Syst Parasitol (2014) 89:167–173 DOI 10.1007/s11230-014-9514-3
Helicometra boseli Nagaty, 1956 (Digenea: Opecoelidae) in Sargocentron spiniferum (Forsska˚l) (Beryciformes: Holocentridae) from New Caledonian waters with a review of the Helicometra spp. in holocentrids
Rodney A. Bray • Jean-Lou Justine
Received: 16 June 2014 / Accepted: 21 July 2014 Ó Springer Science+Business Media Dordrecht 2014
Abstract The species Helicometra boseli Nagaty, family Holocentridae. Most of these are known only 1956 is redescribed from the holocentrid Sargocentron from holocentrids. Several are morphologically dis- spiniferum (Forsska˚l) off New Caledonia. It is char- tinct from the majority of Helicometra spp. in that they acterised by a short forebody, long cirrus-sac, reaching have a relatively short forebody and a cirrus-sac well into the hindbody, and undulating lateral margins. reaching well into the hindbody. In fact, Manter Stenopera rectisaccus Fischthal & Kuntz, 1964 is (1933) considered these features as generic distinc- considered a synonym. The status of the four species tions and erected the genus Stenopera Manter, 1933, of Helicometra Odhner, 1902 from holocentrids is with the type-species S. equilata Manter, 1933, for discussed. Three of the Helicometra species reported species exhibiting them. Most subsequent workers from holocentrids exhibit characteristics used to erect have not recognised Stenopera as distinct (Siddiqi & the genus Stenopera Manter, 1933, which is currently Cable, 1960; Fischthal & Kuntz, 1965; Hafeezullah, considered a junior synonym of Helicometra. 1971; Sekerak & Arai, 1974; Cribb, 2005).
Introduction Materials and methods Six nominal species of the genus Helicometra Odhner, 1902 have been reported in fishes of the beryciform Digeneans were collected live, immediately fixed in nearly boiling saline (Cribb & Bray, 2010; Justine et al., 2012) and then transferred to 80% ethanol. Whole-mounts were stained with Mayer’s paracar- mine, cleared in beechwood creosote and mounted in Canada balsam. Measurements were made through a R. A. Bray (&) drawing tube on an Olympus BH-2 microscope, using Department of Life Sciences, Natural History Museum, a Digicad Plus digitising tablet and Carl Zeiss KS100 Cromwell Road, London SW7 5BD, UK e-mail: [email protected] software adapted by Imaging Associates, and are quoted in micrometres. The following abbreviations J.-L. Justine are used: BMNH, British Museum (Natural History) ´ ISYEB, Institut de Syste´matique, Evolution, Biodiversite´ Collection at the Natural History Museum, London, (UMR7205 CNRS, EPHE, MNHN, UPMC), Muse´um National d’Histoire Naturelle, CP 51, 55 rue Buffon, UK; MNHN JNC, Muse´um National d’Histoire Nat- A9 75231 Paris cedex 05, France urelle, Paris, France. 123 168 Syst Parasitol (2014) 89:167–173
Family Opecoelidae Ozaki, 1925 ventral sucker. Vitellarium follicular, fields reach Subfamily Plagioporinae Manter, 1947 from level of ventral sucker or slightly to distinctly posterior to ventral sucker, to just posterior to caecal Helicometra boseli Nagaty 19561 ends, lateral to caeca and encroaching slightly over Syns Stenopera boseli (Nagaty, 1956) Pritchard, 1966; dorsal and ventral surface of caeca, not confluent even Stenopera rectisaccus Fischthal & Kuntz, 19642; in post-testicular region, follicles increase slightly in Helicometra rectisaccus (Fischthal & Kuntz, 1964) size and density posteriorly. Fischthal & Kuntz, 1965 Excretory pore terminal. Vesicle I-shaped, reaches Host: Sargocentron spiniferum (Forsska˚l). just anterior to ovary. Site in host: Digestive tract. Locality:Re´cif de Crouy, New Caledonia Type-host and locality: Neoniphon sammara (For- ˚ (22°200957S, 166°210375E, 13.v.2008). sskal), Red Sea at Hurghada (= Ghardaga), Egypt. Prevalence: 50% (1 out of 2 hosts examined). References: 1. Nagaty (1956); 2. Fischthal & Kuntz Voucher material: MNHN JNC2530. (1964); 3. Pritchard (1966); 4. Yamaguti (1970); 5. Toman & Kamegai (1974), 6. Present study. Description (Figs. 1–2) Descriptions:1,2,3,4,6. Holocentrid definitive hosts: Neoniphon sammara [Based on 10 measured specimens, see Table 1]. Body (Forsska˚l) (= Holocentrus samara) (1, 4). Sargocen- elongate, linguiform, tapering in forebody, margins