Argulus nobilis Thiele, 1904

Nagasawa, Kazuya, 2023, First Japanese Record of Argulus nobilis (Crustacea: Branchiura: Argulidae), an Ectoparasite of Gars of North American Origin, Species Diversity 28 (2), pp. 205-215 : 206-212

Argulus nobilis Thiele, 1904

[New Japanese name: Odeko-chou] ( Figs 1–5 )

Argulus nobilis Thiele, 1904: 28–32 , pl. 7, figs 64–66, pl. 8, figs 67–76; Wilson 1916: 354; Wilson 1924: 2–4, pl. 1, figs 6–9; Meehean 1940: 515–517, fig. 45; Causey 1960: 74, 75, figs 3–5, 8, 9; Yamaguti 1963: 326, pl. 324, fig. 1; Hoffman 1967: 303; Cressey 1972: 4, 10, figs 1B, 5I; Hoffman 1977: 3; Abele et al. 1989: 685–687; Hoffman 1999: 316; Neethling and Avenant-Oldewage 2016: 1254, 1290, 1297.

Argulus ingens C. B. Wilson, 1912: 253–255 , pl. 30, figs 1–6, pl. 31, fig. 7; Wilson 1916: 354; Yamaguti 1963: 324, pl. 318, fig. 2; Hoffman 1967: 302; Hoffman 1999: 316; Neethling and Avenant-Oldewage 2016: 1254, 1277, 1297.

Argulus nobilis var. nobilis : Wilson 1924: 2; Yamaguti 1963: 326.

Argulus nobilis var. ingens : Wilson, 1924: 2; Meehean 1940: 515; Yamaguti 1963: 326.

Material examined. Five adult females: LBM1430006167 for one specimen [10.2 mm in total length (TL, from anterior tip of carapace to posterior tip of abdomen)]; LBM1430006168 for three specimens (9.2, 9.9, and 10.5 mm in TL) and one dissected specimen (10.1 mm in TL) .

Adult female (based on five specimens, including one dissected specimen). Body dorsoventrally flattened, measuring 9.2–10.5 (mean = 9.9, n = 5) mm in TL and 6.0–7.0 (mean = 6.4, n = 5) mm in maximum body width (around midlength of carapace).

Carapace (including posterolateral lobes) nearly circular, covering almost totally first pair of legs and partially second and third pairs of legs in dorsal view, 6.6–8.5 (mean = 7.4, n = 5) mm long, comprising 65.3–81.5% (mean = 74.5%, n = 5) of total length ( Figs 1 , 5 ). Frontal region of carapace delimited by pronounced anterolateral indentations and protruding anteriorly; anterior margin rounded ( Fig. 2A ). Central longitudinal ribs distinct, curved laterally near compound eyes; transverse ribs evident behind nauplius eye ( Fig. 1A ). Compound eyes well visible, dorsally located at level of anterolateral indentations of carapace ( Figs 1A , 2A , 5 ). Nauplius eye located posterior to compound eyes on 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. 2A ). Posterolateral lobes of carapace not overlapping, ending in rounded margin, separated by sinus 34.1–45.4% (mean = 40.6%, n = 5) length of carapace ( Figs 1A , 5A ). Respiratory areas located at level between second maxillae and second pairs of legs; smaller anterior area nearly oval, located mesially in big anterior notch of posterior area; larger posterior area composed of three portions, i.e., slightly expanded anterior portion, narrow neck-like portion, and large, nearly inverted triangular portion with small notch on anterior margin ( Figs 1B , 2B ). Thorax with four segments, bearing small spiniform projections laterally; fourth segment tapering posteriorly ( Figs 1 , 2B ). Abdomen heart-shaped, with some small spiniform projections on ventral surface; anal indentation 27.6–38.5% (mean = 32.0%, n = 5) as long as abdomen to form two lobes; each lobe becoming wider toward one-quarter length of abdomen, then tapering posteriorly, ending in pointed margin ( Figs 1 , 2B , 5 ). Paired spermathecae each round, located in anterocentral portion of abdomen ( Fig. 1A ); paired spermathecal spines each torpedo-shaped and tapering posteriorly, located on ventral midline between natatory lobes ( Figs 1B , 2B, D , 5B ). Caudal rami located at one-third length of anal indentation, each with five naked setae on posterior margin ( Figs 1 , 2B, E ).

