Argulus coregoni Thorell, 1864

Nagasawa, Kazuya, Uchiyama, Ryu & Tomikawa, Ko, 2024, Argulus coregoni (Crustacea: Branchiura: Argulidae) Parasitic on a Dark Chub Nipponocypris temminckii (Cypriniformes: Xenocyprididae) in a Stream, Central Japan, with a List of Its Known Hosts in East Asia, Species Diversity 29 (2), pp. 181-197 : 183-188

Argulus coregoni Thorell, 1864

[Japanese name: Chou-modoki ( Tokioka 1965)] ( Figs 1B , 2–5 )

Material examined. One adult male (NSMT-Cr 31596).

Adult male. Body dorsoventrally flattened, measuring 4.2 mm in total length (from anterior tip of carapace to posterior tip of abdomen) and 2.5 mm in maximum body width (around midlength of carapace).

Carapace (including posterolateral lobes) nearly circular, covering totally or almost totally coxa and basis of first to third pairs of legs and partially fourth pair of legs in dorsal view; 3.0 mm long, comprising 71.4% of total length ( Figs 2 , 5 ). Frontal region of carapace delimited by anterolateral indentations and protruding anteriorly; anterior margin rounded. Central longitudinal ribs distinct and bifurcated at anterior ends; transverse ribs evident behind nauplius eye ( Fig. 2A ). Paired compound eyes well visible, dorsally located at level of anterolateral indentations of carapace ( Fig. 2A ). Nauplius eye located posterior to compound eyes in midline of carapace. Dorsal surface of carapace smooth without spines. Ventral surface of frontal and anterolateral regions of carapace ornamented with numerous, small posteriorly directed spines ( Fig. 2B ). Posterolateral lobes of carapace not overlapping, ending in rounded margin, separated by sinus 26.7% as long as carapace ( Fig. 2A ). Respiratory areas located at level between second maxillae and third pairs of legs; smaller anterior area nearly oval, located near anterior margin of posterior area; larger posterior area kidney-shaped, with notch on mesial margin ( Figs 2B , 3A , 5 ). Thorax with four segments, bearing small spiniform projections ventrally ( Figs 2 , 5 ). Abdomen longer than wide, with some, very small spines on anterolateral margins; anal indentation 44.4% as long as abdomen to form two lobes; each lobe becoming wider toward mid-length of abdomen, then tapering posteriorly, ending in pointed margin ( Figs 2 , 5 ). Paired testes each elliptical, located in anterocentral portion of abdomen, extending past base of anal indentation ( Figs 2 , 5 ). Caudal rami located at base of anal indentation, with four naked setae on posterior margin of each ramus ( Figs 2A , 3B ).

First antennae with four segments ( Fig. 3C, D ): first segment heavily sclerotized in mesial and posterior regions, with large blunt projection on posterior margin; second segment largest and heavily sclerotized, with large blunt projection on anterior margin, strong lateroventrally directed hook at distal corner, and large projection ventrally near posterior margin; third segment cylindrical, with three naked setae; apical segment shorter than third segment, with four and two naked setae near and at tip, respectively. Second antennae with five segments ( Fig. 3C, E ): first segment sclerotized, with large blunt projection and small swelling bearing six naked setae on posterior margin, and small spine near distal margin; second segment shorter than first, armed with four naked setae on posterior margin and three naked setae near distal margin; third, fourth, and apical segments nearly cylindrical and decreasing in length; third segment with three naked and two short naked setae near distal margin; fourth segment with eight naked setae near distal margin; apical segment with three naked setae at tip. Postantennal spines large and robust, each located posterior to projection of first segment of first antenna ( Fig. 3C ). Preoral sheath cylindrical and visible on ventral midline of carapace posterior to postantennal spines; anterior portion of stylet protruding from opening of preoral sheath ( Figs 2B , 3F ). Mouth tube without ornamentation located posterior to preoral sheath, becoming wider posteriorly; posterior portion composed of anterior labrum and posterior labium bearing pair of tiny spines ( Figs 2B , 3G ).

