Ligictaluridus pricei ( Mueller, 1936 )

Nitta, Masato & Nagasawa, Kazuya, 2015, An Alien Monogenean, Ligictaluridus pricei (Platyhelminthes: Ancyrocephalidae), Parasitic on the Channel Catfish Ictalurus punctatus (Actinopterygii: Siluriformes: Ictaluridae) in Japan, Species Diversity 20, pp. 95-102 : 95-98

Ligictaluridus pricei ( Mueller, 1936)

( Fig. 2 )

Cleidodiscus pricei Mueller, 1936: 459 , 461, 464, figs 11–15; Mueller 1937: 214; Seamster 1938a: 14; Seamster 1938b: 605, 608, 610–611, figs 1–7; Summers and Bennett 1938: 248; Mizelle and Cronin 1943: 206–207, 219, 221, pl. 1: figs 65–74; Mizelle and Donahue 1944: 608–609; Mizelle and Regensberger 1945: 680–681, 697, pl. 1: figs 51–55; Sproston 1946: 233; Seamster 1948: 168; Hargis 1952: 112; Hargis 1953: 95; Mizelle and Klucka 1953: 722–723; Mizelle and Webb 1953: 208; Krueger 1954: 278; Mizelle et al. 1961: 634; Allison 1963: 347; Yamaguti 1963: 63, fig. 771; Žitňan 1965: 38–39, fig. 4; Hoffman 1967: 89; Lawrence and Murphy 1967: 168; Nowlin et al. 1967: 110; Molnár 1968: 301; Allison and Rogers 1970: 22, 23; Clayton and Schlueter 1970: 161; Torres and Price 1971: 132; Dechtiar 1972b: 278; Hanek and Fernando 1972a: 1307; Hanek and Fernando 1972b: 1316; Meade and Bedinger 1972: 283, 286, fig. 15; Miller et al. 1973: 200, 204; Prost 1973: 317–318, fig. 2; Cloutman 1974: 226, 227; Molnar et al. 1974: 721; Rawson and Fox 1974: 620; Hensley and Nahhas 1975: 204; Baker and Crites 1976: 38; Bauer and Hoffman 1976: 165; Musselius et al. 1976: 17; Kiškaroly 1977: 202–203, fig. 7; Lambert 1977: 186, 206, 212, fig. 37; Cloutman 1978: 171–172; Riley 1978: 210; Lubinsky and Loch 1979: 2, 22; Sutherland and Holloway 1979: 130; Cone 1980: 179; Duobinis-Gray and Corkum 1985: 134; Gussev 1985: 198, 204–205, fig. 309; Hoffman 1985: 36–38, fig. 27; Musselius 1988: 147; Mirzoyeva 1988: 160–161; Bunkley-Williams and Williams 1994: 33–34, 130, fig. Cleidodiscus pricei ; Šimková et al. 2003: 5, 7, 8; Šimková et al. 2004: 1007; Plaisance et al. 2005: 427; Pouyand et al. 2006: 245; Zhang 2012: 47, 106.

Ancyrocephalus pricei Roman-Chiriac 1960: 88–89 , fig. 59; Adamczyk 1973: 359–361, fig. 12.

Ligictaluridus pricei Beverley-Burton 1984: 38 , 40, fig. 10.2; Klassen and Beverley-Burton 1985a: 717–720, figs 2–13, table 1; Klassen and Beverley-Burton 1987: 86, fig 2; Klassen and Beverley-Burton 1988: 49; Nepszy 1988: 5, 11, 24, 37, 54, 58, 70, 80, 81; Hoffman 1999: 109, 116, fig. 170; Rosas-Valdez and Pérez-Ponce de León 2005: 222, 224; Castro 2010: 15; Pérez-Ponce de León et al. 2010: 30; Muzzall and Whelan 2011: 83, 117, 184, 249, 250, 289, 331, 406, 407, 460, 505; Truong 2011: 38, 64–73, 126, 153, 158, 159, 163, pls 9–11; Zhang 2012: 106; Salgado-Maldonado and Quiroz-Martínez 2013: 5, 10, 12, 16; Wang et al. 2013: 87–89, fig. 1.