First antennae with four segments ( Fig. 3A, B ): first segment heavily sclerotized in mesial and posterior regions, with large blunt projection on posterior margin; second segment largest and heavily sclerotized, with strong posteroventrally directed hook on anterior margin, strong lateroventrally directed hook at distal corner, and ventral projection near posterior margin; third segment cylindrical and unarmed; apical segment shorter than third segment, with four naked setae at tip. Second antennae with five segments ( Fig. 3A, C, D ): first segment sclerotized, with sharp, strong posteroventral spine and apically rounded protrusion bearing six naked setae on posterior margin; second segment shorter than first segment, with small protrusion bearing four naked setae on posterior margin; third, fourth, and apical segments nearly cylindrical and decreasing in length; third segment with four and four naked setae on lateral and distal margins, respectively; fourth segment with two and four naked setae on lateral and distal margins, respectively; apical segment with two short and three naked setae near and at tip, respectively. Postantennal spines large and robust, each located lateral to spine of first segment of second antenna ( Figs 2A , 3A ). Preoral sheath cylindrical and visible on ventral midline of carapace near anterior region of first maxillae ( Figs 1B , 2A , 3E ); anterior portion of stylet protruding from opening of preoral sheath. Mouth tube without ornamentation located just posterior to preoral sheath, longer than wide; posterior portion composed of anterior labrum and posterior labium ( Figs 1B , 3F ).

First maxillae forming well developed cup-like suckers ( Fig. 1B ), with 59–65 (mean = 62, n = 4) supporting rods in sucker membrane. Supporting rods each composed of 10–12 sclerites [in 30 supporting rods examined, 11 sclerites per rod is the commonest (n = 24, 80.0%), followed by 10 (n = 4, 13.3%) and 12 (n = 2, 6.7%) sclerites, respectively]; sclerites oblong and decreasing in size distally ( Fig. 3G ). Outer margin of rim of sucker membrane with numerous apically pointed projections. Second maxillae with five segments ( Fig. 3H ): first segment robust, with three, almost equally long spines on posterior margin; corpus of first segment with larger papilla bearing five long naked setae, smaller papilla bearing one long and one short naked setae, three short naked setae near outer margin, and several minute denticles; second segment longer than first segment, with distally directed unidentate, bidentate, or tridentate spinules and one long naked seta on ventral surface; third segment shorter and narrower than second segment, with distally directed unidentate, bidentate, or tridentate spinules on ventral surface and short naked setae on posterior margin; fourth segment subquadrate, with two short naked setae on ventral surface and some longer naked setae on ventral surface; terminal segment bearing several setae on posterior marine, ending in three projections (central one stout, lateral ones short). Accessory spines near ventral midline, each located slightly apart from first segment of second maxilla ( Figs 1B , 3H ). Postmaxillary spines small, located on anterior portion of first segment of thorax ( Fig. 1B ).

First to fourth pairs of legs ( Fig. 4 ) biramous, with sympods each composed of coxa and basis; sympods and rami of first to fourth legs ventrally covered with small spiniform projections; rami each issuing two rows of plumose setae; first and second pairs of legs each possessing flagellum projecting from extreme proximal part of exopod. First leg ( Fig. 4A, B ) coxa bearing 15 long plumose setae and one short plumose seta on posterior margin; basis nearly half as wide as coxa, bearing seven plumose setae on posterior margin; exopod unsegmented, with 23 and 20 plumose setae near anterior and posterior margins, respectively; endopod three-segmented, proximal segment long, with 16 and 19 plumose setae near anterior and posterior margins, respectively, and one naked seta in ventrodistal portion, middle segment much shorter than proximal segment, with one short naked seta at posterodistal corner, and terminal segment tapering distally, ending in two short spines; flagellum extending to proximal margin of coxa, with 21 and 13 plumose setae on anterior and posterior margins, respectively. Second leg ( Fig. 4C ) coxa with seven plumose setae on posterior margin; basis slightly shorter than coxa, bearing seven plumose setae on posterior margin; exopod and endopod unsegmented, with two rows of plumose setae near anterior and posterior margins (24 and 21 setae on exopod and 20 and 19 setae on endopod); flagellum extending to proximal margin of coxa, with 23 and 14 plumose setae on anterior and posterior margins, respectively. Third leg ( Fig. 4D ) coxa with six plumose setae on posterior margin; basis slightly shorter than coxa, bearing six plumose setae on posterior margin; exopod unsegmented, with 23 and 25 plumose setae on dorsolateral and ventrolateral sides, respectively; endopod two-segmented, proximal segment with a small process at anterodistal corner, 12 and six plumose setae near dorso- and ventroposterior margins, respectively, terminal segment with 12 and 12 plumose setae near dorso- and ventroposterior margins, respectively. Fourth leg ( Fig. 4E ) coxa forming natatory lobe bearing 11 plumose setae and a group of short spines on proximal, rounded posterior margin, 39 plumose setae on weakly curved, posterior margin, and four plumose setae on anterodistal margin; basis slightly shorter than main portion of natatory lobe, with six plumose setae on posterodistal margin; exopod unsegmented, bearing 19 and 19 plumose setae on dorsolateral and ventrolateral sides, respectively; endopod two-segmented, proximal segment with a small process at anterodistal corner, one naked short seta and 13 plumose setae near dorsoposterior margin and eight plumose setae near ventroposterior margin, and terminal segment with one naked short seta and 12 plumose setae near dorsoposterior margin and 12 plumose setae near ventroposterior margin.

