Unilatus brittani Mizelle, Kritsky, and Crane, 1968

Nitta, Masato & Nagasawa, Kazuya, 2016, Four Alien Monogeneans, Including Trinigyrus peregrinus n. sp., Parasitic on the Invasive Armored Catfish Pterygoplichthys disjunctivus (Siluriformes: Loricariidae) from Okinawa-jima Island, Okinawa Prefecture, Japan, Species Diversity 21, pp. 95-104 : 99-102

Unilatus brittani Mizelle, Kritsky, and Crane, 1968 ( Fig. 3 )

[New Japanese name: hime-rorikaria-era-mushi]

Unilatus brittani Mizelle, Kritsky, and Crane, 1968: 192 , figs 10–18; Suriano 1985: 165–168, figs 1–8; Kohn and Cohen 1998: 1532; Thatcher 2006: 89; Mendoza-Palmero et al. 2012: 493, figs 44–47; Branches and Domingues 2014: 92.

Unilatus longispinus Suriano, 1985: 172 , figs 16–21; Kohn and Cohen 1998: 1533; Thatcher 2006: 89.

Material examined. Only sclerotized structures were observed in two specimens (NSMT-Pl 6193a and 6194a together with five specimens of H. heterotylus ) fixed in APG.

Description. Body elongate, length 367±21.2 (352– 382, n =2) including haptor, width at mid-body 108±7.8 (102–113, n =2). Male copulatory organ ( Fig. 3L ) sclerotized, length 38±1.4 (37–39, n =2), spiral counterclockwise; distal medial portion with small bulb; distal portion thin; basal portion curved. Accessory piece ( Fig. 3L ) 29±2.1 (27– 30, n =2) in length, rod-shaped, distal end bifid and holding tip of male copulatory organ. Vagina ( Fig. 3M ) sclerotized, funnel-shaped, length 8±0.7 (7–8, n =2).

Haptor length 68±8.5 (62–74, n =2), width 118±0.7 (117–118, n =2). Anterior anchor ( Fig. 3A ) smaller than posterior anchor, total length 26±0.7 (25–26, n =2), outer length 20±0.7 (19–20, n =2), base width 7±0.7 (6–7, n =2), point length 13±1.4 (12–14, n =2), lacking accessory structure. Posterior anchor ( Fig. 3B ) lacking sclerotized cap and root, total length 34±0.7 (33–34, n =2), base width 9±0.7 (8–9, n =2), point length 13±1.4 (12–14, n =2). Anterior bar ( Fig. 3C ) broadly V-shaped, with expanded midsection, length 17±1.4 (16–18, n =2), total width 9±0.7 (8–9, n =2), median width 6±0.7 (5–6, n =2). Posterior bar ( Fig. 3D ) with ends curved, length 59±0.0 (59, n =2), total width 8±0.7 (7–8, n =2), median width 6±0.7 (5–6, n =2). Marginal hooks of larval type, 7 pairs; in length, pair I ( Fig. 3E ) 13±0.7 (12–13, n =2); pair II ( Fig. 3F ) 14±0.7 (13–14, n =2); pair III ( Fig. 3G ) 13±0.0 (13, n =2); pair IV ( Fig. 3H ) 13±1.4 (12–14, n =2); pair V ( Fig. 3I ) 12±0.7 (11–12, n =2); pair VI ( Fig. 3J ) 14±0.7 (13–14, n =2); pair VII ( Fig. 3K ) 13±0.0 (13, n =2).

Host. Vermiculated sailfin catfish, Pterygoplichthys disjunctivus ( Siluriformes : Loricariidae ).

Locality. Hija River , Misato, Okinawa city, Okinawajima island, Okinawa Prefecture, Japan .

Site of infection. Gill filaments.

Prevalence and intensity range (mean). 20% (2/10) and 1 (1.0).

Remarks. This monogenean was originally described by Mizelle et al. (1968) from Hypostomus sp. (as Plecostomus sp. ) in the Amazon River Basin, Brazil. Later, this species was reported from Hypostomus sp. in São Paulo, Brazil ( Suriano 1985) and from Pterygoplichthys anisitsi in Iquitos- Belén, Peru ( Mendoza-Palmero et al. 2012). Unilatus longispinus described by Suriano (1985) from P. multiradiatus was regarded as a junior synonym of U. brittani by Mendoza- Palmero et al. (2012). The morphology and measurements of the male copulatory organ and haptoral structures of the specimens examined in this study conform to the descriptions of U. brittani by Mizelle et al. (1968), Suriano (1985), and Mendoza-Palmero et al. (2012). This is the first record of U. brittani in Japan and P. disjunctivus represents a new host record for this monogenean.

