Rodney A. Bray Jean-Lou Justine
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1 Syst Parasitol (2013) 85: DOI /s x Three species of opisthomonorchiine monorchiids (Digenea) in spp. (Perciformes: Carangidae) from off New Caledonia, with a description of Opisthomonorchis dinema n. sp. Rodney A. Bray Jean-Lou Justine Received: 5 December 2012 / Accepted: 13 March 2013 Ó Springer Science+Business Media Dordrecht 2013 Abstract Three opisthomonorchiinae species are described from fishes obtained at the Fish Market in Nouméa, New Caledonia. Opisthomonorchis dinema n. sp. from dinema Bleeker differs from the other recognised species in the genus by the long recurved genital atrium, arcing anteriorly. Also described are Opisthomonorchis carangis Yamaguti, 1952 from sp. and Pseudopisthomonorchis thapari (Varma & Singh, 1979) n. comb. for Opisthomonorchis thapari Varma & Singh, 1979 from chrysophrys (Cuvier). The features distinguishing Opisthomonorchis Yamaguti, 1952 and Pseudopisthomonorchis Madhavi, 1974 are discussed. Introduction The subfamily Opisthomonorchiinae Yamaguti, 1952 and the genus Opisthomonorchis Yamaguti, 1952 were erected by Yamaguti (1952) for an apparently monorchiid which differed from typical monorchiids R. A. Bray (&) Department of Life Sciences, Natural History Museum, Cromwell Road, London SW7 5BD, UK rab@nhm.ac.uk J.-L. Justine UMR 7138 Systématique, Adaptation, Évolution, Muséum National d Histoire Naturelle, Case postale 51, 55 rue Buffon, Paris Cedex 05, France justine@mnhn.fr in its postacetabular genital pore and in the absence of the spined metraterm or terminal organ. In New Caledonian waters, we have found three species belonging to this subfamily, including one we consider as new. Two genera have been included in the subfamily, Opisthomonorchis and Pseudopisthomonorchis Madhavi, Originally, Madhavi (1974) distinguished Pseudopisthomonorchis from Opisthomonorchis by its globular cirrus sac, short unarmed cirrus, spacious genital atrium armed with spines and preacetabular vitellaria. Hafeezullah (1984) in synonymising the genera discussed only the position of the vitellarium ( acetabular and preacetabular ) and considered this as only a specific distinction, thus considering Pseudopisthomonorchis synonymous with Opisthomonorchis. In her review of the family Monorchiidae, Madhavi (2008) retained the genera as distinct, using the globular cirrus-sac and the band of vitelline follicles across the posterior forebody as the distinguishing features. Our observations suggest that the vitellarium also differs in being in more or less one field of irregular follicles in Pseudopisthomonorchis rather than two distinct lateral fields of relatively uniform follicles as in Opisthomonorchis. We feel that these vitelline characteristics and the shape and content of the cirrus-sac maintain a good case for the retention of the genus Pseudopisthomonorchis. All but one report of opisthomonorchiines are from carangids and all are from the Indo West Pacific region, mainly from the genus. The one
