). Thus, the present collection represents the first 1925 (Hoshina and Suenaga 1954, reported as O. masou; record of S. markewitschi from Honshu Island, the largest © 2020 The Japanese Society of Systematic Zoology 370 Kazuya Nagasawa Fig. 1. Salmincola markewitschi, female, NSMT-Cr 28337, from whitespotted char, Salvelinus leucomaenis, from the Zako River, a tributary of the upper Nakatsu River, Nagano Prefecture, central Honshu Island, Japan. A, habitus, lateral view; B, habitus, dorsal view; C, cephalotho- rax, second maxillae and bulla, anterior view; D, first antenna, dorsal view; E, second antenna, anterolateral view; F, exopod of second an- tenna, lateral view; G, H, mandibles, lateral view; I, first maxilla, lateral view; J, maxilliped, dorsolateral view; K, maxilliped, palp, dorsolateral view. Abbreviations: h1, hook 1; p, palp; p4, process 4; p5, process 5; s2, spine 2; t3, tubercle 3. Scale bars: A–C, 1 mm; D, 20 µm; E, 50 µm; F–H, 20 µm; I, 30 µm; J, 100 µm; K, 20 µm. main island of Japan. This paper describes S. markewitschi an Olympus BX51 compound microscope. One specimen using the specimens collected and, as the previous reports of was soaked in lactophenol for 2–3 h, and dissected and ob- the species were all published in Russian, summarizes infor- served using the hanging-drop method devised by Humes mation on its known hosts and distribution records. and Gooding (1964). All drawings were made with the aid of drawing tubes fitted on the stereo microscope (for the habitus, cephalothorax, and bulla) and the compound mi- Materials and Methods croscope (for the first and second antennae, mandible, first maxilla, and maxilliped). Morphological terminology fol- Two whitespotted char were collected using hook and lows Kabata (1979) and that for the armature of the en- line by a member of the Shiga Kogen Fisheries Cooperative dopod of the second antenna is based on Kabata (1969). Association on 17 July 2007 in the Zako River, a tributary Copepod voucher specimens have been deposited in the of the upper Nakatsu River of the Shinano River system, Crustacea collection of the National Museum of Nature near its junction with the Mansui River (at 1180 m altitude, and Science, Tsukuba, Ibaraki Prefecture (NSMT-Cr), and 36°49′29″N, 138°32′46″E), Yamanouchi, Nagano Prefecture, the remaining specimens are retained by the author at the central Honshu Island, Japan. The Zako River population Aquaparasitology Laboratory for a taxonomic study of Sal- of whitespotted char has been strictly conserved without mincola spp. from freshwater salmonids of Japan. Prevalence the introduction of any fish from other locations (Naka- and intensity follow the definitions of Bush et al. (1997). The mura and Iida 2009). Fish were fixed in 10% formalin im- scientific and common names of fishes mentioned in this mediately after capture. In February 2011, the fish were paper conform to FishBase (Froese and Pauly 2019), except transferred into 70% ethanol, by the staff of the Nagano for those of southern Asian Dolly Varden, Salvelinus malma Prefectural Fisheries Experimental Station, and sent to the krascheninnikova Taranetz, 1933, which are based on Naga- laboratory of Hiroshima University, Hiroshima Prefecture, sawa (2020). The scientific names of two subspecies of O. where they were measured for standard length (SL, mm) masou follow Nakabo (2013). and examined for the presence of parasitic copepods. When copepods were found, they were carefully removed and pre- served in 70% ethanol after their attachment sites were re- corded. Subsequently, at the Aquaparasitology Laboratory, Shizuoka Prefecture, the copepods were morphologically examined using an Olympus SZX10 stereo microscope and The fish parasite Salmincola markewitschi from Japan 371 spines on tip; endopod two-segmented; basal segment with Results larger spiny pad on ventral surface; distal segment with api- cal armature consisting of powerful hook 1 arising from Salmincola markewitschi Shedko and Shedko, 2002 dorsal side, small spine 2 and tubercle 3 near base of spine [New Japanese name: Miyama-nagakubi-mushi] 1, and conical process 4 and small process 5 slightly sepa- (Fig. 1) rated from spine 2 and tubercle 3. Mandible (Fig. 1G, H) short and unsegmented with six or seven teeth (n=2) on Salmincola markewitschi Shedko and Shedko, 2002: 147– dentiferous margin; first four distal teeth larger than next 152, figs 3–4 [original description; type locality: a river one or two teeth; proximal tooth smallest. First maxilla (Fig. flowing into Bol’shoye Lake, Shumshu Island, northern 1I) with three terminal papillae on endopod; ventral pa- Kuril Islands, Russia; Bol’shoye Lake, Shantar Islands, pilla shorter than other two; exopod
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