Species Diversity 20: 73–81 25 May 2015 DOI: 10.12782/sd.20.1.073

Rediscovery of a Acanthocephalan, minor (: ), in the Lake Biwa Basin, Central Japan, with a Review of the Fish Acanthocephalan Fauna of the Basin

Kazuya Nagasawa1,2 and Masato Nitta1 1 Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima, Hiroshima 739-8528, Japan E-mail: [email protected] (KN); [email protected] (MN) 2 Corresponding author (Received 28 January 2015; Accepted 30 April 2015)

Specimens of the echinorhynchid acanthocephalan Acanthocephalus minor Yamaguti, 1935 were collected from the rectum of a dark sleeper, Odontobutis obscura (Temminck and Schlegel, 1845), in an irrigation canal near Lake Biwa, Shiga Prefecture, west-central Japan. This represents a rediscovery of A. minor in the Lake Biwa basin after a gap of nearly 80 years. It appears not to be distributed in Lake Biwa proper, but to occur rarely in rivers and irrigation canals of a limited coastal area around the lake. To date, 10 nominal of acanthocephalan in four families and three orders have been re- ported from fish in the Lake Biwa basin. Among these, striking morphological similarities between Acanthocephalus aculea- tus Van Cleave, 1931 and its congener A. opsariichthydis Yamaguti, 1935 are noted. It is furthermore suggested that A. gotoi Van Cleave, 1925 could not maintain its population after the basin’s wild population of its major host, Anguilla japonica Temminck and Schlegel, 1846, disappeared in the mid-1960s. Key Words: Acanthocephalus minor, , Odontobutis obscura, fish parasite, faunistic review, Lake Biwa basin, Japan.

rigation canal near the Ado River, one of the rivers flow- Introduction ing into Lake Biwa. Here we report on this find which rep- resents a rediscovery of the species in the Lake Biwa basin Lake Biwa is located in west-central Honshu, being the after a gap of nearly 80 years. We also take this opportunity largest (670 km2) and oldest (over four million years old) to review the fish acanthocephalan fauna of the Lake Biwa lake in Japan (Horie 1984). The fauna of this lake and its basin based on the literature published between 1918 and watershed has been intensively studied and includes many 2014. endemic species (Timoshkin et al. 2011; Kawanabe et al. 2012). The acanthocephalan fauna of fish in the Lake Biwa basin is also well studied: to date, 10 nominal species in Materials and Methods four families and three orders have been reported (Table 1). Among these species, the extent of occurrence of Acan- One specimen of O. obscura was collected using a hand thocephalus minor Yamaguti, 1935 in Lake Biwa and the net on 14 July 2014 in an irrigation canal (35°19′54″N, lake’s drainage basin remains poorly understood. This spe- 136°2′44″E) along the lower reaches of the Ado River at cies has not been reported since 1936, when it was collected Adogawacho-Kawashima, Takashima city, Shiga Prefec- from the dark sleeper Odontobutis obscura (Temminck and ture, Honshu, west-central Japan. The fish was transported Schlegel, 1845) caught in Lake Biwa (Fukui and Morisita alive to the laboratory at Hiroshima University, Higashi- 1936). Amin (2005) and Amin et al. (2007) examined the Hiroshima city, Hiroshima Prefecture, where it was mea- acanthocephalans isolated from more than 500 inspected sured for standard length (SL) in millimeters and examined fish belonging to 30 species in 12 families collected in Lake for metazoan parasites. Of the 10 acanthocephalans found, Biwa and its tributaries between 1997 and 2002 as part of a eight individuals were flattened between slides and cover large-scale survey involving 62 fish species in total from the glasses with slight pressure, fixed in 70% ethanol, stained region, but did not recover A. minor from them; moreover, in Heidenhain’s iron hematoxylin, dehydrated through a they did not mention A. minor in their discussion of the fish graded ethanol series, cleared in xylene, and mounted in acanthocephalan fauna of the Lake Biwa basin. Canada balsam, while the remaining two individuals were Recently, we found 10 individuals of A. minor infecting preserved in 100% ethanol for future molecular study. The the rectum of a specimen of O. obscura collected in an ir- stained specimens were used for measurements and counts.