Material examined. In total, 28 specimens (NSMT-Pl 6166) were used for the description. Soft anatomy was observed in seven specimens stained in Heidenhain’s iron hematoxylin, and sclerotized structures were measured in 21 specimens fixed in ammonium picrate glycerin.

Description. Body ( Fig. 2A ) elongate, length 695±91.9 (554–833; n =13) including haptor, width at mid-body 127±13.5 (105–155; n =13). Cephalic glands opening on anterolateral sides of head. Two pairs of eyes. Pharynx round, diameter 34±4.9 (26–45; n =13); esophagus present; part of intestinal caeca extending to end of body and rejoining there to form elongate loop. Testis pyriform, posterodorsal to ovary. Vas deferens arising from anterior margin of testis, looping dorsoventrally around left intestinal caecum. Seminal vesicle located posterior to two saccate prostatic reservoirs. Penis ( Fig. 2M, N ) a slender, curved tube, length 35±2.9 (29–41; n =21), diameter 2±0.3 (2–3; n =21), diameter to length ratio 1: 13–19. Accessory piece ( Fig. 2M, N ) 33±2.3 (29–38; n =21) in length, touching base of penis (i.e., concave portion near base of accessory piece fitting base of penis) and extending to tip of penis, twisted one time near tip and also at midlength, usually straight in overall shape ( Fig. 2M ), but in a few specimens bent in middle ( Fig. 2N ). Ovary in mid-body, ovoid. Oviduct arising from anterior side of ovary, continuing as oötype and uterus. Mehlis’ gland connecting lowest part of oötype. Vagina exiting from left side of oviduct, running between vas deferens and left intestinal caecum to vaginal opening on left side of ventral body surface. Vitellaria approximately co-extensive with intestinal caeca.

Haptor length 79±13.0 (60–100; n =13), width 107±12.7 (89–129; n =13). Each hamulus lacking deep root. Dorsal hamuli ( Fig. 2B ) smaller than ventral hamuli, total length 45±3.0 (40–49; n =21), length to notch 43±2.2 (39–48; n =21), superficial root length 13±1.5 (10–16; n =21), blade length 18±1.1 (15–20; n =21). Ventral hamuli ( Fig. 2C ) with total length 51±2.4 (46–55; n =21), length to notch 47±1.9 (44–50; n =21), superficial root length 15±1.6 (12–18; n =21), blade length 18±1.6 (15–21; n =21). Dorsal bar ( Fig. 2D ) with lamella-like flange at midsection, length 49±3.0 (42–54; n =21), median width 10±1.7 (7– 13; n =21). Ventral bar ( Fig. 2E ) V-shaped, length 45±2.4 (41–50; n =21), median width 7±1.2 (6–11; n =21). Marginal hooks of larval type, 7 pairs; hook pair I, hook pair II, and hook pairs III–VII located at center, tip, and each side of haptor, respectively ( Fig. 2A ); in length, pair I ( Fig. 2E ) 14±0.8 (13–16; n =16); pair II ( Fig. 2F ) 12±0.8 (11–13; n =16), smallest; pair III ( Fig. 2G ) 15±0.8 (14–17; n =16); pair IV ( Fig. 2H ) 15±0.7 (14–16; n =16); pair V ( Fig. 2I ) 15±0.6 (14–16; n =16), pair VI ( Fig. 2J ) 15±0.4 (14–16; n =16); pair VII ( Fig. 2K ) 15±0.4 (15–16; n =16) .

Host. Channel catfish Ictalurus punctatus ( Siluriformes : Ictaluridae ).

Locality. Lake Kasumigaura, Tsuchiura city, Ibaraki Prefecture, Japan.

Site of infection. Gills.