tron punctatissium (Cuvier) (= Holocentrus lacteo- undulating, distinctly visible in live worms (Fig. 1). guttatus) (3, 4), Sargocentron xantherythrum (Jordan Tegument unarmed. Preoral lobe absent. Oral sucker & Evermann) (= Holocentrus xantherythrus) (3, 4), oval to slightly infundibuliform, subterminal. Ventral Sargocentron spiniferum (Forsska˚l) (= Holocentrus sucker rounded, in anterior quarter of body, usually spinifer) (4, 6), Sargocentron microstoma (Gu¨nther) slightly bigger than oral sucker. Prepharynx short, (= Holocentrus microstomus) (5), Sargocentron vio- entirely dorsal to oral sucker. Pharynx oval. Oesoph- laceum (Bleeker) (= Holocentrus violaceus) (2). agus distinct. Intestinal bifurcation in posterior fore- Other hosts: Naso unicornis (Forsska˚l) (Perciformes: body. Caeca narrow, end blindly in posterior third of Acanthuridae) (3). post-testicular region. Localities:RedSeaatHurghada,Egypt(1),Puerto Testes 2, irregularly lobate, tandem, separated, in Princesa, Palawan Island, Philippines (2), Oahu, Hawaii posterior half of hindbody. Cirrus-sac long, coiled in (3, 4), Saipan, Micronesia (5), New Caledonia (6). region of ventral sucker, claviform, reaches well into hindbody (Fig. 2). Seminal vesicle long, coiled in Remarks posterior part of cirrus-sac, reaching to about ventral sucker level, narrowing distally. Pars prostatica and Sekerak & Arai (1974) considered that this species ejaculatory duct not clearly differentiated, long, coiled, was a synonym of H. equilata (Manter, 1933) from complex coiling distally. Genital atrium distinct. holocentrids in the Caribbean Sea and Gulf of Mexico. Genital pore median to submedian, just pre-bifurcal. The species are certainly similar, but utilising the Ovary usually lobate (3–5 lobes, but oval in 1 measurements given by Manter (1933), Sekerak & specimen), pre-testicular, separated from anterior Arai (1974) and the illustration in Siddiqi & Cable testis. Seminal receptacle oval, dorsal to ovary. (1960), H. equilata appears to be slightly broader and Mehlis’ gland pre-ovarian. Laurer’s canal opens generally shorter (Fig. 3). These distinctions are dorsally to Mehlis’ gland. Uterus pre-ovarian, inter- certainly minor and may be the result of fixation caecal, coiled. Eggs tanned, operculate, with distinct differences, but as H. equilata is reported only in the filament. Metraterm thick-walled, reaches level of western Atlantic Ocean basin, it is likely that the forms are distinct. We consider H. rectisaccus (Fischthal & Kuntz, 1 urn:lsid:zoobank.org:act:CEE6CB9D-32CD-42B2-80E6-E74 EF6711771. 1964), originally described from the holocentrid 2 urn:lsid:zoobank.org:act:436C9113-3207-412B-8AB0-C696 Sargocentron violaceum from the Philippines, as a A88F90C1. synonym of H. boseli. Sekerak & Arai (1974) 123 Syst Parasitol (2014) 89:167–173 169
Helicometra nasae Nagaty & Abdel Aal, 1962 was considered the senior synonym of H. rectisaccus by Sekerak & Arai (1974). It is reported from ‘Nasa’ sp. (presumably the acanthurid Naso) and the serranid, the blacktip grouper Epinephelus fasciatus (Forsska˚l) in the Red Sea (Nagaty & Abdel Aal, 1962; Hassanine, 2001). It grows to a much larger size than the worms reported from holocentrids (Fig. 2), and is unlikely to be conspecific with the worms described here. Helicometra boseli has now been reported 11 times, ten of these are from holocentrids, and is found only in the Indo-West Pacific Region. A graph showing length vs width of Helicometra spp. from holocentrids (and similar worms from other host groups) is presented in Fig. 3. New measure- ments of ten specimens and data from published descriptions and illustrations are included. These include the measurements of individual specimens of H. equilata listed by Manter (1933) and new measurement ranges of this species given by Sekerak & Arai (1974). In most cases the range of measure- ments is used on the assumption that the shortest specimen is also the narrowest. The measurements of H. pteroisi (Gupta, 1956) from the scorpaenid Pterois russelii Bennett off south-eastern India (Gupta, 1956) appear to suggest that the widths of the worms are not related to the length; the accuracy of these measure- ments must be in doubt (hence the broken trend line).