2 148 Syst Parasitol (2013) 85: species from an ephippid is rather distinct morphologically with a short forebody and the vitellarium close to the anterior extremity. Materials and methods Seven dinema Bleeker [Fork Length (FL), mm; Weight (W), g], three chrysophrys (Cuvier) (FL, mm; W, g) and two sp. (FL, mm; W, g) were obtained from the fish market of Nouméa, New Caledonia. Most fishes were taken with mackerel nets within a few miles off Nouméa and were very fresh. All carangids were relatively young specimens, far from the maximum lengths reported for these species (Smith-Vaniz, 1999). Carangid identification is difficult, especially when they are not fully grown, and ten species of are known from New Caledonia (Fricke et al., 2011). A specimen of C. dinema was previously misidentified as C. oblongus (Cuvier) and the nematode Capillariidae gen. sp. 3 was erroneously reported from this species (Moravec & Justine, 2010). Specimens of our sp. were similar in many aspects to the published description of C. talamparoides Bleeker, but with differences in colour that prevented definitive identification. Specimens of C. chrysophrys were similar to the published description, but with minor differences in colour; one of the ichthyologists consulted did not exclude the possibility that it could be a new species. Digeneans were sometimes extremely numerous, with more than 200 found in one C. dinema. Digeneans were collected live, immediately fixed in nearly boiling saline and then transferred to 80% ethanol (Cribb & Bray, 2010). Whole mounts were stained with Mayer s paracarmine, cleared in beechwood creosote and mounted in Canada balsam. Measurements were made through a drawing tube on an Olympus BH-2 microscope, using a Digicad Plus digitising tablet and Carl Zeiss KS100 software adapted by Imaging Associates, and are quoted in micrometres. The following abbreviations are used: BMNH, British Museum (Natural History) Collection at the Natural History Museum, London, UK; MNHN JNC, Muséum National d Histoire Naturelle, Paris, France. Fish nomenclature mainly follows Froese & Pauly (2012). Family Monorchiidae Odhner, 1911 Subfamily Opisthomonorchiinae Yamaguti, 1952 Genus Opisthomonorchis Yamaguti, Opisthomonorchis dinema n. sp. 2 Type-host: dinema Bleeker, Perciformes, Carangidae, shadow trevally. Type-locality: Nouméa Fish Market, New Caledonia (26.viii.2010). Site: Digestive tract. Prevalence: 43% (3 out of 7 fish). Specimens: Holotype: MNHN ; paratypes: JNC3224A, JNC3225, JNC3226, BMNH Description (Fig. 1; Table 1) [Based on 49 specimens.] Body small, narrow, fusiform, widest at region of ventral sucker and vitellarium. Body spines tiny, in annular rows reaching to mid-level of post-testicular region. Eyespots paired, at level just anterior to middle of oesophagus. Oral sucker oval, subterminal, small. Ventral sucker rounded, larger than oral sucker, in about mid-body. Prepharynx long, narrow. Pharynx subglobular, small. Oesophagus long, narrow. Intestinal bifurcation in about mid-forebody. Caeca wide anteriorly, width varying, run closely parallel in forebody, arcing around central part of body, terminating at or just anterior to testes, distant from posterior extremity. Testis single, oval, edges often obscured by eggs, just anterior to mid-hindbody. Cirrus-sac large, claviform, overlapping testis posteriorly, reaches just antero-dextral to ventral sucker, demarcation from ejaculatory duct indicated by arrowhead in Fig. 1. Internal seminal vesicle oval, in posterior third of cirrus-sac. Pars prostatica large, oval, filled with granular material. Ejaculatory duct wide, rectilinear, lined with long spines. Genital atrium long, curved from distal part of cirrus-sac, over the anterior margin of the ventral sucker, and reaching posteriorly along 1 urn:lsid:zoobank.org:act:8a8c2c4b-d2d2-4ee FEF917FE23C. 2 urn:lsid:zoobank.org:act:396db281-7ac b52f-6fb 1D7101EC4.