© 2015 The Japanese Society of Systematic Zoology 74 K. Nagasawa and M. Nitta

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Echi - Because f ) caught in ) caught asotus P. , and , Ito (1959, as Acantho (1959, as , Ito Reference c sp.), Yamaguti (1935, 1939), Yamaguti sp.), (1975), al. et Nakajima ] sp.), P. parva P. [ sic , a (1975), Nakajima and Egusa Egusa and (1975), Nakajima al. et Nakajima (1975b), Grygier (2007), al. et (2004), Amin Grygier and (2011) Nagasawa (2007), Nagasawa and Grygier and (2007), Nagasawa al. et Amin (2011) Kawamura (1918) Kawamura Kataoka and Momma (1933, 1934, as (1933, 1934, as Momma and Kataoka Echinorhynchus (1999), (1937), Shimazu Morisita and Fukui (2007) al. et Amin (1929) Fukui Yamaguti (1935) Yamaguti Kataoka and Momma (1933, 1934) Momma and Kataoka Yamaguti (1939) Yamaguti Fukui and Morisita (1936), this study Morisita and Fukui (2007) al. et (1927), Amin Fujita (2007), Nagasawa (2007), Nagasawa al. et (2005), Amin Amin Grygierand Neoechinorhynchus (2011, as sp.) (2007) al. et (2005), Amin Amin cepharus al. et (1975a), Amin Egusa and Nakajima (2007) Golvan (1969) described(1969) Golvan newa species, O. platypusO. d , ) , (as (as

Pungtungia ); , Gnathopogon ), , Hemibarbus , Hemibarbus ) (Bagridae); (Cyprinidae); (Cyprinidae); Phoxinus oxycephalus (as Salmo (as gairdnerii ), Gasterosteidae ) ( Sarcocheilichthys variegatus variegatus Sarcocheilichthys O. uncirostrisO. uncirostris , Pseudorasbora parva Pseudorasbora ) (Salmonidae) (Gobiidae); brevispinis Tridentiger sp., (Siluridae) , H. barbus (as Salmo (as gairdnerii irideus , Opsariichthys uncirostris uncirostris Pelteobagrus nudiceps Pelteobagrus (as Leucogobio Leucogobio (as caerulescens ), Gnathopogon by Harada (1935), but Petrochenko (1956) and Yamaguti (1963) listed the former spe - the former (1963) listed Yamaguti (1956) and Petrochenko (1935), but Harada by , Opsariichthys uncirostris uncirostris (Cyprinidae) f ) (Siluridae) asotus Parasilurus (as Rhinogobius ) (Bagridae); Misgurnus anguillicaudatus , C. carpio (); Cyprinus carpio reinii ) (Plecoglossidae) , e (Salmonidae) Fish speciesFish (family) Tanakia lanceolata, Tanakia limbata Tanakia lanceolata, ), Tanakia Opsariicthys uncirostris uncirostris , esocinus esocinus Pseudogobio , , Oncorhynchus mykiss (as Zacco (as platypus (as Zacco (as platypus platypus Opsariichthys , ) castanea isaza Chloea (as Gymnogobius ) (Cyprinidae); (as P. (as altiv eli s ) S. variegatus (as sp. (Cyprinidae) (Sinipercidae) Plecoglossus altivelis altivelis Plecoglossus ) (Osmeridae); nipponensis H. transpacificus (as subsp. 2 (as G. 2 (as microcephalus subsp. aculeatus Gasterosteus (Cyprinidae); (Cottidae); reinii Cottus (Cobitidae); Lefua echigonia (Centrarchidae); (Odontobutidae) Fluvidraco nudiceps Fluvidraco (as The paper of Kataoka and Momma (1937) was part of a set of collected papers, and and of collectedof a set (1937) was papers, part Momma and Kataoka of The paper E. cotti. of synonym a junior to (as Zacco (as sieboldii (Anguillidae); Hemibarbus barbus (Anguillidae); Cyprinus carpio Tachysurus nudiceps (Anguillidae); Tachysurus ] uncirostris sp. (Salmonidae); Silurus (Salmonidae); sp. asotus Cottus pollux Cottus (Channidae); , Hemibarbus barbus elongatus elongatus Gnathopogon (Cobitidae); (Cobitidae) Hemibarbus barbus [ sic sp., was first prepared in 1998 but was not published until 2011. This acanthocephalan was described as Acanthosentis 2011. This acanthocephalan until published not was but in 1998 prepared first was sp., ) (Siluridae) asotus Parasilurus (as 2007). al. et (Amin actually C. reinii was Lake Biwa (1939) from Yamaguti by pollux reported as Cottus fish The , Gymnogobius isaza , Gymnogobius (Cyprinidae); e ), Sarcocheilichthys was collected in Lake Biwa. Thus, this fish is cited here from Yamaguti (1935). Yamaguti from here cited is fish this collected Thus, was Lakein Biwa. ) (Plecoglossidae); Silurus biwaensis altivelis ( as P. ), Oncorhynchus masou ishikawae Hemibarbus longirostris , ), jouyi o. Rhynchocypris (as Micropterus salmoides Micropterus sieboldii Candidia kawamebari Coreoperca Gymnogobius isaza Oncorhynchus (Gobiidae); mykiss Gymnogobius (Gasterosteidae); irideus Tachysurus nudiceps Tachysurus Candidia platypus Candidia (Cobitidae); mayedae Tribolodon hakonensisTribolodon subsp. 2 (as G. 2 (as microcephalus subsp. aculeatus Gasterosteus (Cyprinidae); herzi Anguilla japonica Anguilla jouyi Silrus asotus japonica Anguilla ) (Gobiidae) urotaenia annularis Chaenogobius (as urotaenia Gymnogobius Odontobutis obscura Cobitis biwae labeo Rhodeus ocellatus ocellatus Rhodeus ocellatus microoculus Hypomesus nipponensis caerulescens altivelis Oncorhynchus masou ishikawae Oncorhynchus Cobitis biwae Plecoglossus altivelis altivelis altivelis Plecoglossus japonica Anguilla argusChanna Opsarichthys S. (as pluvius japonicus leucomaenis Salvelinus (Gobiidae); P. parva P.

