Bull. Natl. Mus. Nat. Sci., Ser. A, 44(2), pp. 57–68, May 22, 2018 Adult Digeneans (Trematoda) Parasitic in Hypomesus nipponensis (Osteichthyes, Osmeridae) from Brackish-water Lakes of Japan Takeshi Shimazu 10486–2 Hotaka-Ariake, Azumino, Nagano 399–8301, Japan E-mail: [email protected] (Received 10 March 2018; accepted 28 March 2018) Abstract Adult digeneans (Trematoda) were found in Hypomesus nipponensis McAllister (Oste- ichthyes, Osmeridae) from a brackish-water lake, Lake Abashiri, in Hokkaido, Japan. Some unidentified digenean specimens that had previously been recorded from Hypomesus nipponensis from brackish-water lakes in Japan were also reexamined. The digeneans were classified into three species of marine origin: Pronoprymna petrowi (Layman, 1930) Bray and Gibson, 1980 (Micro- phalloidea, Faustulidae) from Lakes Abashiri and Tofutsu in Hokkaido, Lake Takahoko in Aomori Prefecture, and Lake Koyama in Tottori Prefecture; Brachyphallus crenatus (Rudolphi, 1802) Odhner, 1905 (Hemiuroidea, Hemiuridae) from Lakes Abashiri and Tofutsu; and Lecithaster gib- bosus (Rudolphi, 1802) Lühe, 1901 (Hemiuroidea, Lecithasteridae) from Lakes Abashiri, Tofutsu, and Koyama. They are described and figured. Their geographical distribution and life cycles are briefly discussed. Key words: Adult digeneans, parasites, Hypomesus nipponensis, brackish-water lakes, Japan. Introduction and 2017. In this paper, three species of adult digeneans found in Hypomesus nipponensis are Little is known about adult digeneans (Trema- identified, described, and figured on the basis of toda) parasitic in Hypomesus nipponensis McAl- specimens collected by Ohtomo, Kikuchi, and lister (Osteichthyes, Osmeridae) in brackish me. Their geographical distribution and life waters of Japan. Ohtomo (2003) found three spe- cycles are briefly discussed. cies of adult digeneans, Pronoprymna sp., Brachyphallus sp., and Lecithaster sp., in Materials and Methods Hypomesus nipponensis from Lake Abashiri in Hokkaido. She neither described nor figured Specimens dealt with in this paper were found them. Kikuchi (2014) recorded three species of in Hypomesus nipponensis from Lakes Abashiri adult digeneans in Hypomesus nipponensis: and Tofutsu (brackish-water lakes) in Abashiri Digenea sp. 1, Digenea sp. 2, and Digenea sp. 3 City, Hokkaido, on the coast of the Sea of from Lake Tofutsu in Hokkaido; and Digenea sp. Okhotsk; and Lake Koyama (or Koyama-ike) (a 1 from Lake Takahoko in Aomori Prefecture and brackish-water lake) in Tottori City, Tottori Pre- Lake Koyama in Tottori Prefecture. She figured fecture, on the coast of the Japan Sea. them but did not compare them with Ohtomo’s Some specimens obtained by Ohtomo (2003) three species in morphology. Their adult speci- and Kikuchi (2014) were made available to me mens have remained unidentified to species level. for reexamination by courtesy of Akifumi In order to obtain these unidentified adult Ohtaka. Ohtomo’s two slides contained only digeneans, I examined Hypomesus nipponensis eight specimens of [Trematoda] (most likely from Lake Abashiri for adult digeneans in 2016 referring to “Pronoprymna sp.”) mounted in Can- 58 T. Shimazu ada balsam. Some of Kikuchi’s specimens had seminal receptacle; ss, sinus sac; sv, seminal ves- been mounted in Canada balsam. Many others icle; t, testis; tnc, transverse nerve commissure; were still preserved in 5% formalin. They were u, uterus; usr, uterine seminal receptacle; v, vitel- stained with Heidenhain’s iron hematoxylin and larium; vd, vitelline duct; vh, ventral hollow; vs, mounted in Canada balsam. Kikuchi’s whole- ventral sucker. mounted specimens also included one each of Digenea sp. 1 and Digenea sp. 2 from Lake Class Trematoda Rudolphi, 1808 Abashiri. Although Kikuchi mentioned nothing Subclass Digenea Carus, 1863 about these specimens, she certainly examined Superfamily Microphalloidea Ward, 1901 some individuals of Hypomesus nipponensis Family Faustulidae Poche, 1926 from Lake Abashiri for parasites (Akifumi Genus Pronoprymna Poche, 1926 Ohtaka, personal communication, 12 March Pronoprymna petrowi (Layman, 1930) 2017). Kikuchi (2014) recorded Digenea sp. 1 Bray and Gibson, 1980 from Lake Takahoko (or Takahoko-numa) (a brackish-water lake) in Rokkasho Village, (Figs. 1–3) Aomori Prefecture, on the coast of the North “Monorcheides (?) petrowi” Layman, 1930: 77, 99–100, Pacific; but her specimens reexamined included fig. 35. no specimen from this lake. Orientophorus sayori Yamaguti, 1942: 367–369, fig. 19; A large number of fresh individuals of Yamaguti, 1954: 20. Orientophorus petrowi: Mamaev, Parukhin, Baeva, and Hypomesus nipponensis collected in Lake Oshmarin, 1959: 15, fig. 3, table 1. Abashiri on 25 January 2016, 28 April 2017, and Bacciger petrowi: Zhukov, 1959: 199; Zhukov, 1960: 