Heliconema anguillae Yamaguti, 1935

Moravec, František & Nagasawa, and Kazuya, 2018, Rhabdochona angusticaudata sp. n. (Nematoda: Rhabdochonidae) from the Japanese eel Anguilla japonica, and new records of some other nematodes from inland fishes in Japan, Folia Parasitologica (016) 65, pp. 1-22 : 7-9

Heliconema anguillae Yamaguti, 1935 Fig. 7

Description. Medium sized, whitish nematodes with thick, transversely striated cuticle. Cephalic end rounded. Cuticle in cephalic region inflated to form cephalic vesicle extending posteriorly to about level of deirids and anteriorly forming somewhat extended collar which may exceed pseudolabia anteriorly ( Fig. 7A,B ). Oral aperture dorsoventrally elongate, oval, rather large, surrounded by 2 massive, rounded lateral pseudolabia. Each pseudolabium bears 2 large submedian (dorsolateral and ventrolateral) cephalic papillae and oval lateroterminal depression filled with irregularly lobular mass; small lateral amphids situated between both cephalic papillae ( Fig. 7A,B ). Inner surface of each pseudolabium with elongate lateral mound bearing marked triangular terminal lateral tooth (internolateral tooth) situated immediately near inner border of cephalic depression and simple flat tooth at each dorsoventral extremity; no denticles present near terminal lateral teeth ( Fig. 7A,B ). Buccal cavity short. Oesophagus divided into short, narrow anterior muscular portion and much longer, wide glandular portion. Nerve ring encircles muscular oesophagus at its posterior half. Small simple deirids situated at about level of nerve ring. Excretory pore slightly anterior to anterior end of glandular oesophagus. Tail of both sexes with rounded tip.

Male (5 specimens). Length of body 28.7–33.4 mm, maximum width 462–612. Pseudolabia 12–15 long. Cephalic vesicle approximately 0.6–1.7 mm long and 204– 340 wide. Buccal cavity 39–51 long. Entire oesophagus 3.44–3.96 mm long, representing 11–12% of body length; muscular oesophagus 476–503 long and 81–109 wide; glandular oesophagus 2.9–3.5 mm long and 190–245 wide; length ratio of two parts of oesophagus 1: 6–7. Nerve ring, deirids and excretory pore 299–340, 299–326 and 394–517 from anterior extremity, respectively. Caudal end spirally coiled, provided with lateral alae supported by 4 pairs of subventral pedunculate preanal papillae arranged in couples, and 5 single pairs of subventral postanal papillae, which are rather large and pedunculate; an additional pair of small postanal sessile papillae situated ventrally slightly posterior to level of last subventral postanal pair ( Fig. 7C–F ); pair of very small ventral sessile postanal papillae located just posterior to cloacal aperture present in some specimens but absent in others ( Fig. 7C,E ). Pair of minute phasmids present posterior to ventral pair of posteriormost postanal papillae ( Fig. 7E,F ). Ventral surface between posteriormost ventral postanal papillae and phasmids elevated to form distict small protuberance ( Fig. 7E,F ). Cloacal lips somewhat elevated ( Fig. 7C,E ). Ventral precloacal surface with about 14 longitudinal tesselated ridges (area rugosa) ( Fig. 7C–E ). Spicules unequal and dissimilar; left spicule 544–748 long, with sharply pointed tip; right spicule broader, boat-shaped, 240–306 long, tapered towards distal tip. Length ratio of spicules 1: 1.9– 2.7. Length of tail 299–394.