b

sp. was described. was sp. Acanthocephalus echigoensis Acanthocephalus with been had synonymized Nakajima Nakajima , curta ( P. sevenfish speciesfrom of specimens using d Yamaguti, 1935 Yamaguti, (2007), only only (2007), al. et ) alternatspinus ) parareceptacilis Van Cleave, 1931 Cleave, Van - as S. variega (1927) Fujita by reported 2013), the fish (Hosoya watershed its ) occur and in Lake Biwa microoculus S. variegatus , and variegatus S. variegatus Fukui, 1929 Fukui, Yamaguti, 1935 Yamaguti, Van Cleave, 1925 Cleave, Van Yamaguti, 1935 Yamaguti, (Van Cleave, 1925) Cleave, (Van sp. and species and Genus ( Acanthosentis ( Acanthosentis Acanthocephalus aculeatus Acanthocephalus , ( S. biwaenisis b Southwellina hispida Southwellina Pseudorhadinorhynchus samegaiensisPseudorhadinorhynchus 1975 Egusa, and Echinorhynchus parasiluri Echinorhynchus Acanthocephalus gotoi Acanthocephalus Acanthocephalus minor Acanthocephalus Acanthocephalus opsariichthydis Acanthocephalus Amin, 2005 Amin, Acanthosentis Acanthosentis 2005 Amin, Acanthocephalus aculeatus Acanthocephalus Echinorhynchus cotti by Amin (2005). Amin by Family Polymorphidae Quadrigyridae Echinorhynchidae (2007) relegated E. oblitus (2007) relegated al. et Nagasawa (1937), but Momma and Kataoka citing , by alternatspinus ) Acanthocephalus opsariichthydis described (1935) Acanthocephalus Yamaguti c Acanathocephalans reported from fish in the Lake Biwa basin, Shiga Prefecture, Japan. Prefecture, Shiga in basin, Biwa the fish Lake from reported Acanathocephalans 1. cannot be exactly identified. cannot Acanthocephala s report, including information on Neoechinorhynchus on information Grygier and including ’ s report, Nagasawa of manuscript The three localities, Lake Biwa (Shiga Prefecture), Lake Ogura (Kyoto Prefecture), and the Yodo River (Osaka Prefecture), all of which belong to the same river system, but he did not differentiate these localitieseach from differentiate did not he but system, river the same to which belong all of (Osaka Prefecture), River the Yodo and Prefecture), Lake Ogura (Kyoto Prefecture), localities,three (Shiga Lake Biwa Amin to according the species. However, of description his in other ( Acanthosentis three species and subspecies of Sarcocheilichthys subspecies of speciesthree and tus a norhynchus oblitus the original work was Kataoka and Momma (1934), in which Echinorhynchus Momma and Kataoka was the original work cies as valid. valid. as cies Unidentified Unidentified Gyracanthocephala Echinorhynchida Table A fish parasite from the Lake Biwa basin 75

All measurements in the text are given in millimeters as the range followed by the mean in parentheses, unless other- wise stated. Drawings were made with the aid of a drawing tube fitted on an Olympus BX 51 compound microscope. The mounted specimens are deposited in the Aschelmin- thes (As) collection of the National Museum of Nature and Science (NSMT–As 4293), Tsukuba city, Ibaraki Prefecture, Japan. The scientific names of fish, amphipods, and isopods used in this paper follow those recommended by Nakabo (2013), Tomikawa and Morino (2012), and Matsumoto (1973), respectively.

Acanthocephalus minor Yamaguti, 1935 (Fig. 1)

Acanthocephalus minor Yamaguti, 1935: 253–254, figs 3–5 (type locality: Toyama Prefecture, Japan); Fukui and Morisita 1936: 761; Yamaguti 1939: 322–323; Petro- chenko 1956: 311, fig. 126; Fukui 1962: 128; Yamada 1962: 277, fig. H; Yamaguti 1963: 47; Fukui 1965: 468, figs 1–3; Golvan 1969: 276, fig. 213; Awakura 1972: 1–12, figs 1–8; Fukui 1973: 275, fig. 14-5; Uchida 1979: 149, fig. 6; Awakura 1980: 207; Nagasawa et al. 1982: 229–231; Awakura et al. 1984: 10; Amin 1985: 42; Nagasawa et al. 1987: 35; Awakura 1989: 608; Golvan 1994: 137; Shima- zu 1999: 23–24; Araki 1999: 159; Araki 2003: 149; Amin 2013: 285; Yokoyama and Nagasawa 2014: 84. Acanthocephalus echigoensis: Anonymous 1972: 146–148; Awakura 1973: 12–14, unnumbered fig.