Other species of Helicometra reported from holocentrids
Helicometra aegyptense Hassanine, 2007
Type-host and locality: Sargocentron spiniferum (Forsska˚l), Red Sea off the coast of Sharm El-Sheikh, Figs. 1–2 Helicometra boseli Nagaty, 1956. 1, Ventral view, South Sinai, Egypt. Scale-bars with uterus in outline; 2, Terminal genitalia. : A, 500 Reference lm; B, 200 lm : Hassanine (2007). considered it a synonym of H. nasae Nagaty & Abdel Remark Aal, 1962, following the suggestion of Pritchard (1966), distinguishing it from H. equilata (= H. boseli) This species is distinguished by the very large ventral by the degree of curvature of the cirrus-sac. In all our sucker, the spatulate body shape and the vitellarium specimens the cirrus-sac is coiled at the level of the reaching well into the forebody (i.e. short pre-vitelline ventral sucker, but passes into the hindbody along the distance). median line. In this regard our specimens most closely Helicometra aposinuata Pritchard, 1966 resemble H. rectisaccus, but it should be born in mind that Pritchard (1966), in redescribing H. boseli, said Type-host and locality: Neoniphon scythrops (Jordan that she found the cirrus-sac ‘sigmoid to straight’. & Evermann), Oahu, Hawaii. 123 170 Syst Parasitol (2014) 89:167–173
Fig. 3 Graph showing length versus width of Helicometra spp. from holocentrids, and similar worms, including new data and data from published descriptions and illustrations References: 1. Pritchard (1966); 2. Yamaguti (1970); References:1.Manter(1933); 2. Manter (1947); 3. 3. Wang et al. (1992). Sparks (1957); 4. Sogandares-Bernal (1959); 5. Siddiqi Descriptions:1,2,3. &Cable(1960); 6. Nahhas & Cable (1964); 7. Fischthal Holocentrid hosts: Neoniphon scythrops (Jordan & (1977); 8. Fischthal (1978); 9. Dyer et al. (1985); 10. Evermann) (= Holocentrus scythrops) (1), Sargocen- Nahhas (1993); 11. Nahhas & Carlson (1994). tron spiniferum (Forsska˚l) (= Holocentrus spinifer) Descriptions: 1, 5 (illustration only), 8 (allometry). (2), ‘Holocentrid’ (1). Hosts: All belonging to Holocentridae: Holocentrus Other hosts: Thalassoma duperrey (Quoy & Gaimard) ascensionis (Osbeck) (1, 2, 3, 4, 5, 6, 7, 8, 11), (Perciformes: Labridae) (1); Epinephelus awoara Holocentrus rufus (Walbaum) (9), Neoniphon mari- (Temminck & Schlegel) (Perciformes: Serranidae) (3). anus (Cuvier) (= Holocentrus marianus) (10). Localities: Oahu, Hawaii (1, 2), Fujian, China (3). Localities: Tortugas, Florida, USA (1, 2), Nassau, Bahamas (3), Eleuthera, Bahamas (3), Lerber Fish Remark Pens, North Bimini, Bahamas (4), Near Cat Cay, Bahamas (4), Mona Island, Puerto Rico (5), Jamaica This species is a more typical species of Helicometra (6, 11), Drowned Cays, Belize (7, 8), Mario Island, in that it has a relatively long forebody and short Puerto Rico (9), Grand Cayman, Cayman Islands (10). cirrus-sac. It also differs from H. boseli in its broader body, the vitellarium reaching to about the bifurcal Remark level, and in the contiguous or overlapping gonads. Sekerak & Arai (1974) considered it a synonym of H. This species, the type-species of the genus Stenopera, pulchella (= H. fasciata). is discussed above and is certainly similar to H. boseli, but is geographically separated. The record of Helicometra equilata (Manter, 1933) Siddiqi & ‘Stenopera equilata’ from the perciform ‘Labrus Cable, 1960 bergylata’ from off the Libyan coast in the Mediter- Syn. Stenopera equilata Manter, 1933 ranean by Al-Bassel (2001) is clearly not a correct identification. Amongst other differences, the eggs Type-host and locality: Holocentrus ascensionis (Os- are figured as lacking a filament and no filament is beck), Tortugas, Florida, USA. described. 123 Syst Parasitol (2014) 89:167–173 171
Table 1 Measurements and ratios of Helicometra boseli Table 1 continued Range Mean Range Mean