Remarks. This monogenean was originally described by Mueller (1936) as Cleidodiscus pricei from Ictalurus punctatus , Ameiurus nebulosus (Lesueur, 1819) (as I. meiurus nebulosus ), and A. natalis (Lesueur, 1819) (as I. natalis ) ( Siluriformes : Ictaluridae ) in Florida, U.S.A. It was transferred to the genus Ligictaluridus by Beverley-Burton (1984). The specimens examined in this study approximately conform to the descriptions of L. pricei by Mueller (1936), Mizelle and Cronin (1943), Mizelle and Regensberger (1945), Prost (1973), Kiškaroly (1977), Žitňan (1965), Gussev (1985), Klassen and Beverley-Burton (1985a, b), Truong (2011), and Wang et al. (2013). The sclerotized structures of L. pricei are known to show marked variation in morphology and measurements ( Seamster 1938b, Mizelle and Cronin 1943, Mizelle and Donahue 1944, Mizelle and Regensberg- er 1945), but Mizelle and Donahue (1944) suggested that such variation is caused by differences in fixation method. On the other hand, the length of the accessory piece reported by Hargis (1953) is quite short: 10–18 µm. He presented no drawings of the accessory piece, but since it is sometimes bent (cf. Prost 1973: fig. 2f, this study: fig. 2N), Hargis (1953) probably measured a bent one. Until now, the vagina has not been described clearly, because it is obscured by well-developed vitellaria ( Klassen and Beverley-Burton 1985a). Based on the specimens stained in Heidenhain’s iron hematoxylin, the present study has revealed that it runs between the vas deferens and the left intestinal caecum ( Fig. 2A ).

At present, the genus Ligictaluridus consists of six valid species ( Klassen and Beverley-Burton 1985a, b): L. bychowskyi ( Price and Mura, 1969) , L. floridanus ( Mueller, 1936) , L. mirabilis ( Mueller, 1937) , L. monticellii (Cognetti de Martiis, 1924) , L. posthon Klassen, Beverley-Burton and Dechtiar, 1985 , and L. pricei . Ligictaluridus pricei is readily separated from L. monticellii by the presence of a deep root ( Klassen and Beverley-Burton 1985a) on each hamulus. The distal limb of the accessory piece has a single terminal projection in L. pricei , while those of L. floridanus and L. mirabilis have two and four terminal projections, respectively ( Mueller 1936, 1937; Klassen and Beverley-Burton 1985a). Unlike L. pricei , L. bychowskyi has a tapered penis ( Price and Mura 1969; Klassen and Beverley-Burton 1985a). Ligictaluridus pricei and L. posthon are separated from each other by the diameter to length ratio of the penis: 1: 18 ( Klassen and Beverley-Burton 1985b) or 1: 13–19 (this study) for L. pricei versus 1: 6 ( Klassen and Beverley-Burton 1985b) for L. posthon .

Roman-Chiriac (1960) reported a monogenean as Ancyrocephalus pricei (Mueller, 1934) Mizelle and Cronin, 1943 , an attribution later repeated by Adamczyk (1973). Howev- er, Mueller (1934a, b) did not describe the species, nor did Mizelle and Cronin (1943) transfer it to Ancyrocephalus . Rather, Mueller (1936) described it, and it has recently been placed in Ligictaluridus (Beverley-Burton 1984) . Specimens reported by Dechtiar (1972a) as Cleidodiscus pricei from stonecat Noturus flavus Rafinesque, 1818 ( Siluriformes : Ictaluridae ) were regarded as Ligictaluridus posthon by Klassen and Beverley-Burton (1985b).

Figures

Fig. 2. Ligictaluridus pricei (Mueller, 1936). NSMT-Pl 6166. A, Whole mount (ventral view); B, dorsal hamuli; C, ventral hamuli; D, dorsal bar; E, ventral bar; F, marginal hook of pair I; G, marginal hook of pair II; H, marginal hook of pair III; I, marginal hook of pair IV; J, marginal hook of pair V; K, marginal hook of pair VI; L, marginal hook of pair VII; M and N, penes and accessory pieces from two specimens. Scale bars: A, 50µm; B–N, 10µm. Abbreviations: ap, accessory piece; cgo, opening of cephalic gland; e, eye; i, marginal hook of pair I; ii, marginal hook of pair II; iii, marginal hook of pair III; in, intestinal caeca; iv, marginal hook of pair IV; mg, Mehlis’ gland; o, oötype; od, oviduct; ov, ovary; p, penis; ph, pharynx; pr, prostatic reservoir; sv, seminal vesicle; t, testis; u, uterus; v, marginal hook of pair V; vi, marginal hook of pair VI; vii, marginal hook of pair VII; vl, vitellaria; va, vagina; vp, vaginal pore; vd, vas deferens.