Description. General. Trunk subcylindrical, unarmed, slightly tapering posteriorly. Body wall thick. Proboscis cy- lindrical, armed with 12–14 (usually 13) longitudinal rows of 5–7 (usually 5 or 6) hooks in both sexes. Second or third hook from distal end largest and basal hook smallest in each row. Hook blade longer than root. Neck short. Proboscis re- ceptacle double-walled, with cerebral ganglion near its pos- terior end. Lemnisci saccular or elongate, longer than pro- boscis receptacle. Genital pore terminal. Male (based on four specimens). Trunk 2.45–3.03 (2.72) long, 0.79–0.91 (0.84) wide. Proboscis 0.35–0.45 (0.39) long, 0.21–0.23 (0.21) wide. Blade of largest (i.e. second or third) hook in each row 65–74 (70) µm long; blade of smallest (i.e. basal) hook in each row 38–51 (47) µm long. Neck 0.15– 0.21 (0.18) long (n = 2), 0.37–0.41 (0.39) wide at junction with trunk (n = 2). Proboscis receptacle 0.34–0.40 (0.38) long, 0.19–0.23 (0.21) wide. Lemnisci 0.26–0.48 (0.36) long, 0.6–0.18 (0.11) wide. Testes oval, slightly oblique. Anterior testis 0.34–0.35 (0.34) long, 0.22–0.28 (0.25) wide; posterior testis 0.30–0.34 (0.33) long, 0.20–0.27 (0.22) wide. Cement glands pyriform, close together, 0.10–0.18 (0.12) wide in diameter, immediately behind posterior testis. Saefftigen’s pouch bulb-shaped, 0.35–0.43 (0.39) long, 0.20 (0.20) wide (n = 2). Female (based on four specimens). Trunk 2.05–3.35 Fig. 1. Acanthocephalus minor Yamaguti, 1935, NSMT–As 4293, (2.62) long, 0.88–1.18 (1.03) wide. Proboscis 0.40–0.50 from rectum of Odontobutis obscura (Temminck and Schlegel, (0.47) long, 0.19–0.29 (0.24) wide. Blade of largest (i.e. sec- 1845). A, Entire body of male; B, proboscis of female. Scale bars: A, ond or third) hook in each row 85–92 (87) µm long; blade 1 mm; B, 100 µm. 76 K. Nagasawa and M. Nitta of smallest (i.e. basal) hook in each row 43–75 (60) µm long. Neck 0.17–0.23 (0.19) long, 0.38–0.53 (0.44) wide at junc- Discussion tion with trunk. Proboscis receptacle 0.30–0.54 (0.42) long, 0.19–0.26 (0.24) wide. Lemnisci 0.23–0.48 (0.36) long, 0.8– Occurrence and geographical distribution of Acan- 0.15 (0.10) wide. Reproductive system 0.50–0.73 (0.61) long, thocephalus minor in the Lake Biwa basin. There is a 21.6–25.5% (23.6%) of trunk length. Mature eggs with polar nearly 100-year history of research on the fish acantho- prolongations of middle shell 96–104 (99) µm long, 17–20 cephalans of Lake Biwa and its drainage basin (Kawamura (18) µm wide when measured through body wall. 1918; Fujita 1927; Fukui 1929; Kataoka and Momma 1933, Host. Dark sleeper Odontobutis obscura (Perciformes: 1934; Yamaguti 1935, 1939; Fukui and Morisita 1936, 1937; Odontobutidae). Ito 1959; Nakajima et al. 1975; Nakajima and Egusa 1975a, Locality. Irrigation canal near Ado River at Adogawa- 1975b; Shimazu 1999; Grygier 2004; Amin 2005; Amin et cho-Kawashima, Takashima city, Shiga Prefecture, Honshu, al. 2007a, 2007b). In particular, during the 1930s, Yamaguti Japan. (1935, 1939) conducted a systematic survey of fish parasites Site of infection. Rectum. in Japan including the Lake Biwa basin but did not report Occurrence in fish. Ten individuals of A. minor were A. minor from the basin. Later, Amin et al. (2007) reported found in one specimen of O. obscura (64.3 mm SL). The acanthocephalans recovered from an examination of over eight stained specimens comprised four individuals of each 500 individuals of fish belonging to 30 species in 12 families sex. collected from 22 localities including Lake Biwa proper and Remarks. The morphology of the specimens collected various rivers, irrigation canals, and ponds in Shiga Prefec- in this study almost fully corresponds to the original de- ture during 1997–2002, but did not report A. minor among scription of A. minor by Yamaguti (1935) and the subse- them. Only Fukui and Morisita (1936) found A. minor in O. quent brief descriptions of the species by Fukui and Morisita obscura from the Lake Biwa basin 80 years ago, which sug- (1936), Yamaguti (1939), and Awakura (1972), except that gests that this acanthocephalan is a rare species occurring in the number (5–7) of hooks per longitudinal row is fewer a limited area of this basin. than in previous reports (7–9: Yamaguti 1935; 6–7: Fukui Fukui and Morisita (1936) simply reported “Lake Biwa” and Morisita 1936; 6–8: Yamaguti 1939; 7–9: Awakura as the sampling locality of A. minor, but this may not be 1972). wholly accurate because Lake Biwa is the largest lake in Acanthocephalus minor was originally described based Japan and many rivers, streams, and irrigation canals flow on specimens from Amur catfish Silurus asotus Linnaeus, into it. The acanthocephalan specimens were not collected 1758 (as Parasilurus asotus) in Toyama Prefecture, central by these authors but were given to them by a colleague. The Honshu, Japan (Yamaguti 