Heliconema, Travassos, 1919

Boyko, Christopher B., Williams, Jason D. & Shields, Jeffrey D., 2017, Parasites (Isopoda: Epicaridea and Nematoda) from ghost and mud shrimp (Decapoda: Axiidea and Gebiidea) with descriptions of a new genus and a new species of bopyrid isopod and clarification of Pseudione Kossmann, 1881, Zootaxa 4365 (3), pp. 251-301 : 282-283

Heliconema sp.

Fig. 11

Material examined. United States: 2 worms (7.4, 8.2 mm), ex gill tissue of ovigerous female Lepidophthalmus louisianensis (13.0 mm CL), Grande Terre, Lousiana, coll. unknown, 25 May 1988 ( ULLZ 3531); 8 worms (3 extracted: 7.5, 9.7, 11.5 mm; one specimen on SEM stub, USNM 1459849 ex ULLZ 10208), ex ventral thorax and base of third pereopods of female L. louisianensis (8.8 mm CL), inshore, Bay St. Louis, Mississippi, coll. unknown, 18 Jul 1990 ( ULLZ 10208); 1 worm (not extracted), ex gill tissue of female L. louisianensis (8.9 mm CL), outer beach, Bay St. Louis, Mississippi, coll. R. Griffis & D. L. Felder, 26 Jan 1991 ( ULLZ 10203).

Distribution. Mississippi and Louisiana, U.S. A.

Host. Lepidophthalmus louisianensis (Schmitt, 1935) .

Remarks. Three specimens of Lepidophthalmus louisianensis (Schmitt, 1935) were parasitized by juvenile non-encysted nematodes ( Fig. 11 ). One of the parasitized hosts (ULLZ 3531) was an ovigerous female and contained two worms extending into the gills and thorax. The other two hosts were non-ovigerous females and contained one worm (ULLZ 10203) in the gill tissue and eight worms (ULLZ 10208) in the ventral thorax and bases of third legs. The extracted nematodes ranged in length from 7.4 to 11.5 mm (8.9±1.7, n=5). Based on the morphology of the nematodes, particularly the structure of the mouth ( Fig. 11B, C ), they are members of Physalopteridae , most closely matching the genus Heliconema Travassos, 1919 . The oral aperture of each of our specimens has two pseudolabia; each pseudolabium has a pair of cephalic papillae, a large median conical tooth and ridged teeth ( Fig. 11B ) while the amphids are indistinct. These characters are similar to those of H. brooksi Crites & Overstreet, 1991 , which was described from the shrimp eel, Ophichthus gomesii (Castelnau, 1855) , collected in Mississippi Sound, Gulf of Mexico. Crites & Overstreet (1991) also found a juvenile nematode in a shrimp, Penaeus setiferus (Linnaeus, 1767) , and suggested that the juvenile specimen may also be H. brooksi but noted that additional research was required for verification. In addition to H. brooksi , an undescribed species of Heliconema from the sharptail eel, Myrichthys acuminatus (Gronow, 1854) , also exists in the Gulf of Mexico (Moravec, pers. comm.).

Larvae of other Heliconema species are known from crustacean intermediate hosts. Those of Heliconema anguillae Yamaguti, 1935 , are known to occur in the brachyurans Hemigrapsus sp. and Perisesarma bidens (De Haan, 1835) in Japan ( Katahira & Nagasawa 2015) and it is possible that the “ Ascarophis ” third-stage larvae described by Moravec et al. (2003) from the brachyuran Macrophthalmus hirtipes (Heller, 1865) (= Hemiplax hirtipes (Jacquinot, in Hombron & Jacquinot, 1846)) in New Zealand were also larvae of a species of Heliconema (Moravec, pers. comm.). Species of nematodes from other families also use callianassids as intermediate hosts and are trophically transmitted to elasmobranchs or bony fish as definitive hosts ( Poinar & Thomas, 1976). For example, two unidentified species of Ascarophis van Beneden, 1871 , were found in Neotrypaea californiensis (Dana, 1854) from California ( Poinar & Thomas 1976).

There are no reports on the specific diet of the shrimp eel, O. gomesii , but it is likely an opportunistic feeder, based on the stomach contents of congeners ( Casadevall et al. 1994) and has been reported to feed “heavily on shrimps” ( Crites & Overstreet 1991); L. louisianensis is therefore a potential prey item. Based on stomach content analyses, potential definitive hosts in the Gulf of Mexico for this species of Heliconema are bottom feeding fish predators of L. louisianensis , including croaker ( Menticirrhus sp., Sciaenidae ) and unspecified catfish ( Felder & Rodrigues 1993). Stingrays are also possible predators of L. louisianensis based on observations of their feeding habits ( Felder & Rodrigues 1993).

Anguilliform fish host the highest diversity of Heliconema species but nematodes in this genus are also known from four other actinopterigian orders, as well as two orders of elasmobranchs (see Akram 1996; Li et al. 2013). Although two species of Heliconema have been reported from snakes, Moravec et al., (2007) summarized the persistent doubts as to the identity of the type hosts for H. longissimum ( Ortlepp, 1923) . The host of this nematode was originally identified as “snakes” (in quotation marks as originally given by Ortlepp, 1923) but this species has subsequently been reported several times from eel hosts. Interestingly, only one species of Heliconema was ever described from adult worms extracted from a host verified as a snake: H. serpens Fusco & Palmieri, 1980 , described from Cerberus rynchops (Schneider, 1799) and found in only a single host individual ( Fusco & Palmieri 1980). Because these snakes are well-known consumers of eels ( Gorman et al. 1981) it is possible that the snake picked up the nematodes through parasitized prey and thus served as a postcyclic host (sensu Odening 1976) for H. serpens ; the snake was not a paratenic host because the worms were mature. If true, this would be analogous to the situation reported by Goldberg et al. (2002) who found mature lizard-parasitizing nematodes in the lumen of the digestive tract of snakes who preyed on parasitized lizards. Indeed, Goldberg et al. (2002) cautioned that any finding of adult nematodes in a snake must consider the possibility that the nematodes entered via the snake’s prey, their definitive host, and not because the snake ingested an intermediate host of the parasite.

Figures

FIGURE 11. Scanning electron micrographs of Heliconema sp. ex Lepidophthalmus louisianensis (Schmitt, 1935) (USNM 1459849ex ULLZ 10208).A, whole juvenileworm,lateral view;B,anterior end, en face view; C, anteriorend, lateral view; D, posterior end, oblique view. P = cephalic papillae, to = median conical tooth, te = ridged teeth. Scale bars: A = 1 mm; B = 30 µm; C = 50 µm; D = 200 µm.