Parasitol Res (2013) 112:3981–3989 DOI 10.1007/s00436-013-3642-6
ORIGINAL PAPER
Lepidapedon sereti n. sp. (Digenea: Lepidapedidae) in Coelorinchus sereti (Gadiformes: Macrouridae) from deep waters off Vanuatu Rodney A. Bray & Elisabeth Faliex & Jean François Allienne & Gabriel Mouahid
Received: 30 May 2013 / Accepted: 7 August 2013 / Published online: 8 November 2013 # Springer-Verlag Berlin Heidelberg 2013
Abstract Lepidapedon sereti n. sp. is described from the macrourid Coelorinchus sereti from the deep water off Vanuatu. It is placed in the Elongatum group and Elongatum subgroup. It differs from the other species described in this subgroup by the distinctly dorsally subterminal excretory pore. It also differs from other species in combinations of size, excretory vesicle length, proportions of forebody, posttesticular region and other metric features. This constitutes the first record of a Lepidapedon (sensu stricto) from the Central Western Pacific Ocean.
Introduction Lepidapedon Stafford, 1904 is a large genus, mainly of deepwater fish parasites, with a distinct predilection for gadiforms. According to Bray and Gibson (1995), 61 % of records were from gadiforms, with the families Gadidae (35 %) and Macrouridae (22 %) as the most frequently reported host families. Most of the gadid records are of a few relatively shallow-water species, but the macrourids harbour many distinct species. Bray et al. (1999) presented phylogenetic R. A. Bray (*) Department of Life Sciences, Natural History Museum, Cromwell Road, SW7 5BD London, UK e-mail: [email protected] E. Faliex : J. F. Allienne : G. Mouahid Université de Perpignan, Via Domitia, 52, Avenue Paul Alduy, 66860 Perpignan Cedex, France E. Faliex UMR 5110, CEFREM, CNRS, 52, Avenue Paul Alduy, 66860 Perpignan Cedex, France J. F. Allienne UMR 5244, Ecologie et Evolution des Interactions, CNRS, 52, Avenue Paul Alduy, 66860 Perpignan Cedex, France
estimates inferred from LSU rDNA and ND1 mtDNA sequences, indicating that this genus probably radiated in the deep sea and has encroached into shallower waters in relatively few cases. They considered Lepidapedon to be ‘the most common deep-water digenean genus’, a conclusion which Blend et al. (2000) found to be supported by their findings. Bray (2004) illustrated the bathymetry of deep-water digeneans and showed further data to support this assertion, pointing out that two species, namely Lepidapedon discoveryi Bray and Gibson, 1995 and Lepidapedon beveridgei Campbell and Bray, 1993 had been reported from the northeastern Atlantic abyssal plain at nearly 5,000 m in depth. Lepidapedon has, until recently, been considered a member of the family Lepocreadiidae Odhner, 1905, but molecular estimates of its relationships by Bray et al. (2009) have shown that the family is polyphyletic and Bray and Cribb (2012) suggested that the subfamily Lepidapedinae Yamaguti, 1958 should be raised to family level to better reflect the relationships in the superfamily. This is supported not only by molecular results but also by morphology and biology (Bray et al. 2009; Bray and Cribb 2012).
Material and methods Material was collected in October 1994 during a trawling operation in Vanuatu near the islands of Espiritu Santo (sampling site 15°48.42′S; 167°24.27′E; depth of 775– 798 m). Digenean (a total of three worms) were removed from the digestive tract of a single female specimen of macrourid (female Coelorinchus sereti Iwamoto and Merrett, 1997; standard length 470 mm) and fixed in Bouin's solution (Langeron 1949). Whole mounts (two specimens) were stained with Grenacher's boric acid alcohol-based carmine solution (Langeron 1949) and mounted in Canada balsam. Sections (from one specimen) were cut using a manual
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microtome at 6 μm and stained with Heidenhain's azan (Heidenhain 1915). 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.
posterior extremity of external seminal vesicle or just posterior, confluent in post-testicular region; fields may be slightly interrupted at level of gonads, but not on both sides and not consistently; lateral, ventral and dorsal to caeca. Excretory pore on dorsal surface (Figs. 6 and 7); vesicle reaches dorsally to posterior testis and to posterior edge of anterior testis.
Results
Taxonomic summary
Superfamily Lepocreadioidea Odhner, 1905 Family Lepidapedidae Yamaguti, 1958 Genus Lepidapedon Stafford, 1904 urn:lsid:zoobank.org:act:CBDC3DD9-F745-4CE1-B752955EA2C97B80 Syn. Lepodora Odhner, 1905
Type host: Coelorinchus sereti Iwamoto and Merrett, 1997, female Type locality: Vanuatu, island of Espiritu Santo (15°48.42′S; 167°24.27′E) Deposition of specimens: Museum National d'Histoire Naturelle Paris, France. Holotype MNHN HEL346, paratype MNHN HEL347–357 (11 slides of serial sections); Natural History Museum, London, England, paratype 2013.8.22.1. Etymology: The specific name refers to Dr Bernard Séret (Institut de Recherche pour le Développement (IRD), Museum National d'Histoire Naturelle, Paris, France), in recognition of his expertise in fish taxonomy.