Body length 2,243–3,128 2,727 Posterior testis length (%)* 8.9–13.0 11.1 Body width 361–577 476 Pre-vitelline distance 453–713 548 Forebody length 383–508 450 Pre-vitelline distance (%)* 16.1–24.2 20.2 Oral sucker length 115–146 129 Vitellarium to ventral sucker (%)** 0–13.1 3.1 Oral sucker width 117–141 130 Pre-bifurcal distance 318–375 345 Pharynx length 63–84 77 Pre-bifurcal distance (%)* 11.7–14.2 12.7 Pharynx width 71–90 81 Cirrus-sac reach 806–1,088 1,001 Oesophagus 131–196 159 Cirrus-sac reach (%)* 34.5–37.0 35.8 Intestinal bifurcation to ventral sucker 65–133 105 * percentage of body length; ** percentage of ventral sucker to Vitellarium to ventral sucker 0–100 21 ovary distance Ventral sucker length 119–171 152 Ventral sucker width 114–178 155 Cirrus-sac length 571–873 717 Helicometra fasciata (Rudolphi, 1819) Odhner, Cirrus-sac width 52–103 89 1902 Extent of cirrus-sac into hindbody 303–488 400 Ventral sucker to ovary 500–772 650 Remark Ovary length 94–210 165 Ovary width 81–221 155 Parukhin (1970) reported this species from the holo- Ovary to anterior testis 0–144 51 centrid Myripristis murdjan (Forsska˚l) from the Red Anterior testis length 200–381 284 Sea. Specimens recognised as H. fasciata are reported Anterior testis width 158–273 222 from many host species, and many localities (e.g., Distance between testes 21–198 101 Sekerak & Arai, 1974; Aken’Ova et al., 2005). Enzyme Posterior testis length 215–352 301 electrophoretic studies have shown that cryptic species Posterior testis width 195–289 250 occur in this ‘complex’ (Reversat et al., 1989, 1991). Post-testicular region 488–746 567 Considering the morphological similarity, this record Post-caecal distance 175–265 223 may be of Helicometra aposinuata. Egg-length 40–48 44 Egg-width 19–32 24 Helicometra sp. Width (%)* 16.1–19.6 17.4 Reference: Rigby et al. (1999) Forebody (%)* 14.8–18.5 16.6 Hosts: Sargocentron diadema (Lacepe`de), Sargocen- Sucker length ratio 1.04–1.43 1.18 tron microstoma (Gu¨nther), Sargocentron spiniferum Sucker width ratio 0.98–1.35 1.19 (Forsska˚l). Oral sucker: pharynx ratio 1.47–1.68 1.61 Locality: Moorea, Society Islands, French Polynesia. Ventral sucker to ovary (%)* 20.6–26.3 23.8 Extent of cirrus-sac into hindbody** 53.5–66.4 58.8 Discussion Post-testicular region (%)* 18.8–26.3 20.9 Oesophagus (%)* 5.23–6.63 5.85 Our results indicate that there are four species of Intestinal bifurcation to ventral 2.92–5.10 3.82 sucker (%)* Helicometra commonly found in holocentrid (Beryci- Vitellarium to ventral sucker (%)* 0–3.40 0.76 formes) fishes. Three, H. boseli (syn. H. rectisaccus), H. Ovary to anterior testis (%)* 0–5.49 1.87 equilata and H. aegyptense, have unusually short Distance between testes (%)* 0.74–6.71 3.69 forebodies and long cirrus-sacs and fit into the concept Manter (1933)calledStenopera. Not all Stenopera-like Cirrus-sac length (%)* 21.3–28.1 25.5 species are associated with holocentrids however. Anterior testis length (%)* 7.6–13.9 10.4 Helicometra nasae has been reported in the acanthurid
123 172 Syst Parasitol (2014) 89:167–173
Naso (presumably, see above) (Nagaty & Abdel Aal, Lepidophyllinae and comments on some aspects of biol- 1962) and a serranid (Hassanine, 2001)andH. pteroisi ogy. Systematic Parasitology, 9, 83–123. Cribb, T. H. (2005). Family Opecoelidae Ozaki, 1925. In: Jones, (Gupta, 1956) is reported only in the scorpaenid Pterois A., Bray, R. A. & Gibson, D. I. (Eds) Keys to the Trema- russelii from Mandapam Camp, southeastern India toda. Volume 2. Wallingford: CABI Publishing and the (Gupta, 1956). Pritchard (1966), who continued to Natural History Museum, pp. 443–531. recognise Stenopera,reportedH. boseli in an acanthurid Cribb, T. H., & Bray, R. A. (2010). Gut wash, body soak, blender, and heat-fixation: approaches to the effective as well as holocentrids. As far as we are aware there are collection, fixation and preservation of trematodes of 26 host-parasite records of Stenopera-like worms, 22 fishes. Systematic Parasitology, 55, 45–52. (85%) of which are from holocentrids. 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