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Research Article Heliconema Anguillae Yamaguti, 1935 © Institute of Parasitology, Biology Centre CAS Folia Parasitologica 2015, 62: 028 doi: 10.14411/fp.2015.028 http://folia.paru.cas.cz Research Article Heliconema anguillae Yamaguti, 1935, a physalopterid nematode found in Japanese eels: taxonomic resurrection with a note on the third-stage larva from intertidal crabs in western Japan Hirotaka Katahira1 and Kazuya Nagasawa2 1 Graduate School of Environmental Earth Science, Hokkaido University, Sapporo, Hokkaido, Japan; 2 Graduate School of Biosphere Science, Hiroshima University, Hiroshima, Japan Abstract: A parasitic nematode from the stomach of Japanese eel Anguilla japonica Temminck et Schlegel in western Japan, pre- [Heliconema longissimum (Ortlepp, 1922), was morphologically re-examined and compared with the previous descriptions. In addition, the third-stage larva of this nematode is described, based on the specimens of encapsuled larvae found in musculature of two crabs, Hemigrapsus sp. and Perisesarma bidens (De Haan), caught from the upper-intertidal zone of the same local- [ the character of H. longissimum[H. longissimum; [ found in the original description and the syntype specimens of H. anguillae Yamaguti, 1935 that has been synonymised with H. longis- simum, we thus here resurrect H. anguillae as an accepted species. For the life-cycle of the present nematode, littoral crabs, including the two infected species, are likely to be the source of infections for Japanese eels, acting as intermediate hosts. Keywords: Nematoda, parasitic nematode, taxonomy, morphology, intermediate hosts, littoral crabs The genus Heliconema Travassos, 1919 (Physalopteri- this genus from the other related genera belonging to the dae) is a group of parasitic nematodes characterised by subfamily Proleptinae, in addition to the redescription of [ H. longissimum based on the specimens from rice-paddy on the internal border of each pseudolabium with a lateral eels Pisodonophis boro (Hamilton) in brackish waters of marked-tooth and two dorsoventral simple-teeth (Moravec Thailand. Li et al. (2013) subsequently discovered an un- 2007, Moravec et al. 2007, Chabaud 2009). This nematode described species from congers Uroconger lepturus (Ri- [ - chardson) (type host), Muraenesox cinereus (Forsskål) son 2000) and presently consists of 14 species (see Crites and Congresox talabonoides (Bleeker) in the South China and Overstreet 1991, Moravec 1998, Moravec et al. 2007, Sea, which was described as H. hainanensis. Meanwhile, 2008, 2013a, b): 12 valid species, namely H. africanum Moravec et al. (2013b) have recognised that a species, pre- (Linstow, 1899), H. heliconema Travassos, 1919 (type- viously thought as H. longissimum (see Taraschewski et species), H. longissimum (Ortlepp, 1922), H. brevispicu- !""#$[Anguilla mossambica lum Baylis, 1934, H. ahiri Karve, 1941, H. baylisi Ogden, (Peters) in freshwater habitats of South Africa can be iden- 1969, H. serpens Fusco et Palmieri, 1980, H. psammo- tical with H. africanum. Moravec et al. (2013a) further- batidus Threlfall et Carvajal, 1984, H. kherai Gupta et more re-examined taxonomic status of H. ahiri, previously Duggal, 1989, H. brooksi Crites et Overstreet, 1991, and considered as a junior synonym as H. longissimum, and H. savala Akram, 1996; H. hainanensis Li, Liu, Liu et resurrected it based on the material from Indonesian short- Zhang, 2013, and two species inquirendae, H. urolophi [Anguilla bicolor bicolor McClelland of southern (Johnston et Mawson, 1951) and H. hamiltonii Bilqees et India. Khanum, 1970. Due to the sequence of awareness on the previous con- In recent years, taxonomic reviews have been conducted [ % on the genus Heliconema, which has improved our under- the obtained specimens of the genus Heliconema. In par- [ ticular, Moravec et al. (2013b) doubted taxonomic status (2007) provided useful taxonomic criterion to discriminate of H. longissimum and suggested a possibility of its com- Address for correspondence: H. Katahira, Graduate School of Environmental Earth Science, Hokkaido University, N10W5, Sapporo, Hokkaido 060-0810, Japan. Phone: +81-11-706-2245; Fax: +81-11-706-4864; E-mail: [email protected] This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. doi: 10.14411/fp.2015.028 Katahira and Nagasawa: Taxonomic status of Heliconema anguillae plexity consisting of several morphologically closely re- species of pilumnid rock crab, Pilumnopeus makianus (Rathbun) lated species. Under this situation, it is questionable that (n = 2; 12–15 mm CW); three species of varunid crabs, Hem- H. longissimum has so far been reported not only from sa- igrapsus sanguineus (De Haan) (n = 13; 6–14 [average 10] mm line environments in Japan and Thailand (Moravec et al. CW), Hemigrapsus sp. (n = 39; 7 –21 [12] mm CW) and Hel- 2007, Katahira et al. 2011) but also from fresh waters in ice tridens (De Haan) (n = 4; 17 –25 [21] mm CW); two species other regions (Ogden 1969, Sood 1970, De et al. 1978, De of sesarmid crabs, Sesarma dehaani H. Milne Edwards (n = 2; 1988; see also Moravec et al. 2007). It thus appears that the 25–30 mm CW) and Perisesarma bidens (De Haan) (n = 8; 8–18 [H. longissimum, need [15] mm CW); and one species of macrophthalmid crabs, Macro- &'[- phthalmus (Macrophthalmus) abbreviatus Manning et Holthuis ity. (n = 1; 17 mm CW). In addition, 13 decapod specimens were In Japanese waters, H. longissimum is known as a stom- caught from freshwater environments in the Renjoji River and the ach parasite of Japanese eels Anguilla japonica Temminck Sozu River: they were one species of palaemonid shrimp, Mac- et Schlegel (see Nagasawa et al. 2007). Although Yamaguti robrachium nipponense (De Haan) (n = 12; 63–90 [78] mm TL); (1935) originally described H. anguillae Yamaguti, 1935 and one species of varunid crab, Eriocheir japonica (De Haan) from Japanese eels without stating its sampling locality, (n = 1; 39 mm CW). Like the adult specimens from Japanese eels, this nematode was synonymised with H. longissimum by the larval nematodes recovered were washed in physical saline, *<=>=$[?<=Q#$ 'X"[X"[ morphological investigation has never been conducted on For a microscopic examination, the nematode specimens the Japanese material of H. longissimum. In this paper, we Q#[{ re-examine the morphology of Japanese H. longissimum, mature males and gravid females were randomly chosen from based on the specimens collected by Katahira et al. (2011) the specimens from Japanese eels. The specimens were exam- from Japanese eels in a brackish-water cove of western Ja- ined under an Olympus BX51 light microscope using phase con- pan. We also describe the third-stage larva of the genus trast optics. Drawings were made with the aid of a drawing tube Heliconema found during a survey of decapods sympatri- and measurements were taken using an ocular micrometre; all cally occurring with Japanese eels. )$ indicated and provided as the range followed by the mean in pa- MATERIALS AND METHODS rentheses. For scanning electron microscopy (SEM), three male Two Japanese eels Anguilla japonica were caught with cov- specimens from a Japanese eel caught on 18 October 2008 were ert traps in the innermost part of Misho Cove (32°57'30''N; dehydrated in an ethanol series, dried by hexamethyldisilazane, 132°33'58''E) in Ehime Prefecture, western Japan, on 31 August sputter-coated with gold and observed at 15 kV accelerating 2008 and 18 October 2008 (see Katahira et al. 2011). These eels voltage with a Hitachi S-3000N instrument. In addition to the were kept alive in oxygenated containers with ambient waters and above procedure, the syntype specimens of H. anguillae depos- brought to the laboratory of the Hiroshima University, where they ited in the Meguro Parasitological Museum, Tokyo (MPM Coll. were measured for total length (TL) in millimetres and examined No. 23939–23940) were examined because they were recently for nematodes under a stereomicroscope. All nematode speci- \ 'X"[ [ %X"[ dried lactophenol), only limited body structures were measured. Sampling of decapod crustaceans for larval nematodes was [ \ paper follow WoRMS (2013). Cove (32°57'35''N; 132°33'05''E) and two adjacent rivers, the Renjoji River (32°57'27''N; 132°34'05''E) and the Sozu River RESULTS Q!#X^__^^`{ <Q!QQ^Q"^^|$ \ { Of the two Japanese eels examined, the smaller these localities have been described elsewhere (see Mizuno and one (386 mm TL, 31 August 2008) was infected with Nagasawa 2010, Katahira et al. 2011). Decapods were caught by 151 worms, whereas the larger one (415 mm TL, 18 Octo- hands or hand nets in Misho Cove during low tides on 11 Novem- ber 2008) harboured 389 worms. ber 2013 and in the rivers on 10 November 2013. These decapods Two species, i.e. Hemigrapsus sp. and Perisesarma bi- were kept alive in containers and brought to the laboratory of the dens, were found infected with nematode larvae; two of 39 Hiroshima University, where they were measured for carapace Hemigrapsus sp. and one of eight P. bidens were infected width (CW) or total length (TL) in millimetres, and immediately with the intensity of one worm in each individual. Infection examined for nematode larvae under a stereomicroscope. A total site is the musculature at the mouthpart and the basal part of 82 decapod specimens (nine families, 11 genera, 13 species) of legs, where the larvae were encapsulated among muscle [ [ shrimp (n = 1; 50 mm TL); two species of palaemonid shrimps, The syntype specimens of Heliconema anguillae con- [ (Stimpson) (n = 6; 29–42 [34.8] mm TL) tained eight individuals (two males and two females col- and Palaemon serrifer (Stimpson) (n = 1; 25 mm CW); one uni- lected on 27 January 1927, and one male and three females [Alpheus sp. (n = 1; 35 mm collected on 5 February 1927). The measurements of these TL); one species of upogebiid mud shrimp, Upogebia yokoyai specimens are presented in Table 1.
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