Unilatus brittani is separated from U. unilatus by the posterior anchor’s lack of a sclerotized cup and its having a longer blade than its base ( Fig 3B ), the length of the vagina, and the anterior bar being more than twice as long as the posterior bar (see Remarks for U. unilatus ). The length of the posterior bar in U. brittani (59–64 µm: Mizelle et al. 1968; 60–66 µm: Suriano 1985; 57–72 µm: Mendoza-Palmero et al. 2012; 59 µm: this study) is greater than that of U. dissimilis (21–23 µm: Suriano 1985) and U. scaphirhynchae (14–17 µm: Suriano 1985) but shorter than that of U. irae (82–95 µm: Branches and Domingues 2014). By the length of the male copulatory organ, U. brittani (52–55 µm: Mizelle et al. 1968; 17–35 µm: Suriano 1985; 33–37 µm: Mendoza-Palmero et al. 2012; 37–39 µm: this study) differs from U. anoculus (61–66 µm: Price 1968) and U. irae (65–67 µm: Branches and Domingues 2014).

Japanese name. The new Japanese name refers to the small size of this species compared to U. unilatus : “hime” and “rorikaria-era-mushi” mean small and the genus Unilatus , respectively.

Genus Trinigyrus Hanek, Molnar, and Fernando, 1974 [New Japanese name: to-ashi-era-mushi-zoku] Trinigyrus peregrinus n. sp. ( Fig. 4 ) [New Japanese name: ito-naga-to-ashi-era-mushi]

Holotype. NSMT-Pl 6195 fixed in APG from the Hija River on 25 June 2015.

Paratypes. Twenty-two specimens: four and two specimens stained in Heidenhain’s iron hematoxylin from the Hija River (NSMT-Pl 6196–6197) and the Sembaru Reservoir (NSMT-Pl 6203), respectively; and nine and seven specimens fixed in APG from the Hija River (NSMT-Pl 6198–6200) and the Sembaru Reservoir (NSMT-Pl 6201– 6202), respectively .

Additional specimens. Two and four specimens from the Hija River (RUMF-ZF-00010b–00011) and the Sembaru Reservoir (RUMF-ZF-00012), respectively .

Description. Body ( Fig. 4A ) subconical, length 647±119.8 (460–819, n =18) including haptor, width at mid-body 217±46.9 (148–321, n =18). Alimentary system consisting of ovate pharynx (length 39±6.6 [25–52, n =21], width 40±9.3 [25–55, n =21]), short esophagus, and bifurcate intestinal caeca united posterior to testis. Testis pyriform, in mid-body, intercaecal, posterior to ovary, length 75±15.6 (62–102, n =5), width 89±4.8 (84–94, n =8). Vas deferens arising from anterior margin of testis, looping dorsoventrally around left intestinal caecum, distending to form seminal vesicle, and entering base of male copulatory organ. Two prostatic reservoirs saccate, located to right of oötype. Male copulatory organ ( Fig. 4E ) a coiled tube, forming circle of diameter 25±3.8 (21–36, n =19), curve length 60±2.5 (55–64, n =19). Accessory piece ( Fig. 4E ) c-shaped, length 31±3.2 (25–38, n =20), not articulating with male copulatory organ. Ovary in mid-body. Oviduct arising from anterior side of ovary, continuing as oötype surrounded by thick wall and located left of prostatic reservoirs. Mehlis’ gland not observed. Seminal reservoir located left of oviduct, opening to left side of oviduct. Vagina unsclerotized, exiting from anterior side of seminal reservoir, running ventrally to vaginal opening on right lateral side of body surface. Vitellaria approximately co-extensive with intestinal caeca. Egg ( Fig. 4F ) ovate, length 63±11.7 (50–72, n =3), width 32±4.0 (28–36, n =3), with long filament (about 4.5 mm, n =1) coiled in oötype.

Haptor with 5 pairs of haptoral appendages, length 158±24.2 (130–195, n =18), width 342±72.4 (230–435, n =18). Pair of anchors ( Fig. 4B ) with subrectangular base, total length 64±3.4 (59–71, n =22), base width 17±1.3 (15–20, n =20), point length 4±0.5 (3–5, n =21). Bar ( Fig. 4C ) broadly W-shaped, total length 154±13.7 (126–178, n =22), total width 38±4.5 (30–45, n =22), median width 4±0.7 (3–6, n =22). Marginal hooks ( Fig. 4D ) of larval type, 7 pairs, all of approximately same length, 13±0.8 (11–14, n =22).