First maxillae forming well developed cup-like suckers ( Fig. 2B ), each with 60 supporting rods in sucker membrane. Supporting rods each composed of six or seven sclerites; sclerites at base nearly oblong but others oval or slightly trapezoidal and decreasing in size distally ( Fig. 3H ). Outer margin of rim of sucker membrane ornamented with numerous apically pointed projections. Second maxillae with five segments ( Fig. 3I ): first segment robust, with three large, blunt, almost equally long projections on posterior margin; corpus of first segment with raised oval field bearing many denticles plus two long and 14 shorter naked setae near and on posterior margin, respectively ( Fig. 3J ); second segment longer than first, with two long naked setae and denticles (some with serrated margin) on distal portion of anteroventral surface ( Fig. 3I ); third segment shorter and narrower than second segment, with field bearing many denticles with serrated margin on anteroventral surface; fourth segment subquadrate, with small field bearing denticles with serrated margin; terminal segment shortest with several denticles, ending in three projections (one is blunt and two are point- ed apically) ( Fig. 3K ). Accessory spines near ventral midline, each located slightly apart from first segment of second maxilla ( Fig. 2B ). Postmaxillary spines small, each located anterior to first segment of thorax ( Fig. 2B ).

First to fourth pairs of legs ( Fig. 4 ) biramous with sympods two-segmented, each composed of coxa and basis; rami each consisting of exopod and endopod; sympods and rami of first to fourth legs ventrally covered with small, simple cuticular scales; rami bearing two rows of plumose setae each near ventro- or dorsoposterior margin; first and second pairs of legs each possessing flagellum projecting from base of exopod. First leg ( Fig. 4A, B ) coxa bearing six plumose setae near ventroposterior margin; basis nearly half as wide as coxa, bearing four plumose setae near ventroposterior margin; exopod unsegmented, with 16 ventral plumose setae; endopod three-segmented, proximal segment long, with 12 ventral plumose setae and one short naked seta, middle segment much shorter than proximal segment, and terminal segment tapering distally, ending in two short spines; flagellum extending to proximal margin of coxa, with 17 plumose setae on ventroposterior margin. Second leg ( Fig. 4C, D ) coxa with two protrusions adorned with small, apically truncated spines on ventroposterior margin and posteriorly directed digitiform projection on dorsoposterior margin; basis slightly shorter than coxa, bearing four plumose setae near ventroposterior margin; exopod and endopod unsegmented, with two rows of plumose setae (15 and 17 ventral setae on exopod and endopod, respectively); flagellum extending to proximal margin of coxa, with 16 plumose setae on ventroposterior margin. Third leg ( Fig. 4E, F ) coxa with irregularly shaped, raised fields adorned with denticles on anterior and dorsal surface; basis slightly short- er than coxa, bearing raised disk-shaped field covered with denticles on anterior surface and three plumose setae near ventroposterior margin; large swelling (= socket) present on posterior margin of coxa and basis; exopod unsegmented, with 21 plumose setae near ventroposterior margin; endopod two-segmented, proximal segment with seven plumose setae near ventroposterior margin, terminal segment with nine plumose setae near ventroposterior margin. Fourth leg ( Fig. 4G, H ) coxa forming natatory lobe, bearing 15 plumose setae on posterior margin and two short naked setae near ventroposterior margin; basis with peg on anterior margin and six plumose setae on posterior distal margin; peg bearing pair of triangular-shaped processes on anterodistal surface and ending in three spines (one heavily ornamented with minute processes); exopod unsegmented, bearing 17 plumose setae near ventroposterior margin; endopod two-segmented, proximal segment with seven plumose setae near ventroposterior margin and short naked seta near posterodistal corner, and terminal segment with nine plumose setae near ventroposterior margin.

Color. When fresh, body almost transparent; compound eyes and naupliar eye dark brown; respiratory areas fringed by dark brown pigment; central portion of third segment of trunk black; black spots scattered on pale-yellow testes ( Fig. 5A ). In 70% ethanol (the specimen was fixed on 21 September 2021 and observed on 20 July 2022), body white; compound eyes and naupliar eye black; outline of respiratory areas recognized ventrally by dark brown pigment; black spots scattered on pale-yellow testes ( Fig. 5B, C ).

Host. Dark chub Nipponocypris temminckii ( Cypriniformes : Xenocyprididae ).

Attachment site. Dorsal body surface at the boundary between the head and trunk ( Fig. 1B ). The individual of A. coregoni was found to be oriented anteriorly.

Locality. The middle reaches of the Takase River (33°39′04″N, 135°25′14″E, 15 m elevation; Fig. 1B ), a tributary of the Tonda River, at Tsuzurafuchi in Shirahama, Wakayama Prefecture, central Japan .