31, 4 December 2017 were examined for adult dige- fig. 21. neans. Specimens found were either slightly flat- Pentagramma petrowi: Margolis and Ching, 1965: 393– tened and fixed in AFA or fixed in hot 10% for- 394, figs. 9–13, table 5. Faustula sayori: Yamaguti, 1958: 34; Yamaguti, 1971: 74. malin and refixed in AFA. They were then Pseudopentagramma petrovi [sic, should be petrowi]: stained with Heidenhain’s iron hematoxylin and Yamaguti, 1971, 74. mounted in Canada balsam. Pronoprymna petrowi: Bray and Gibson, 1980: 255. Measurements (length by width) are given in millimeters unless otherwise stated. Drawings Host. Hypomesus nipponensis. were made with the aid of a camera lucida. The Sites of infection. Intestine and pyloric ceca. specimens used have been deposited in the Localities. Lake Abashiri (Ohtomo, 2003; this Muguro Parasitological Museum (MPM; regis- paper); Lake Tofutsu (Kikuchi, 2014; this paper); tration code, MPM Coll. No.), Tokyo; and the Lake Takahoko (Kikuchi, 2014); and Lake National Museum of Nature and Science Koyama (Kikuchi, 2014; this paper). (NMNS; registration code, NSMT-Pl), Tsukuba. Material examined. (1) Ohtomo’s (2003) 8 Abbreviations used in the figures. cp, cirrus specimens (MPM Coll. No. 21351) of [Trema- pouch; cvd, common vitelline duct; e, esophagus; toda] (species name not given, but most likely ed, ejaculatory duct; egg, eggs in uterus and me- referring to “Pronoprymna sp.”), adult, whole- traterm; ep, excretory pore; eso, ecsoma; ev, mounted, ex intestine, [Lake Abashiri], 12 Febru- excretory vesicle; ga, genital atrium; gev, glandu- ary 2002. (2) Kikuchi’s many specimens of Dige- lar ejaculatory vesicle; gp, genital pore; hd, her- nea sp. 1 : 1 (MPM Coll. No. 21352), adult, maphroditic duct; i, intestine; Jo, Juel’s organ; whole-mounted, ex intestine, Lake Abashiri, 28 Lc, Laurer’s canal; m, metraterm; Mg, Mehlis’ May 2013 (see the Materials and Methods gland; o, ovary; od, oviduct; os, oral sucker; p, above); many (labeled Prinoprymna? [sic], Dige- pharynx; pc, prostatic cells; pp, pars prostatica; nea sp. 1 in separate fig. 1) (MPM Coll. 21353- psp, presomatic pit; sd, sperm duct; so, soma; sr, a), adult, whole-mounted, site of infection not Adult Digeneans of Hypomesus nipponensis 59 Figs. 1–3. Pronoprymna petrowi, adult specimens (NSMT-Pl 6343a) found in intestine and pyloric ceca of Hypomesus nipponicus from Lake Abashiri. 1, relatively young adult specimen, with many malformed eggs in uterus, entire body, ventral view; 2, terminal genitalia, ventral view; 3, ovarian complex, ventral view. Scale bars: 0.3 mm in Fig. 1; 0.1 mm in Figs. 2 and 3. given [most likely intestine], Lake Tofutsu, 21 adult, whole-mounted, ex intestine and pyloric April 2013 (Kikuchi, 2014); and many (MPM ceca, Lake Abashiri, 25 January 2016. (4) 22 Coll. No. 21354-a), adult, whole-mounted, site of specimens (MPM Coll. No. 21356), adult, infection not given [most likely intestine], Lake whole-mounted, ex intestine, Lake Abashiri, 28 Koyama, 2 March 2002 (Kikuchi, 2014). (3) April 2017. Many specimens (MPM Coll. No. 21355-a, Description. Based on adult specimens from NSMT-Pl 6343a, NSMT-Pl 6346b), immature, Lake Abashiri (MPM Coll. No. 21355-a, NSMT- 60 T. Shimazu Pl 6343a); 10 of them measured (Figs. 1–3). filling most of hindbody in fully mature adults; Body fusiform to ovate, small, 1.01–1.54 long, metraterm may be short. Eggs numerous, oval, 0.32–0.54 wide at testicular level; forebody operculate, bright brown, 27–32 by 16–19 µm 0.30–0.51 long, occupying 28–35% of body (collapsed). Vitellaria two, entire (not compact length. Tegument unarmed, with fine annular clusters of small follicles, enclosed by single wrinkles. Transverse nerve commissure dorsal to membrane), elliptical, 0.13–0.19 by 0.05–0.09, pharynx. Cervical glands well developed. Ventral symmetrical, immediately posterolateral to ven- hollow present, large, 0.23–0.28 by 0.20–0.30, tral sucker, immediately anterolateral to testes; surrounding ventral sucker and genital pore; con- vitelline ducts running toward median line of centric rings of muscles constituting its internal body, ventral to testes; common vitelline duct wall. Oral sucker cup-shaped, 0.11–0.16 by median, running posteriorly between testes. 0.16–0.23, subterminal. Prepharynx very short. Excretory vesicle almost V-shaped, ventral; arms Pharynx barrel-shaped, 0.05–0.07 by 0.04–0.05. reaching to esophageal level; excretory pore pos- Esophagus bifurcating anterior to ventral sucker, teroterminal. 0.02–0.05 long. Intestines ending blindly, usually Remarks. The present specimens including in testicular region. Ventral sucker 0.15–0.21 by Kikuchi’s unpublished specimen (MPM Coll. No. 0.14–0.20, sometimes embedded in ventral hol- 21352) from Lake Abashiri morphologically low; sucker width