1935). Subsequently, this acantho- host, Odontobutis obscura, is usually found in the upper and cephalan has been recorded from various freshwater fish in middle reaches of the lake’s tributaries and only rarely oc- central Honshu and Hokkaido, Japan (Fukui and Morisita curs in coastal waters of the lake (Shiga-Kenritsu Biwako- 1936; Yamaguti 1939; Awakura 1972; Nagasawa et al. 1982). Bunkakan 1980). Two large-scale surveys of the freshwa- There is no record of this species from other countries. Pet- ter fish fauna of Lake Biwa and its tributaries conducted in rochenko (1956: 293) doubted the generic assignment of the 1994–1995 and 2002–2003 also showed that the fish does species, but subsequent authors (e.g., Yamaguti 1963; Gol- not occur in Lake Biwa proper (Anonymous 1996, 2004). van 1969, 1994; Amin 1985, 2013) have continued to place it Therefore, the specimen of O. obscura reported by Fukui in Acanthocephalus Koelreuther, 1771. Awakura (1973) used and Morisita (1936) most probably was not caught in “Lake Acanthocephalus echigoensis Fujita, 1920 as the scientific Biwa” but in one of the rivers flowing into the lake. Since A. name of acanthocephalans that had heavily infected fish at a minor utilizes the asellid isopod Asellus hilgendorfii Boval- trout hatchery in Hokkaido (see also Anonymous 1972), but lius, 1886 as its intermediate host (Awakura 1972; Nagasawa this was definitely wrong because the same author (Awakura et al. 1982), it is desirable to clarify the distribution pattern 1972) had already identified the parasite as A. minor based of infected isopods in those rivers and irrigation canals. on its morphological characteristics. Currently, some irrigation canals close to the shore of In 1936, A. minor was found in Odontobutis obscura in Lake Biwa have been recognized as habitats of O. obscura “Lake Biwa” (Fukui and Morisita 1936; see the Discussion (Funao et al. 2010; Natsuhara and Akiyama 2012). In the section herein concerning this locality), but this acantho- present study, the infected specimen of O. obscura came cephalan has not been reported from the lake or associated from an irrigation canal in Takashima city, near (7–8 km waters by any subsequent researcher (e.g., Fukui and Moris- away from) an other irrigation canal in which Amin et al. ita 1937; Yamaguti 1939; Amin et al. 2007). The finding of (2007: fig. 1) found four species of acanthocephalan, viz., A. minor in this study confirmed its occurrence in the Lake Acanthocephalus opsariichthydis Yamaguti, 1935; Echino- Biwa basin. rhynchus cotti Yamaguti, 1935; Pseudorhadinorhynchus sa- All of the present individuals of A. minor were found in megaiensis Nakajima and Egusa, 1975; and Southwellina the rectum of the fish examined. This site specificity of A. hispida (Van Cleave, 1925). The irrigation canals sampled minor within the host’s intestine was previously noticed by are both located near the northwestern shore of Lake Biwa. Nagasawa et al. (1982). Abundant water is stably supplied from springs to the irri- gation canals throughout the year (Yasuhiro Fujioka, Lake A fish parasite from the Lake Biwa basin 77

Biwa Museum, personal communication). Considering the (Van Cleave 1931), and 72–150 µm long in A. opsariichthy- fact that as many as five species of acanthocephalan oc- dis (Yamaguti 1935). The specimens reported as A. aculea- curred in such irrigation canals, it is likely that the canals tus from Lake Biwa possessed 8–10 longitudinal rows of 3–6 provide favorable environmental and biological conditions hooks (Kataoka and Momma 1933, 1934), fewer hooks per for the parasites to complete their life cycles. row than Van Cleave (1931) reported. A clarification of the The fish acanthocephalan fauna of the Lake Biwa taxonomic status of A. aculeatus vis-à-vis A. opsariichthydis basin. To date, 10 nominal species of fish acanthocepha- is necessary but is beyond the scope of this paper. lan have been reported from the Lake Biwa basin (Table 1). No similar suggestion of synonymy applies to two other Nishino (2012) made a similar list of fish acanthocephalans species of Echinorhynchus Zoega in Müller, 1776: E. cotti of the basin, but some references (viz., Kawamura 1918; and E. parasiluri Fukui, 1929. Like A. opsariichthydis, E. cotti Fujita 1927; Fukui and Morisita 1936; Ito 1959; Amin et al. is a common parasite of fish in the Lake Biwa basin (Amin 2007b; Nagasawa and Grygier 2011) were not cited. Because et al. 2007; see Table 1 herein), but there is only one record Lake Biwa is an ancient lake (over four million years old; of E. parasiluri from this basin (Fukui 1929). Both species Horie 1984) and many endemic species occur in it (Nishino are easily differentiated from each other by the proboscis ar- and Watanabe 2000; Kawanabe et al. 2012), potential ende- mament: 16–20 longitudinal rows of 11–13 hooks in E. cotti mism of