Remarks. Argulus coregoni was originally described by Thorell (1864) based on specimens collected from three species of salmonids, i.e., European whitefish Coregonus lavaretus (Linnaeus, 1758) (reported as Coregono lavareto), grayling Thymallus thymallus (Linnaeus, 1758) (as Thymallo vulgari), and sea trout Salmo trutta Linnaeus, 1758 (as Salmone trutta ), in Sweden. This parasite has since been reported from European countries, including Sweden ( Thorell 1866), Norway ( Økland 1985; Bristow 1993; Dolven 2020), Finland (e.g., Pasternak et al. 2004; Mikheev et al. 2007, 2015; Bandilla et al. 2008; Hakalahti-Sirén et al. 2008), Russia ( Markevich 1937; Gusev 1987), Poland ( Penczak 1972), the Czech Republic and the Slovak Republic ( Romanovoský 1955; Moravec 2001), Germany ( Wagler 1935; Stammer 1959), France ( Roland 1963), and the U.K. ( Martin 1932; Gurney 1948; Rizvi 1969; Campbell 1971; Fryer 1982; Taylor et al. 2006). The species is also known to occur in East Asia, including the Russian Far East ( Markevich 1937; Dogiel and Akhmerov 1952; Smirnova 1971; Gusev 1987; Ermolenko and Kazachenko 1989; Ermolenko 1992, 2004a, b; Sokolov et al. 2012), China ( Wang 1958, 1964; Yin 1962; Chen 1973; Ding 1977; Song and Kuang 1980; Kuang and Qian 1991; Zang and Ma 1994; Yue et al. 1997; Wadeh et al. 2008), Malaysia ( Everts and Avenant-Oldewage 2009), and Japan (see below). Moreover, A. coregoni was reported from India ( Saha and Bandyopadhyay 2015; Khwaja and Tripathi 2022) and Pakistan ( Khan et al. 2017), South Asia, and from Iran ( Mousavi et al. 2011), West Asia, but since its morphology was not studied in detail, a reassessment of the identification of the species from these countries is necessary.

In Japan, A. coregoni has been described mainly from specimens taken from fishes in the two salmoniform families ( Salmonidae and Plecoglossidae ) ( Yamaguti 1937; Hoshina 1950). Yamaguti (1937) described a new species ( Argulus plecoglossi Yamaguti, 1937 ) from ayu Plecoglossus altivelis altivelis (Temminck and Schlegel, 1846) ( Plecoglossidae ), but it has been regarded as a junior synonym of A. coregoni ( Tokioka 1965; Shimura 1981: 347). In contrast to this, there is limited information on the morphology of A. coregoni from cypriniform fishes, and its specimens have only been collected from bitterlings ( Acheilognathidae ) ( Tokioka 1936; Nagasawa and Taniguchi 2021).

The morphological characters of the specimen collected from dark chub ( Xenocyprididae ) in this study corresponds to the descriptions of the male of A. coregoni from European countries ( Thorell 1864; Thiele 1904; Gurney 1948; Romanovoský 1955; Stammer 1959; Roland 1963; Penczak 1972; Fryer 1982), China ( Wang 1958; Chen 1973; Kuang and Qian 1991), Malaysia ( Everts and Avenant-Oldewage 2009), and Japan ( Tokioka 1936; Yamaguti 1937; Hoshina 1950), and the specimen is thus identified as A. coregoni . The male of this species is characterized by the presence of two protrusions adorned with small spines and a digitiform projection on the ventro- and dorsoposterior margins, respectively, of the coxa of the second leg ( Fig. 4C, D ) and the abdominal lobes have pointed posterior ends ( Figs 2 , 5 ). These characters were clearly recognizable in the original description of A. coregoni ( Thorell 1864: figs 2, 10, 15). Regarding the dorsal digitiform projection, Tokioka (1936: fig. 3) reported that it is “very long” and actually illustrated a long projection, which is similar to that of our specimen ( Fig. 4D ). The Chinese specimens have also a similar long dorsal projection ( Chen 1973: fig. 216; Kuang and Qian 1991: fig. 98D). Nevertheless, there are some variations in the second leg morphology between the specimens reported in other regions. In the European specimens, a well-developed dorsal projection was recognized by Thiele (1904: fig. 86), Romanovoský (1955: fig. 32) and Penczak (1972: fig. 13) but not by Fryer (1982: fig. 92). Roland (1963: fig. 6A, B) illustrated only two protrusions. The Malaysian specimens have a short dorsal projection and two ventral protrusions (reported as projections) of different sizes ( Everts and Avenant-Oldewage 2009: fig. 10).