Color (based on ethanol-preserved specimens). Carapace and abdomen brownish white; legs white; thorax pale brown with irregularly shaped, dark brown spots scattered on dorsal surface; respiratory areas weakly fringed by dark brown pigment ( Fig. 5 ).

Hosts. Shortnose gar, Lepisosteus platostomus , and an unidentified lepisosteid fish (recorded as “garpike” on the label of the specimen, LBM1430006167).

Attachment site. No record on the labels.

Localities. In Japan. No record on the labels, but they were most probably collected in Shiga Prefecture, where Lake Biwa Museum is located, or its adjacent region.

Japanese name. The new Japanese name for A. nobilis is formed as a compound of “odeko” (meaning “bulging forehead”), referring to the protruding frontal region of the carapace and “chou” (meaning “freshwater branchiuran”).

Remarks. The morphology of the female argulid examined in this study is identical to the original and subsequent descriptions of female A. nobilis given by Thiele (1904), Wilson (1912, 1924), and Meehean (1940), and the specimens are thus identified as A. nobilis . This species is characterized by the anterior protrusion of the frontal region of the carapace ( Figs 1 , 2A , 5 ), a heart-shaped abdomen ( Figs 1 , 2B , 5 ), the transverse ribs of the carapace ( Figs 1A , 5A ), the boot-shaped natatory lobes of the fourth pairs of legs ( Figs 1B , 2B , 4E , 5B ), the peculiar nested shape of the respiratory areas ( Fig. 2C ), the presence of 10 and more sclerites per supporting rod of the first maxillae ( Fig. 3G ), the small processes at each anterodistal corner of the proximal segment of the endopod of the third and fourth legs ( Fig. 4D, E ), the prominent torpedo-shaped spermathecal spines ( Fig. 2B, D ), and the papillae bearing naked setae of different lengths on the corpus of the first segment of the second maxillae ( Fig. 3H ). Although Cressey (1972) stated that only setae exist on this corpus, Meehean (1940) recognized both a small rounded papilla and long setae on it. In the present study, very tiny denticles were also found on the corpus ( Fig. 3H ). Moreover, the unusual shape of the respiratory areas was reported by Wilson (1912: pl. 30, fig. 5), Meehe- an (1940: fig. 45a), and Cressey (1972: fig. 1B). According to Cressey (1972), more than 10 sclerites are found in each supporting rod of the first maxillae: their number was reported to be ca. 13 ( Thiele 1904) and 12–14 ( Meehean 1940) and, in this study, ranges from 10–12 (mostly 11). The presence of a small process at the anterodistal end of the proximal segment of the endopod of the third and fourth legs was first noticed by Wilson (1924) and later confirmed by Meehean (1940: fig. 45c). The well-developed spermathecal spines were figured by Thiele (1904: pl. 8, fig. 76) and reported as “tactile papillae” by Wilson (1912). The presence of the transverse ribs of the carapace was previously noted by Wilson (1924). In this study, I could not observe the mandibles because I lost them during my dissection of the mouth tube. In the original description of A. nobilis, Thiele (1904) found six teeth each on the mesial margins of the mandibles. No subsequent observations have been reported on the mandibles or their number of teeth.