3 Syst Parasitol (2013) 85: sinistral margin of ventral sucker; distal, posteriorly directed part lined with long spines. Genital pore wide slit, postero-sinistral to ventral sucker. Ovary oval, edges often obscured by eggs, ventral to cirrus-sac, occasionally may overlap ventral sucker, pre-testicular, close or adjacent to testis. Mehlis gland, seminal receptacle and Laurer s canal obscured by eggs. Uterus reaches from anterior edge of ovary to posterior part of post-testicular region, distal extremity passes ventrally to cirrus-sac. Eggs numerous, small, with distinct aporal filament of similar length to egg; eggs in whorls typical of filamented eggs. Metraterm not differentiated. Vitellarium follicular, in lateral fields reaching from just anterior to ventral sucker to ovary, follicles irregular in shape and size. Excretory pore terminal. Vesicle I-shaped, apparently reaching ventrally to testis. Remarks This new species has a unique, curved genital atrium reaching into the posterior forebody and then opening in the anterior hindbody. Other features distinguishing this species from the type- and only other species recognised in the genus here, O. carangis Yamaguti, 1952 are: length 776 1,151 vs 1,361 2,850; oesophagus 10 18% of body length vs 3 5%; ventral sucker to ovary distance 0 9% of body length vs 12 21%; and post-caecal distance 19 46% of body length vs 10 15%. In addition, the vitellarium in O. dinema reaches into the forebody. As far as we are aware, this is only the second digenean reported from this species of host, Stephanostomum noumeaense Bray & Justine, 2012 having recently been described by us from this host and locality (Bray & Justine, 2012). Opisthomonorchis carangis Yamaguti, Host: sp., Perciformes, Carangidae (close to C. talamparoides Bleeker). Site: Digestive tract. Locality: Nouméa Fish Market, New Caledonia (13/ 05/2011). Prevalence: 50% (1 out of 2 fish). 3 urn:lsid:zoobank.org:act:44bd324f-27b6-4e9a-8e85- E0DCA96F9C52. Voucher specimens: MNHN JNC3386, BMNH Description (Fig. 2; Table 1) [Based on 2 specimens.] Body small, narrow, elongate pyriform, widest in forebody. Tegument spined throughout, spines tiny. Eyespots pigment granules scattered at level of oesophagus. Oral sucker oval, subterminal. Ventral sucker rounded, slightly larger than oral sucker, in about mid-body. Prepharynx short, narrow. Pharynx oval. Oesophagus relatively short. Intestinal bifurcation in anterior forebody. Caeca narrow, run more or less parallel, termination posterior to testis. Testis single, oval, but somewhat flattened anteriorly, in posterior half of hindbody. Cirrus-sac oval, overlapping ovary posteriorly, reaching anteriorly to about half distance between ovary and ventral sucker. Internal seminal vesicle globular, in posterior third of cirrus-sac. Pars prostatica short, narrow, distinct gland-cell ducts feed into it. Ejaculatory duct wide, rectilinear, lined with long spines. Genital atrium long, rectilinear, with thick folded undulating walls, apparently unarmed but lined with narrow filamentous structures, Genital pore submedian, closely posterior to ventral sucker. Ovary rounded, distant from ventral sucker, pretesticular, close to testis. Mehlis gland postero-dorsal to ovary. Seminal receptacle uterine, posterior to testis. Laurer s canal opens dorsally to ovary. Uterus mostly post-testicular, reaches close to posterior extremity. Eggs numerous, small, asymmetrical, with short aporal filament. Metraterm slightly shorter than cirrus-sac, runs ventrally to cirrus-sac, enters base of genital atrium. Vitellarium follicular, in lateral fields reaching from just posterior to ventral sucker to mid-level of cirrus-sac, follicles relatively few, irregular in shape and size. Excretory pore terminal. Vesicle I-shaped, extent not detected. Type-host and locality: Caranx sp., Makassar, Sulawesi. Records References: 1. Yamaguti (1952); 2. Parukhin (1966); 3. Lebedev (1968); 4. Lebedev (1970); 5. Parukhin (1970); 6. Parukhin (1976); 7. Present study. Descriptions: 1,3,5,7. Definitive hosts: Perciformes: Carangidae: Caranx sp. (1); malabaricus (Bloch & Schneider)
4 150 Syst Parasitol (2013) 85:
5 Syst Parasitol (2013) 85: b Figs Opisthomonorchis dinema n. sp., Ventral view of holotype, uterus in outline, demarcation between cirrus-sac and genital atrium indicated by arrowhead; and egg. 2. Opisthomonorchis carangis Yamaguti, 1952, Ventral view, uterus in outline, and egg Pseudopisthomonorchis thapari (Varma & Singh, 1979) n. comb. 3. Ventral view, uterus in outline. 4. Lateral view of terminal genitalia. Scale-bars: 1, 2, 3 (worms), 200 lm; 1, 2 (eggs), 10 lm; 4, 100 lm (2, 3, 4, 6); plagiotaenia Bleeker (as Caranx compressus) (5); sp. (7); Carangidae gen. sp. (2, 6); Scomberoides lysan (Forsskål) (as Chorinemus lysan) (6); Pseudocaranx dentex (Bloch & Schneider) (as Caranx adsensionis) (6); Caranx sp. (6); Alectis indicus (Rüppell) (6). Distribution: Makassar, Sulawesi (1); South China Sea (2, 3, 4, 6); Red Sea (5); Masirah Bay (6); Sawquirah Bay (6); Gulf of Mannar (6); New Caledonia (7). Remarks We consider our specimens practically indistinguishable from Opisthomonorchis carangis as described by Yamaguti (1952). The genital atrium appears shorter in Yamaguti s illustration, but he describes it as lm long (c lm long for our specimens). Parukhin (1970) illustrated a worm he considered to be this species, but did not illustrate the genital atrium. Apart from the length (our specimens are shorter, 1,361 1,461 lm vs 1,750 2,850 lm), no metrical or ratio distinctions were detected. Genus Pseudopisthomonorchis Madhavi, As mentioned above, we consider the features distinguishing this genus from Opisthomonorchis to be the globular cirrus-sac and the band of vitelline follicles across the posterior forebody. We could not detect spines in the ejaculatory duct in the specimens described below, and it appears probable that members of Pseudopisthomonorchis have small spines or no spines in the ejaculatory duct; this is another feature which may distinguish this genus from Opisthomonorchis which has large, prominent ejaculatory duct spines. The type species, P. carangi Madhavi, 1974 is described as having an unspined cirrus, but the spacious genital atrium is armed with several rows of spines (Madhavi, 1974); a later description considers the cirrus spined (Hafeezullah & Dutta, 1999). Pseudopisthomonorchis hanumanthai Gupta & Singh, 1985 has a thick-walled cirrus (no spines mentioned) opening into spinose genital atrium (Gupta & Singh, 1985). Pseudopisthomonorchis secundus Ahmad, 1982 has a cirrus armed with bristle-like spines and a genital atrium with triradiate spines (Ahmad, 1982). In none of the descriptions do the spines appear as large as those in the ejaculatory duct of Opisthomonorchis spp. Pseudopisthomonorchis thapari (Varma & Singh, 1979) n. comb. 5 Syn. Opisthomonorchis thapari Varma & Singh, 1979 Host: chrysophrys (Cuvier), Perciformes, Carangidae, longnose trevally. Locality: Nouméa Fish Market, New Caledonia (21/ 07/2010). Site: Digestive tract. Prevalence: 67% (2 out of 3 fish). Voucher specimens: MNHN JNC3210D, JNC3210E, JNC3212, BMNH Description (Figs. 3 4, Table 1) [Based mainly on 2 specimens, 11 specimens examined.] Body small, elongate, narrow, more or less parallel-sided posterior to pharyngeal level (illustrated specimen slightly twisted on slide). Tegument spined, spines tiny, in annular rings, reaching to testis. Eyespot pigment in few spots anterior and posterior to pharynx. Oral sucker oval, small, subterminal. Ventral sucker oval, of similar size to oral sucker, in about mid-body. Prepharynx long, narrow. Pharynx oval. Oesophagus of similar length to prepharynx, narrow. Intestinal bifurcation in anterior forebody. Caeca narrow, closely parallel in forebody, termination not detected, obscured by eggs. Testis single, oval, but outline obscured by eggs, in anterior half of hindbody. Cirrus-sac oval, just overlapping testis posteriorly. Internal seminal vesicle oval, large. Pars prostatica narrow, surrounded by large prostatic cells. Ejaculatory duct short. Genital atrium narrow, in distinct sucker-like protuberance. Genital pore submedian, closely posterior to ventral sucker. 4 urn:lsid:zoobank.org:act:b4cad8ae-a1ef-45f1-851f-35 B4951BD1A0. 5 urn:lsid:zoobank.org:act:7d3e912d-fd7f-4c2f-a0da-76a 4DB68C7CA.