Although only one male specimen of A. coregoni was collected in this study, there are several morphological differences between the sexes of the species. The male has accessory copulatory structures, i.e., two protrusions and a digitiform projection on the coxa of the second leg, a large swelling (= socket) on the coxa and basis of the third leg, and the peg on the basis of the fourth leg ( Fig. 4C–H ), all of which are not present in the female (Nagasawa 2021: fig. 2). In addition, black spots are found on the surface of the testes ( Figs 2 , 5 ; Thorell 1864: fig. 2; Hoshina 1950: fig. 1A; Romanovoský 1955: fig. 35; Roland 1963: fig. 2; Penczak 1972: fig. 2; Nagasawa and Kawai 2008: fig. 1).

The flagella are known to project each from the extreme proximal part of the exopod of both the first and second pairs of legs in branchiurans of the genus Argulus ( Boxshall and Jaume 2009) . In this study, we have confirmed that the flagella project at the base of the exopod of the first and second legs in A. coregoni ( Fig. 4A, C ). In Japan, such flagella have been reported from three other congeneric species, i.e., A. japonicus (Nagasawa 2021) , A. mongolianus Tokioka, 1939 (Nagasawa et al. 2022a), and A. nobilis Thiele, 1904 (Nagasawa 2023b).

In this study, we collected the specimen of A. coregoni from dark chub ( N. temminckii ) in a stream in Wakayama Prefecture, central Japan. Dark chub is distributed in central and western Japan and the southwestern region of the Korean Peninsula ( Hosoya 2015), but there is no record of A. coregoni from this fish species elsewhere in Japan or in Korea. Thus, dark chub is herein regarded as a new host of A. coregoni . There are five previous records of this parasite from Wakayama Prefecture, where it infects red-spotted masu salmon Oncorhynchus masou ishikawae Jordan and McGregor, 1925 [reported as Salmo (On.) masou macrostomus (Günther, 1877) ] in the Hiki River near the Takase River ( Takegami 1984) and also reared red-spotted masu salmon (reported as On. mas . ishikawai), rainbow trout On. mykiss (Walbaum, 1792) (reported as Salmo irideus Gibbons, 1855 ), and ayu Pl. a. altivelis (reported as Pl. altivelis ) ( Hoshina 1950; Nagasawa and Ohya 1996a, b; Kaji et al. 2011).

The specimen of A. coregoni was found attached on the dorsal body surface at the boundary between the head and trunk of the dark chub ( Fig. 1B ). A similar attachment site was also reported in the same species of parasite infecting oily bitterling Tan. limbata from the Asahi River, Okayama Prefecture ( Nagasawa and Taniguchi 2021: fig. 1). This may indicate that, in these cypriniform fishes, the anterior, dorsal body surface is commonly used by A. coregoni as its attachment site. Nonetheless, in salmonids inhabiting mountains streams in central Japan, this parasite is also found on the lateral body surface under and near the pectoral fins (Nagasawa et al. 2022b). This use of the pectoral fin area by A. coregoni may be associated with the hosts’ habitat. Because salmonids usually occur in fast-flowing streams, it has been inferred that this parasite uses such an area as a shelter to lessen the chance of being detached from the host (Shimura 1983a; Nagasawa et al. 2022b).

As stated above, the male of A. coregoni examined in this study has a posteriorly directed digitiform projection on the dorsoposterior margin of the coxa of the second leg ( Fig. 4C, D ). Despite its size variation, a similar projection has been recognized in the male of the species in Europe and East Asia, and it is regarded as the morphological feature that characterizes A. coregoni . In contrast, the male of A. japonicus is morphologically similar to A. coregoni but has no such digitiform projection ( Tokioka 1936: fig. 2; Yamaguti 1937: fig. 8; Chen 1973: fig. 194; Fryer 1982: fig. 94; Kuang and Qian 1991: fig. 100D). Thus, the presence or absence of the digitiform projection on the second leg can be used in identification of males of these congeneric species.