fish acanthocephalans has also been discussed. In (Yamaguti 1935, 1939) versus 22–26 longitudinal rows of particular, Pseudorhadinorhynchus samegaiensis has been 10–11 hooks in E. parasiluri (Fukui 1929). Fukui (1929) re- suggested to have such a status (Grygier 2004; Amin et al. ported the host of E. parasiluri as Amur catfish Silurus aso- 2007; Nagasawa and Grygier 2011). This acanthocephalan tus, but because two other, endemic species of Silurus were was originally described from rainbow trout Oncorhynchus later described from Lake Biwa, and the identity of Fukui’s mykiss (Walbaum, 1792) (as Salmo gairdnerii iredeus Gib- fish could not be checked, this host was later reported as “Si- bons, 1885) at a trout hatchery in the basin (Nakajima and lurus sp. (presumably S. asotus Linnaeus, 1758)” (Amin et Egusa 1975b), but this salmonid is not a native host, hav- al. 2007). Amin et al. (2007) did not find E. parasiluri in five ing been introduced into Japan from North America from specimens of S. asotus and two specimens of rocky catfish S. 1877–1934 and 1951–1955 as eyed eggs (Maruyama et al. lithophilus (Tomoda, 1961) but these authors attributed the 1987). Pseudorhadinorhynchus samegaiensis does not occur absence of infection to the small number of fish examined. in North America (Hoffman 1999), and is surely native to Acanthocephalus gotoi Van Cleave, 1925 was reported, Japan. Among seven other species of infected fish in the similarly to A. aculeatus, only once in the late 1930s in the basin reported by Amin et al. (2007), only big-scaled redfin Lake Biwa basin (Yamaguti 1939; see Table 1 herein). Since Tribolodon hakonensis (Günther, 1877) harbored gravid fe- its original description from Japanese eel Anguilla japonica males, so this cyprinid may be the native preferred host. If Temminck and Schlegel, 1846 in Tokyo, Japan (Van Cleave so, endemic status of P. samegaiensis in the Lake Biwa basin 1925), this acanthocephalan has been found in several would be doubtful because T. hakonensis is not endemic to freshwater fish, especially from A. japonica, in various parts the basin but is widely distributed in Japan, ranging from of Japan (Yamaguti 1935, 1939; Fukui and Morisita 1936; Hokkaido to Kyushu (Kurawaka 1977; Sakai 1995). The Katahira and Nagasawa 2014; Nagasawa unpublished data), acanthocephalan fauna of T. hakonensis in other parts of its so it cannot be said to be rare in Japan. The current appar- range should be intensively examined. ent absence of A. gotoi in the Lake Biwa basin is, therefore, Of the four species of Acanthocephalus reported in the unusual. One reason for this absence may be that the wild Lake Biwa basin, A. opsariichthydis has been found in a total population of A. japonica disappeared in the basin after of 15 species of fish in five families, whileA. aculeatus Van 1964 when the Amagase Dam was completed in the Uji Cleave, 1931 was collected only from ayu Plecoglossus altive- River, which flows, first as the Seta River, from Lake Biwa. lis altivelis (Temminck and Schlegel, 1846) (as P. altiv eli s ) in As a result, the acanthocephalan might have lost its major the early 1930s (Kataoka and Momma 1933, 1934). The tax- (perhaps preferred) host (A. japonica), resulting in its disap- onomic status of A. aculeatus remains poorly understood. It pearance from the basin. Since the dam prevents juveniles was originally described from sockeye salmon (as the land- of A. japonica from migrating upstream to the lake (Anony- form of blue-back salmon) Oncorhynchus nerka (Walbaum, mous 2007), no wild population of eels has existed in Lake 1792) in Lake Aoki (as Aoki Lake), Nagano Prefecture (as Biwa and its watershed since the mid-1960s. Currently, A. Shinano Province), central Japan (Van Cleave 1931). Harada japonica is found in the lake, released by fishermen after (1935) synonymized it with A. echigoensis, but since then having been raised at fish farms. No infection by A. gotoi its taxonomic relations with other Japanese species of the was actually detected in recently collected individuals of genus, including A. opsariichthydis, have not been examined A. japonica in the Lake Biwa basin (Amin et al. 2007). This or discussed. may imply, in other words, that A. gotoi needs A. japonica to Morphologically, A. aculeatus and A. opsariichthydis are sustainably maintain its population even though this worm quite similar to each other. The proboscis armament, for can infect various freshwater fish. example, is 8–10 longitudinal rows of seven or eight hooks Unidentified acanthocephalans were found by Fujita in A. aculeatus (Van Cleave 1931), and nine longitudinal (1927) in eight species of fish in Lake Biwa (see Table 1). rows of 5–7 hooks in A. opsariichthydis (Yamaguti 1935); the These fish were reported as “the most common in Lake blade of the longest hook is 94–161 µm long in