6 152 Syst Parasitol (2013) 85: Table 1 Measurements and ratios (with means in parentheses) for three opisthomonorchiines Species Opisthomonorchis dinema n. sp. Opisthomonorchis carangis Pseudopisthomonorchis thapari Host dinema sp. chrysophrys n Body length 776 1,150 (993) 1,361 1,461 1,318 1,438 Body width (140) Forebody length (421) Oral sucker ( ) Prepharynx length (43) Pharynx ( ) Oesophagus length () Intestinal bifurcation to ventral sucker (199) Pre-vitelline distance (389) Pre-genital pore distance (491) Pre-ovarian distance (524) Pre-testicular distance (597) 947 1, Long vitelline field length (162) Short vitelline field length (149) Ventral sucker ( ) Cirrus-sac ( ) Ventral sucker to ovary 0 93 (41) Ovary ( ) Ovary to testis 0 56 (12) Testis ( ) Post-testicular distance (298) Post-vitelline distance (440) Post-uterine distance (59) Post-caecal distance (401) ? Post-ovarian distance (411) Egg (19 9 9) Width (%)* (14.2) Forebody (%)* (42.5) Sucker length ratio 1: (1.70) 1: : Sucker width ratio 1: (1.54) 1: : Pharynx: oral sucker width ratio 1: (0.82) 1: : Oral sucker length (%)* (3.39) Pharynx length (%)* (2.54) Ventral sucker length (%)* (5.71) Oesophagus length (%)* (12.4) Pre-vitelline distance (%)* (39.3) Pre-genital pore distance (%)* (48.9) Pre-ovarian distance (%)* (51.3) Pre-testicular distance (%)* (59.4) Long vitelline field length (%)* (16.3) Ovary length (%)* (7.90)
7 Syst Parasitol (2013) 85: Table 1 continued Species Opisthomonorchis dinema n. sp. Opisthomonorchis carangis Pseudopisthomonorchis thapari Host dinema sp. chrysophrys n Ovary to testis(%)* (1.08) Testis length (%)* (9.96) Cirrus-sac length (%)* (24.6) Ventral sucker to ovary (%)* (3.57) Intestinal bifurcation to ventral sucker (%)** (47.0) Post-testicular distance (%)* (30.0) Post-vitelline distance (%)* (44.2) Post-uterine distance (%)* (5.98) Post-caecal distance (%)* (34.6) ? Post-ovarian distance (%)* (40.7) Prepharynx (%)* (4.30) * (%) of body length; ** (%) of forebody length Ovary rounded, pre-testicular, overlapping testis. Mehlis gland, uterine seminal receptacle and Laurer s canal obscured by eggs. Uterus mostly posterior to ovary, reaches close to posterior extremity. Eggs numerous, small, with distinct aporal filament of similar length to egg; eggs in whorls typical of filamented eggs. Metraterm narrow distally, length not clear. Vitellarium follicular, often appears as single field, but could be interpreted as two confluent or closely adjacent fields, in posterior forebody; follicles relatively few, highly irregular in shape and size. Excretory pore terminal. Vesicle I-shaped, extent not detected. Type-host and locality: Caranx armatus (Cuv. & Val.) [presumably armatus (Rüppell)], Arabian Sea off Quilon, India. Records: 1. Varma & Singh (1979); 2. Present study. Descriptions: 1,2. Definitive hosts: armatus (1); C. chrysophrys (2). Distribution: Arabian Sea off Quilon, India (1); New Caledonia (2). Remarks Unfortunately, most specimens are not in good condition and we could not distinguish the posterior extent of the caeca, but the other characters are very similar to those described by Varma & Singh (1979) for O. thapari. Hafeezullah (1984) considered this species synonymous with P. carangi, which he placed in Opisthomonorchis. We agree that these forms are similar, but think they may be distinguishable by body length, sucker width ratio, possibly forebody length [maximum measurements in Madhavi (1974) are clearly in error, being the same for both forebody and total body length], pre-vitelline distance and postvitelline distance (Table 2). These characters may not represent a sustainable distinction when the true variation in these species is known, but data to hand indicate these distinctions. However, the considerable variation found between the two specimens we have measured should be noted. Varma & Singh (1979) described the cirrus (= ejaculatory duct) and genital sinus (= atrium) as spined, but we could detect neither in our specimens. These spines are not detectable on the original illustration, so they must be very small. Details of other Pseudopisthomonorchis spp. Pseudopisthomonorchis carangi Madhavi, 1974 Syn. Opisthomonorchis carangi (Madhavi, 1974) Hafeezullah, 1984 Type-host and locality: malabaricus (Bloch & Schneider), Perciformes, Carangidae, Malabar trevally; Waltair coast, Bay of Bengal.