In addition, for identification of both sexes of A. coregoni and A. japonicus , the number of plumose setae on the posterior margin of the coxa of the first leg and the number of supporting rods in sucker membrane of the first maxilla are useful ( Nagasawa and Taniguchi 2021). Based on observations in Japan, the number of plumose setae ranges from four to nine in A. coregoni [four to seven in Yamaguti (1937); four to nine in Hoshina (1950); six in Nagasawa and Taniguchi (2021); six in this study], whereas it is constantly one in A. japonicus ( Yamaguti 1937; Nagasawa 2021). The number of supporting rods per first maxilla is usually 60 or more in A. coregoni [ca. 60 in Tokioka (1936); 60–70 in Yamaguti (1937); 54–73 in Hoshina (1950); 67 and 72 in Nagasawa and Taniguchi (2021); 60 in this study], but it ranges from 40 to 52 in A. japonicus [ca. 50 in Tokioka (1936); 40–50 in Yamaguti (1937); 50 and 52 in Nagasawa (2021)]. A similar difference in the number of supporting rods per first maxilla between the two species has been reported from China as well [64 and 71 ( Wang 1958) and 68 ( Chen 1973; Kuang and Qian 1991) in A. coregoni ; 50 ( Wang 1958) and 43–46 ( Chen 1973; Kuang and Qian 1991) in A. japonicu s]. The Malaysian specimens of A. coregoni have ca. 62 supporting rods ( Everts and Avenant-Oldewage 2009).

There is a paper on argulid branchiuran identified as “ A. japonicus ” from Malaysia ( Seng 1986), but its leg structure does not correspond to that of A. japonicus . The Malaysian specimens had seven setae on the posterior margin of the coxa of the first leg and three protrusions (reported as knobs, two are ventral but one is dorsal) on the posterior margin of the coxa of the second leg ( Seng 1986: figs 18, 20). As stated above, these characters are identical to the leg morphology of A. coregoni . When Everts and Avenant-Oldewage (2009) later reported A. coregoni as a new country record from Malaysia, they did not mention that the species had been misidentified before. Seng (1986) suggests that A. coregoni (reported as A. japonicus ) has been widely spread in Malaysia.

Figures

Fig. 1. Argulus coregoni and its collection site. A, Middle reaches of the Takase River where dark chub were collected; B, a dark chub (ca. 70mm total length) infected with an adult male of A. coregoni (arrowhead) on the dorsal body surface at the boundary between the head and trunk. Scale bar: 5mm.

Fig. 2. Argulus coregoni, adult male, NSMT-Cr 31596.A, Habitus, dorsal view; B, habitus, ventral view.Scale bar: 1mm.

Fig. 3. Argulus coregoni, adult male, NSMT-Cr 31596. A, Respiratory areas, ventral view; B, caudal rami, ventral view; C, first antenna (a1), second antenna (a2), and postantennal spine (pas), ventral view; D, third and apical segments of first antenna, ventral view; E, second, third, fourth, and apical segments of second antenna, ventral view; F, preoral sheath and stylet, ventral view; G, mouth tube, ventral view; H, three anterior supporting rods and marginal projections from rim of first maxilla sucker, ventral view; I, second maxilla and denticle (enlarged) on second segment, ventral view; J, raised field on first segment of second maxilla, ventral view; K, third, fourth, and terminal segments of second maxilla, ventral view. Scale bars:A, 0.2mm; B, E–G, J, K, 0.05mm; C, I, 0.1mm; D, H, 0.03mm.

Fig. 4. Argulus coregoni, adult male, NSMT-Cr 31596. A, First leg, ventral view; B, distal part of endopod of first leg, ventral view; C, second leg, ventral view; D, coxa of second leg, ventral view; E, third leg, ventral view; F, coxa, base, and part of exopod of third leg, dorsal view; G, fourth leg, ventral view, H, base (with peg) and part of endopod of fourth leg, anteroventral view. Scale bars: A, C, E, G, 0.3mm; B, D, F, H, 0.1mm.

Fig. 5. Argulus coregoni, adult male, NSMT-Cr 31596. A, Habitus, fresh specimen, dorsal view; B, C, habitus, ethanol-preserved specimen, dorsal and ventral views, respectively. The specimen was fixed in 70% ethanol on 21 September 2021 and photographed on 20 July 2022. Scale bars: 1mm.