A. aculeatus Biwa” (Fujita 1927: 39), but yamato char Salvelinus leu- 78 K. Nagasawa and M. Nitta comaenis japonicus Oshima, 1961 (as S. pluvius (Hilden- phipod Gammarus sp. (misspelled as Gonmarus sp. and dorf, 1876)), one of the fish examined by him, could not Ganmarus sp.) and the asellid isopod Asellus hilgendorfii (as have been caught in the lake proper, because this species A. nipponensis Nicholas, 1929) at a trout hatchery. However, is restricted to the upper reaches of rivers in the lake basin two species of acanthocephalan, Acanthocephalus opsariich- (Shiga-Kenritsu Biwako-Bunkakan 1980; Anonymous 1996, thydis and Pseudorhadinorhynchus samegaiensis, and the an- 2004). The fish parasite surveys on which Amin et al. (2007) isogammarid amphipod Jesogammarus (Annanogammarus) was based included as many as 62 species of fish from Lake fluvialis Morino, 1985 (as J. fluvialis) are known to occur at Biwa and its tributaries, but not S. leucomaenis japonicus. this hatchery (Nakajima et al. 1975; Nakajima and Egusa An appraisal of its acanthocephalan parasites is desirable. 1975a, 1975b for the acanthocephalans: Morino 1985; Ku- Another fish from which Fujita (1927) reported an un- sano 2009 for the amphipod), thus Ito’s (1959) work needs identified acanthocephalan was pond loach Misgurnus an- a re-study. guillicaudatus (Cantor, 1842), but this fish is rare in the lake Without providing any information on the larval mor- proper and occurs in shallow swamps, ponds, brooks, and phology of E. cotti, sampling locality, or date, Shimazu paddy fields around it (Shiga-Kenritsu Biwako-Bunkakan (1999) stated that the intermediate host of E. cotti in Lake 1980). Knowledge of the acanthocephalan fauna of M. an- Biwa is the anisogammarid amphipod Jesogammarus (An- guillicadatus is quite limited in Japan, with only the descrip- nanogammarus) naritai Morino, 1985 (as J. naritai). This tion of the pomphorhynchid (originally referred to as an amphipod is found in coastal waters of the lake throughout echinorhynchid) Tenuiproboscis misgurni Yamaguti, 1935 the year (Narita 1976; Morino 1985, 1994). A detailed life- from an unknown locality (Yamaguti 1935). As Amin et al. history study of E. cotti using this amphipod intermediate (2007: 250) pointed out, M. anguillicaudatus is a future tar- host is desired in the field and the laboratory. In addition, get for better understanding the fish acanthocephalan fauna another species of anisogammarid amphipod Jesogammarus of Japan as well as the Lake Biwa basin. (Annanogammarus) annandalei (Tattersall, 1922) occurs in As a result of the large-scale parasitological survey of fish offshore, deeper waters of Lake Biwa (Narita 1976; Morino in and around Lake Biwa on which Amin et al. (2007) was 1985, 1994; Ishikawa and Urabe 2002). It is thus important based, information on the comparative host utilization, oc- to search for larval E. cotti in material of this amphipod as currence, and maturity between two seasons (spring and well, and assess a difference in host utilization by the acan- autumn) and on geographical distribution of fish acantho- thocephalan in these congeneric amphipods at various cephalans in this region is now available. Of the three most depths in the lake. common acanthocephalans (viz., A. opsariichthydis, E. cotti, Asakawa and Nishino (2011) reported 10 juveniles of a and P. samegaiensis) in this region, E. cotti has been sug- polymorphid acanthocephalan collected in a free condition gested to be restricted to “Lake Biwa proper, including river from a benthos sample taken in Lake Biwa. These authors mouths” (Amin et al. 2007: 251, fig. 1). This acanthocepha- stated that the juveniles resembled an acanthocephalan of lan was originally described by Yamaguti (1935) from Japa- aquatic-birds, Polymorphus (Polymorphus) strumosoides nese fluvial sculpin Cottus pollux Günther, 1873 in Shiga Lundström, 1942, but based on the morphological features Prefecture (in the Lake Biwa basin) and later collected by given by the authors, they seem almost identical with Pseu- the same author (Yamaguti 1939) from the same host spe- dorhadinorhynchus samegaiensis. The only difference is the cies (C. pollux) in the lake. Two species of the genus Cottus number of hook rows on the proboscis, i.e., 16 rows in the Linnaeus, 1758, C. pollux and C. reinii Hilgendorf, 1879 (the benthic-caught juveniles (Asakawa and Nishino 2011) and latter called utsusemi-kajika), occur in the Lake Biwa basin, 13–14 rows in P. samegaiensis (Nakajima and Egusa 1975b; but their distribution ranges do not overlap: C. pollux in- Amin et al. 2007). It is desirable to re-examine Asakawa and habits the upper reaches of rivers, while C. reinii is distrib- Nishino’s (2011) specimens to ascertain their identity at the uted in the lake and the lower reaches of rivers (Anonymous generic and specific levels. 