Female (5 gravid specimens). Length of body 40.2– 52.4 mm, maximum width 612–966. Pseudolabia 15–21 long. Cephalic vesicle 340–381 wide. Buccal cavity 45–68 long. Entire oesophagus 3.8–4.7 mm long, representing 9% of body length; muscular oesophagus 503–680 long and 78–95 wide; glandular oesophagus 3.3–4.0 mm long and 177–258 wide; length ratio of two parts of oesophagus 1: 6. Nerve ring, deirids and excretory pore 340–367, 272–313 and 462–571 from anterior extremity, respectively. Vulva situated 17.8–23.2 mm from anterior end of body, at 44% of body length. Vulval lips not elevated.Vagina narrow, muscular, directed posteriorly from vulva. Uteri containing numerous oval, thick-shelled, embryonated (larvated) eggs; eggs 45–51 × 27–30, with wall 3 thick. Tail short, 190–204, with rounded tip.

Host: Japanese eel, Anguilla japonica ( Anguillidae , Anguilliformes ).

Site of infection: Stomach.

Locality : Misho Cove (near the mouth of the Renjoji River ), Ainan, Ehime Prefecture, Shikoku, Japan (collected 16 June 2007) .

Prevalence and intensity: 5 fish infected, 33.0– 44.6 cm TL /5 fish examined; 31–185 (mean 95) nematodes per fish.

Deposition of voucher specimens: IPCAS N-1091.

Remarks. Heliconema anguillae , originally described by Yamaguti (1935) from A. japonica from an unknown locality in Japan, was subsequently synonymised by Ogden (1969) with Heliconema longissimum (Ortlepp, 1922) . However, Katahira and Nagasawa (2015) resurrected this species and provided its detailed redescription based on newly collected specimens from A. japonica in Misho Cove, Ehime Prefecture, western Japan. The morphology of the present nematodes, collected from the same host species and the same locality, is in agreement with the species redescription, but the specimens are much larger (males and females approximately 29–33 and 40–52 mm long, respectively vs 16–23 and 20–29 mm), extending the biometrical variability of this species considerably.

While describing Heliconema hainanensis Li, Liu et Zhang, 2013 (correctly hainanense – see International Code of Zoological Nomenclature), Li et al. (2013) provided a key to species of Heliconema Travassos, 1919 . However, two congeneric species, Heliconema africanum (von Linstow, 1899) and Heliconema ahiri Karve, 1941 , both parasites of freshwater eels ( Anguilla spp. ) in South Africa and India, respectively, were not included; the former species was assigned to Heliconema and the latter one was revalidated only in 2013 ( Moravec et al. 2013a,b). Although the morphology of these two species is very similar to that of H. anguillae , H. africanum differs from this east-Asian species mainly in the number and character of postanal papillae (the pair of small sessile papillae located just posterior to the cloaca is absent), whereas H. ahiri mainly in the presence of minute denticles on pseudolabia in the region between the terminal lateral tooth and the submedian flat teeth and in the number and character of postanal papillae. In contrast to the three above-mentioned species, H. hainanense , a parasite of anguilliform fishes of the families Congridae and Muraenesocidae in the South China Sea, has each pseudolabium without a subterminal lateral depression and all six pairs of postanal papillae are subventral and pedunculate.

Heliconema anguillae is a brackish-water parasite which uses intertidal crabs as its intermediate hosts and A. japonica as its definitive hosts ( Katahira and Nagasawa 2015, see Nagasawa and Katahira 2017). Katahira et al. (2011) carried out some ecological observations on H. anguillae (reported as H. longissimum ) in A. japonica in Misho Cove and the lower reaches of the Renjoji River.

Figures

Fig. 7. Heliconema anguillae Yamaguti, 1935 from Anguilla japonica Temminck et Schlegel, scanning electron micrographs. A, B – cephalic end, subapical views (arrow indicates amphid); C – tail of male, sublateral view; D – ventral precloacal ridges and first two pairs of preanal papillae, ventral view; E – tail of male, ventral view; F – tail tip of male, ventral view (arrows indicate phasmids). Abbreviations: a – cephalic papilla; b – submedian tooth; c – lateral tooth; d – pseudolabial lateroterminal depression; e – cloacal aperture; f – papillae of first two preanal pairs; g – small ventral postanal papilla.