Host. Vermiculated sailfin catfish, Pterygoplichthys disjunctivus ( Siluriformes : Loricariidae ).

Localities. Hija River , Misato, Okinawa city, and Sembaru Reservoir, Sembaru, Nishihara town, Okinawa-jima island, Okinawa Prefecture, Japan .

Sites of infection. Gill rakers, arches, and filaments.

Prevalence and intensity range (mean). 40% (4/10) and 4–13 (8.5) in the Hija River, and 100% (5/5) and 4–9 (6.4) in the Sembaru Reservoir.

Sequence data. A BLAST search of a 954-bp sequence that spanned the partial 28s rDNA region (accession no. LC104308 ) did not have any identical hits. The closest hits showed an 89–90% similarity with the following species: Ancyrocephalus percae (Ergens 1966) ( KF499080 ), A. paradoxus Creplin, 1839 ( AJ969952 ), Thaparocleidus siluri (Zandt, 1924) ( AJ969940 ), T. vistulensis ( AJ969941 ), Euryhaliotrema johni (Tripathi, 1959) ( DQ157657 ), Urocleidus similis (Mueller, 1936) ( AJ969951 ), and Actinocleidus recurvatus Mizelle and Donahue, 1944 ( AJ969951 ).

Remarks. The specimens examined in this study conform to the generic diagnosis of Trinigyrus as emended by Kritsky et al. (1986). Currently, four species are assigned to this genus: T. acuminatus Kritsky, Boeger, and Thatcher, 1986 ; T. hypostomatis Hanek, Molnar, and Fernando, 1974 ; T. mourei Boeger and Belmont-Jegu, 1994 ; and T. tentaculoides Kritsky, Boeger, and Thatcher, 1986 . Trinigyrus peregrinus n. sp. is readily separated from T. acuminatus , which has an elongate cirrus and a complex accessory piece ( Kritsky et al. 1986). The new species with its c-shaped accessory piece is also readily distinguishable from T. tentaculoides and T. mourei , both of which have a J-shaped accessory piece ( Kritsky et al. 1986; Boeger and Belmont-Jegu 1994). The male copulatory organ of the new species is coiled and forms a circle, while that of T. hypostomatis is J-shaped and tapers distally ( Hanek et al. 1974). Furthermore, the accessory piece articulates with the base of the male copulatory organ in T. hypostomatis ( Hanek et al. 1974; Boeger and Belmont-Jegu 1994), but not (or at least not clearly) in the new species.

Li et al. (2009) showed eggs of Trinigyrus hypostomatis with a short filament (fig. 1-4) and Unilatus unilatus with a long coiled filament (fig. 2-6), but they appear to have gotten the species (or their eggs) confused, because U. unilatus has an egg with a short filament ( Zica et al. 2012) whereas T. peregrinus n. sp. has an egg with a long filament (this study).

Etymology. The specific name of this new species, “ peregrinus ” meaning “foreign” or “exotic” in Latin, refers to our supposition that this is a non-native species in Japan.

Japanese name. In the new Japanese generic and specific names, “to-ashi” (ten legs) refers to the opisthohaptor’s ten appendages, “era-mushi” means gill monogeneans, and “zoku” means genus, and “ito-naga” means long string, referring to the long filament of the egg.

Figures

Fig. 3. Unilatus brittani Mizelle, Kritsky, and Crane, 1968. NSMT-Pl 6193. A, anterior anchors; B, posterior anchors; C, anterior bar; D, posterior bar; E, marginal hook of pair I; F, marginal hook of pair II; G, marginal hook of pair III; H, marginal hook of pair IV; I, marginal hook of pair V; J, marginal hook of pair VI; K, marginal hook of pair VII; L, male copulatory organ; M, vagina. Scale bars: 10µm.

Fig. 4. Trinigyrus peregrinus n. sp. Holotype (NSMT-Pl 6195) for B–E, paratypes for A (NSMT-Pl 6198, 6200) and for F (NMST-Pl 6202). A, whole mount (ventral view, composite); B, anchors; C, bar; D, marginal hook; E, male copulatory organ; F, egg. Scale bars: A and F, 200µm; B–E, 20µm. Abbreviations: ap, accessory piece; cg, cephalic glands; in, intestinal caecum; mco, male copulatory organ; mh, marginal hook; o, oötype; od, oviduct; ov, ovary; ph, pharynx; pr, prostatic reservoir; sr, seminal reservoir; sv, seminal vesicle; t, testis; va, vagina; vd, vas deferens; vl, vitellaria; vp, vaginal pore.