There are several minor differences in the morphology of A. nobilis between the previous and present descriptions. It has been reported that two distal spines on the first segment of the second maxilla are close together and slightly separat- ed from the remaining one ( Thiele 1904: pl. 8, fig. 68; Wilson 1912, 1924). In the present study, a similar arrangement is found in two of the five specimens examined, whereas in the other three specimens the three spines are almost equally separated ( Fig. 3H ). The ventral surface of the third segment of the second maxilla was figured to have a swelling or a lamellar process ( Thiele 1904: pl. 8, fig. 69; Wilson 1912: pl. 30, fig. 3; Meehean 1940), but no such structure was observed in the specimens examined in this study ( Fig. 3H ). The size of the notch on the anterior or mesial margin of the main portion of the posterior respiratory area appears variable: it was figured to be larger ( Wilson 1912: pl. 30, fig. 5; Meehean 1940: fig. 45a) than observed in this study ( Fig. 2C ), whereas Cressey (1972: fig. 1B) recognized almost no notch on that mesial margin. Furthermore, the number of setae on each caudal ramus was previously reported to be “three” ( Wilson 1912), but the specimen dissected in this study has five setae ( Fig. 2E ).

Although only female specimens of A. nobilis were examined in this study, several morphological differences are known between both sexes of the species. The male has a more anteriorly protruding frontal region of the carapace and longer posterolateral lobes overlapping the anterior region of the abdomen than the female ( Wilson 1912: pl. 30, fig. 1, pl. 31, fig. 7) and the abdomen of the male has its anterior corners forming narrow knobs or processes ( Thiele 1904: pl. 7, fig. 65). The male also has accessory copulatory structures, i.e., a finger-like flap and the socket on the coxa and basis of the third pair of legs, respectively; and the peg on the basis of the fourth pair of legs ( Thiele 1904: pl. 8, figs 71, 79; Wilson 1912: pl. 30, fig. 4; Meehean 1940: fig. 45c).

In some branchiurans of the genus Argulus , the flagella are known to project each from the extreme proximal part of the exopod of both the first and second pairs of legs ( Boxshall and Jaume 2009), and two species from Japan, A. japonicus Thiele, 1900 and A. mongolianus Tokioka, 1936 , have been reported to have such flagella (Nagasawa 2021; Nagasawa et al. 2022a). Their presence is confirmed in A. nobilis in this study ( Fig. 4A, C ).

Morphologically, especially in the habitus and the outline of the respiratory areas, A. nobilis resembles three congeneric species ( A. lepidostei ; A. meehani Cressey, 1971 ; and A. mexicanus Pineda, Páramo, and Del Río, 1995 ), all of which are parasites of gars. However, A. nobilis can be separated from these three species by having 10 or more sclerites per supporting rod of the first maxilla: 10–14 in A. nobilis ( Thiele 1904; Meehean 1940; Cressey, 1972; this paper) vs. 7 ( Wilson 1916: pl. 62, fig. 18) and 8 or 9 in A. lepidostei ( Meehean 1940) , less than 10 in A. meehani ( Cressey 1971, 1972), and 7–9 (usually 8) in A. mexicanus ( Pineda et al. 1995) . The position of the respiratory areas on the carapace also differs between A. nobilis and A. lepidostei : these areas are located nearly at midlength of the posterolateral lobes in A. nobilis ( Fig. 1A ), whereas they are close to the posterior end of the lobes in A. lepidostei ( Wilson 1916) . Also a patch of readily visible denticles (reported as scales) is found on the corpus of the first segment of the second maxillae in A. lepidostei ( Cressey 1972: fig. 6B), such denticles are not present in A. nobilis ( Fig. 3H ).

Argulus nobilis is known as one of the largest species in this genus ( Wilson 1912). Females reach 18 mm ( Thiele 1904), 21.5–25 mm ( Wilson 1912), and up to 25 mm ( Meehean 1940) in total length. While the five females examined herein are considerably smaller (9.2–10.5 mm) than those previously reported, four of them possess eggs in the ovary ( Figs 1B , 5B ). Males are smaller than females, reaching 16 mm in total length ( Wilson 1912; Meehean 1940). Wilson (1924) collected “young” female and male (ca. 4 mm long) of the species.

The hosts of A. nobilis reported in this paper are shortnose gar ( L. platostomus ) and an unidentified gar. In the U.S.A., three species of gars, i.e., alligator gar ( At. spatula ), longnose gar ( L. osseus ), and spotted gar ( L. oculatus ), are known as the hosts of A. nobilis (see the Introduction for the literature). The shortnose gar represents a new host record for A. nobilis .

The specimens of A. nobilis examined in this study were collected in 1992. It is unknown whether those specimens were taken from gars soon after being imported from abroad or those that had been held in Japan because gars had been imported alive from North America to Japan prior to 2018.