8 154 Syst Parasitol (2013) 85: Table 2 Tabular key to the species of the opisthomonorchiine genera Opisthomonorchis and Pseudopisthomonorchis Species/Feature O. dinema n. sp , : Present study O. carangis 1,361 1, : Present study O. carangis 1,750 2, : Yamaguti (1952) O. carangis 1, : ? Parukhin (1970) O. carangis 2, : Lebedev (1968) P. thapari 1,318 1, : ? Present study P. thapari 1,900 2, : Varma & Singh (1979) P. carangi 1,220 1, : * ? Madhavi (1974) P. carangi 1,220 2, Hafeezullah & Dutta (1999) P. hanumanthai 940 1, : Gupta & Singh (1985) P. secundus 2,320 2, : Ahmad (1982) Key to the features 1. Body length; 2. Body width as % of body length; 3. Sucker width ratio; 4. Prepharynx as % of body length; 5. Oesophagus as % of body length; 6. Forebody as % of body length; 7. Pre-vitelline distance as % of body length; 8. Length of vitelline fields as % of body length; 9. Distance between ventral sucker and ovary as % of body length; 10. Post-testicular distance as % of body length; 11. Post-vitelline distance as % of body length; 12. Post-uterine distance as % of body length; 13. Post-caecal distance as % of body length; 14. Egg size * These data are based partly on metric information in the description and partly on measurements of the illustration. The upper extent of the range of forebody length given in the description coincides with the maximum length of the worm, clearly an error
9 Syst Parasitol (2013) 85: References: 1. Madhavi (1974); 2. Hafeezullah (1984); 3. Hafeezullah & Dutta (1999). Descriptions: 1,3. Host: malabaricus (1, 2, 3). Distribution: Waltair coast, Bay of Bengal (1); Bombay, Arabian Sea (2); West Bengal (Digha, District Medinipur); Andhra Pradesh, Kerala and Maharashtra coasts (3). Remark This species is compared with O. thapari above. Pseudopisthomonorchis hanumanthai Gupta & Singh, 1985 Type- and only host and locality: malabaricus (Bloch & Schneider), Perciformes, Carangidae, Malabar trevally; Puri coast, Bay of Bengal. Reference, description: Gupta & Singh (1985). Remark This species is distinct in the long prepharynx and very long oesophagus (Table 2). Pseudopisthomonorchis secundus Ahmad, 1982 Type- and only host and locality: Platax teira (Forsskål), Perciformes, Ephippidae, roundface batfish; Bombay, Arabian Sea. Reference, description: Ahmad (1982). Remark This species, the only opisthomonorchiine described so far from a non-carangid host, is distinct in several features, most notably the width of the body, the sucker ratio, the lack of prepharynx, the short forebody and pre-vitelline distance, the long post-vitelline distance and large eggs (Table 2). Acknowledgements Bernard Marchand helped in some fish examinations. Bernard Séret and Samuel Iglésias (Muséum National d Histoire Naturelle, Paris) and Ronald Fricke (Staatliches Museum für Naturkunde, Stuttgart) helped in the identification of fishes. References Ahmad, J. (1982). Studies on digenetic trematodes of the families Monorchiidae and Lepocreadiidae from marine fishes of India. Kanpur University Research Journal (Science), 1, Bray, R. A., & Justine, J.