1996, 2004; Fujioka and Kido 1998; Fujioka et al. 2014). Amin et al. (2007) examined well-developed cystacanths Thus, the host reported by Yamaguti (1939) was definitely of S. hispida from the body cavity of six species of fish in the not C. pollux but C. reinii, and as suggested by Amin et al. Lake Biwa basin. The final hosts of this acanthocephalan (2007), the host in the original description (Yamaguti 1935) are fish-eating birds (García-Verela et al. 2012), and the fish was perhaps also C. reinii. The observed high proportion reported by Amin et al. (2007) are considered to serve as (63%) of gravid females of E. cotti in C. reinii (Amin et al. paratenic hosts for the parasite. Yamaguti (1935, 1939) and 2007: table 1) implies that this acanthocephalan should be Katahira and Nagasawa (2014) provide the other known fish able to use its close relative C. pollux as a preferred host as hosts from Japan. It is necessary to discover the first inter- well. However, seven specimens of C. pollux from the Seri mediate hosts of this species (e.g., amphipods; see Lisitsyna River examined in November, 2000, in the course of the 2011) in order to clarify its life cycle in the basin. No infor- above-mentioned surveys were not infected (Mark J. Grygi- mation is yet available on the life history of the two quad- er, Lake Biwa Museum, personal communication). rigyrids, Acanthogyrus (Acanthosentis) alternatspinus Amin, Little information is available as to the life history of fish 2005 and A. (A.) parareceptaclis Amin, 2005, which were acanthocephalans in the Lake Biwa basin. Ito (1959) found recently described from the basin (Amin 2005). Acantho- larval acanthocephalans, identified as Acanthocephalus sp. gyrus (A.) alternatspinus was from an introduced fish host, (misspelled as Acanthocepharus sp.) in the gammarid am- Rhodeus ocellatus ocellatus (Kner, 1866), but it is unknown A fish parasite from the Lake Biwa basin 79 whether this acanthocephalan is an introduced species. etc.]. The Investigative Commission on Evaluation of the Impact of the Amagase Dam on Upstream and Downstream Migration of In conclusion, the Lake Biwa basin is the best studied Fish, etc., Osaka, 380 pp. [In Japanese] body of freshwater in Japan as concerns the fish acantho- Araki, J. 1999. [Acanthocephalans from Japan]. Pp. 147–162. In: Otsu­ cephalan fauna, and no other lake basin in Japan has been ru, M., Kamegai, S. and Hayashi, S. (Eds) Nihon ni okeru Kisei- reported to bear such a rich fauna of these parasites. Nev- chugaku no Kenkyu [Progress of Medical Parasitology in Japan], ertheless, the past investigations of fish acanthocephalans Vol. 6. Meguro Parasitological Museum, Tokyo. [In Japanese] in this basin have focused on their . As reviewed Araki, J. 2003. Acanthocephalans from Japan. Pp. 147–159. In: Otsuru, above, no paper except Amin et al. (2007) has treated their M., Kamegai, S., and Hayashi, S. (Eds) Progress of Medical Para- ecology and host-parasite relationships, and much remains sitology in Japan, Vol. 7. Meguro Parasitological Museum, Tokyo. poorly understood about their life cycles. More work is Asakawa, M. and Nishino, M. 2011. A case report of acanthocephalans found in dredging samples derived from Lake Biwa, Japan. Jour- needed on various aspects of the biology of fish acantho- nal of Rakuno Gakuen University 35: 91–94. [In Japanese with cephalans in the Lake Biwa basin. English abstract] Awakura, T. 1972. Studies on acanthocephaliasis of the salmonid infected by Acanthocephalus minor Yamaguti, 1935. Scientific Re- Acknowledgments ports of the Hokkaido Fish Hatchery 27: 1–12. [In Japanese with English abstract] We thank Tomohiko Morimune, Taiki Ito, and Kazuhiro Awakura, T. 1973. [Acanthocephaliasis]. Uo to Mizu 8: 12–14. [In Tanaka, Faculty of Agriculture, Kinki University, for as- Japanese] sistance in fish sampling. We are also grateful to Yasuhiro Awakura, T. 1980. On the parasites and parasitic diseases of salmonid Fujioka, Lake Biwa Museum (LBM), for support during the fish in Hokkaido. Fish Pathology 14: 207–209. [In Japanese with English abstract] study. Thanks go to Mark J. Grygier, LBM, and two anony- Awakura, T. 1989. Parasitology of masu salmon, Oncorhynchus masou, mous reviewers for valuable comments to improve the man- in northern Japan. Physiology and Ecology Japan, Special Volume uscript. 1: 605–614. Awakura, T., Tanaka, T., Sakai, K., and Koide, N. 1984. [Survey of pathogens in masu and amago salmon in rivers. 1. Masu salmon References of Hokkaido, 2. masu salmon of Honshu (the Sea of Japan side)]. Pp. 3–12. In: Showa 55–57-nendo Kinkai-gyogyo-shigen no Kagyo- Amin, O. M. 1985. Classification. Pp. 27–72.In : Crompton, D. W. T. ka Sisutemu no Kaihatsu ni kansuru Sogokenkyu (Marin Rantingu and Nickol, B. B. (Eds) Biology of the Acanthocephala. 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