In this study, no information was available on the attachment site of the specimens of A. nobilis . However, as its congeneric species are usually found on the body surface of their host fishes, A. nobilis is very likely to be a skin parasite, although there is a record of the species from the mouth of alligator gar ( Wilson 1912).

Now, six species of Argulus ( A. japonicus ; A. coregoni Thorell, 1864 ; A. americanus Wilson, 1902 ; A. mongolianus ; A. lepidostei or a related species; and A. nobilis ) are known to parasitize freshwater fishes in Japan ( Nagasawa 2009, 2011; Nagasawa et al. 2022a; this paper). The first two species are native to Japan, whereas the other four species were introduced from other countries. Both A. japonicus and A. coregoni are found on both wild and farmed fishes across a wide area of Japan: A. japonicus usually infects cyprinids (e.g., Nakazawa 1914; Tokioka 1936; Yamaguti 1937; Takeda et al. 2000; Nagasawa 2017; Nagasawa et al. 2018a, 2021, 2023) but, due to its low host specificity, also occurs on fishes of other families, such as silurids and centrarchids ( Nagasawa et al. 2010; Yamauchi et al. 2011; Nagasawa 2021), and A. coregoni parasitizes mainly salmonids and ayu, P. a. altivelis (e.g., Yamaguti 1937; Hoshina 1950; Shimura 1983; Nagasawa et al. 2018b, 2022b; Nagasawa and Yuasa 2020) but is also found on cyprinids, odontobutids, and amblycipitids ( Tokioka 1936; Nagasawa et al. 2014; Nagasawa and Ishikawa 2015; Nagasawa and Taniguchi 2021). Argulus americanus was found at a public aquarium in Tokyo, where it occurred on bowfin, Amia calva Linnaeus, 1766 , imported from North America and its hatched larvae experimentally infected Mozambique tilapia, Oreochromis mossambicus (Peters, 1852) (reported as Tilapia mossambica ) ( Shimura and Asai 1984). Argulus mongolianus is most probably of Chinese origin and was recently discovered in two lakes in northern Honshu, Japan, where it was found to parasitize four species of freshwater fishes: largemouth bass, Micropterus salmoides (Lacepède, 1802) ; common carp, Cyprinus carpio Linnaeus, 1758 ; Japanese white crucian carp, Carassius cuvieri Temminck and Schlegel, 1846 ; and silver crucian carp, Carassius sp. ( Nagasawa et al. 2022a).

Figures

Fig. 1. Argulus nobilis, adult female, LBM1430006168. A, Habitus, dorsal view; B, habitus, ventral view. Part of the ventral surface of the thorax was damaged and eggs were seen (Fig. 1B). Scale bar: 3mm.

Fig. 2. Argulus nobilis, adult female, LBM1430006168. A, Frontal region of carapace, ventral view; B, posterior region of body, ventral view; C, respiratory areas, ventral view; D, spermathecal spines, ventral view; E, caudal ramus, ventral view. Scale bars: A, B, 0.5mm; C, 1mm; D, 0.2mm; E, 0.1mm.

Fig. 3. Argulus nobilis, adult female, LBM1430006168. A, First antenna (a1), second antenna (a2), and postantennal spine (pas), ventral view; B, third and apical segments of first antenna, ventral view; C, third, fourth, and apical segments of second antenna, ventral view; D, swelling bearing six naked setae on posterior margin of first segment of second antenna, ventral view; E, preoral sheath and stylet, ventral view; F, mouth tube, ventral view; G, two anterior supporting rods and marginal projections from rim of first maxilla sucker, ventral view; H, second maxilla and spinules (circled) on second and third segments, ventral view. Scale bars: A, F, H, 0.2mm; B–E, G, 0.1mm.

Fig. 4. Argulus nobilis, adult female, LBM1430006168. A, First leg, dorsal view; B, distal part of endopod of first leg, dorsal view; C, second leg, dorsal view; D, third leg, dorsal view; E, fourth leg, dorsal view. Ventral rows of plumose setae on rami of third and fourth legs not shown (D, E). Scale bars: A, C–E, 0.5mm; B, 0.1mm.

Fig. 5. Argulus nobilis, adult female, LBM1430006168, ethanol-preserved specimen. A, Habitus, dorsal view; B, habitus, ventral view. This specimen was collected on 17 July 1992 and photographed on 2 October 2022. Scale bar: 3mm.