-L. (2012). Further reports of Acanthocolpidae Lühe, 1906 (Digenea) from fishes off New Caledonia, with descriptions of two new species. Systematic Parasitology, 83, Cribb, T. H., & Bray, R. A. (2010). Gut wash, body soak, blender, and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Systematic Parasitology, 55, Fricke, R., Kulbicki, M., & Wantiez, L. (2011). Checklist of the fishes of New Caledonia, and their distribution in the Southwest Pacific Ocean (Pisces). Stuttgarter Beiträge zur Naturkunde Serie A (Biologie), 4, Froese, R., & Pauly, D. (2012). FishBase. World Wide Web electronic publication. Available on Gupta, P. C., & Singh, R. B. (1985). Studies on digenetic trematodes of the families Monorchiidae and Hemiuridae from marine fishes of Puri coast, Bay of Bengal. Kanpur University Research Journal (Science), 2(1981), Hafeezullah, M. (1984). On the status of some digenetic trematodes of marine fishes of India. Bulletin of the Zoological Survey of India, 6, Hafeezullah, M., & Dutta, I. B. (1999). Digenetic trematodes of fishes. Zoological Survey of India, State Fauna Series 3: Fauna of West Bengal, 11, Lebedev, B. I. (1968). [Helminth fauna of carangid fish in the Pacific Ocean]. Soobshcheniya Dal nevostchnogo Filiala im. B.L. Komarova Akademii Nauk SSSR, 26, (In Russian). Lebedev, B. I. (1970). [Helminths of fish of the South China Sea]. In: Oshmarin, P. G., Mamaev, Y. L. & Lebedev, B. I. (Eds) [Helminths of animals in south-eastern Asia]. Moscow: Nauka, pp (In Russian). Madhavi, R. (1974). Digenetic trematodes from marine fishes of Waltair Coast, Bay of Bengal. Family Monorchiidae. Rivista di Parassitologia, 35, Madhavi, R. (2008) Family Monorchiidae Odhner, In: Bray, R.A., Gibson, D.I. & Jones, A. (Eds) Keys to the Trematoda. Volume 3. Wallingford: CABI Publishing and The Natural History Museum, pp Moravec, F., & Justine, J.-L. (2010). Some trichinelloid nematodes from marine fishes off New Caledonia, including description of Pseudocapillaria novaecaledoniensis sp. nov. (Capillariidae). Acta Parasitologica, 55, Parukhin, A. M. (1966). [Helminth fauna of carangid fish from the South China Sea]. Biologiya Morya, Kiev [Helminth fauna of animals in southern seas], (In Russian). Parukhin, A. M. (1970). [On the study of trematode fauna in fish from the Red Sea and Aden Bay]. Biologiya Morya, Kiev, 20, (In Russian). Parukhin, A. M. (1976). [Parasitic worms of food fishes of the southern Seas]. Kiev: Naukova Dumka, 183 pp. (In Russian).
10 156 Syst Parasitol (2013) 85: Smith-Vaniz, W.F. (1999) Carangidae. In: Carpenter, K. E. & Niem, V. H. (Eds) FAO species identification guide for fishery purposes. The living marine resources of the Western Central Pacific. Volume 4. Bony fishes part 2 (Mugilidae to Carangidae). Rome: FAO, pp Varma, P. K., & Singh, J. P. (1979). Opisthomonorchis thapari n. sp. from a marine fish Caranx armatus (Cuv. and Val.) from the Arabian Sea at Quilon, India. Indian Journal of Zootomy, 20, Yamaguti, S. (1952). Parasitic worms mainly from Celebes. Part 1. New digenetic trematodes of fishes. Acta Medicinae Okayama, 8,
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