Lepidapedon sereti n. sp. (Figs. 1, 2, 3, 4, 5, 6, 7, 8, and 9; Table 1) urn:lsid:zoobank.org:act:FB9E1567-8787-4EB3-A6ECC53519017F20 Description is based on two whole-mounted specimens and one set of serial sections; the measurements are shown in Table 1. Body elongate linguiform (Figs. 1 and 4). Tegument finely spined, becoming sparser in hindbody, none beyond level of testes. Neither eye spots nor eye-spot pigment seen. Oral sucker small, subglobular, subterminal. Ventral sucker oval, slightly smaller than oral sucker, in anterior quarter of body. Prepharynx long. Pharynx small, oval. Oesophagus long, narrow. Intestinal bifurcation in mid forebody. Caeca narrow, end blindly anterior to excretory pore (Fig. 6), termination may be amongst dense patches of vitelline follicles. Testes two, oval, entire, tandem, separated, in anterior part of posterior half of hindbody. External seminal vesicle elongate sigmoid, reaches about quarter of distance to ovary; surrounded by membrane-bound gland cell mass which narrows anteriorly forming narrow neck before male duct enters cirrus sac (Figs. 2, 5 and 9). Cirrus sac narrow claviform, mainly dorsal to ventral sucker. Internal seminal vesicle gently undulating, narrow. Pars prostatica oval, vesicular (Figs. 2, 5 and 8). Ejaculatory duct short, extended to form short cirrus. Genital atrium distinct. Genital pore sinistral, submedian, at level just anterior to ventral sucker. Ovary oval to weakly trilobate, pretesticular with distinct gap. Laurer's canal long, opens dorsally lateral to left caecum at level of anterior part of ovary (Fig. 3). Seminal receptacle elongate saccular, mainly postero-dorsal to ovary. Mehlis' gland dorsal to ovary. Uterus mainly intercaecal, preovarian, almost entirely in hindbody, runs ventrally to external seminal vesicle. Eggs tanned operculate. Metraterm of similar length to cirrus sac, wall weakly muscular. Vitellarium follicular, anterior extent of follicular field in hindbody, at about 26– 31 % of distance from ventral sucker to ovary, at level of
Discussion This species is a fairly typical member of the genus but is particularly large, and the excretory pore is distinctly dorsal. Initial observations on whole mounts suggested that a cyclocoel (i.e. the caeca unite close to the posterior end of the body) might be present, but sections showed that the caeca terminate blindly. In the whole mounts, the terminations are not easy to see as they occur amongst dense bunches of vitelline follicles. The feature giving the superficial appearance of a cyclocoel is two concentric irregular patches of stained tissue (Fig. 7). The genus Lepidapedon now has over 50 recognised species, although the status of some is doubtful. Bray and Gibson (1995) and Blend et al. (2000) have summarised our knowledge on the genus, with only one species, Lepidapedon alvigae Tkachuk, 2002, having been named since. This latter species is a renaming by Tkachuk (2002) of Tormopsolus coelorhynchi Gavrilyuk-Tkachuk, 1979, which, if considered a Lepidapedon, as suggested by Bray (1995), is preoccupied by Lepidapedon coelorhynchi Yamaguti, 1938. Multivariate analysis of measurements (Bray and des Clers 1992) and molecular studies (Bray et al. 1999, 2009) indicate that although many species are similar morphologically, there are numerous species, particularly in the deep sea. Bray and Gibson (1995) divided the genus into three groups, each separated into subgroups, for some of which they supplied keys. These keys were extended and updated by Blend et al. (2000). The characters of these groups and
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Figs. 1–3 L. sereti n. sp. 1 Ventral view of holotype, uterus in outline. 2 Terminal genitalia, viewed from ventral plane. 3 Proximal female genitalia, viewed from ventral plane. ca, caecum; cs, cirrus sac; e, egg; esv, external seminal vesicle; gp, Genital pore; gs, glandular sheath; isv, internal seminal vesicle; Lc, Laurer's canal; Mg, Mehlis' gland; od, oviduct; ov, ovary; pecs, posterior extent of cirrus sac; pp, pars prostatica; sr, seminal receptacle; ut, uterus; vr, vitelline reservoir; vs, outline of ventral sucker. Scale bars: 1, 1,000 μm; 2, 3, 200 μm
subgroups and the currently recognised species in these groups are summarised in Table 2. The species L. sereti n. sp. fits into the ‘Elongatum group’, where the vitellarium does not reach to the ventral sucker. It fits into the Subgroup i (Elongatum subgroup) in which the excretory vesicle reaches to about the level of posterior margin of the anterior testes. Unfortunately, due to the morphological similarity of many of the species in this subgroup, a key was not produced. The subgroup was considered by Bray and Gibson (1995) to contain eight species, and two have been added subsequently, Lepidapedon ninae Zdzitowiecki and Cielecka, 1997 and Lepidapedon mexicanensis Blend, Dronen and Armstrong, 2000.
L. sereti n. sp. is distinguished from other members of the subgroup and possibly from all described species by its dorsally situated excretory pore. In addition, it is unusually large; only L. discoveryi and, possibly, L. coelorhynchi grow to a similar size. Species in the ‘Elongatum group, Elongatum subgroup’ category are all superficially similar, such that, as stated above, a key to them was not produced by Bray and Gibson (1995). Also two new species have been added since, making it necessary to compare all of the species in this subgroup with L. sereti n. sp. The differentiating features of biology and morphology are discussed below.
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Figs. 4–9 L. sereti n. sp. 4 Whole mount of holotype. 5 Ventral view of terminal genitalia. 6 Sagittal section of posterior part of worm showing caecal extent and dorsal position of excretory pore. 7 Posterior extremity of worm showing posterior vitelline follicles, excretory pore and concentric stained patches of tissue around excretory pore. 8 Sagittal section showing cirrus sac. 9 Sagittal section showing external seminal vesicle and membrane-bound glandular sheath. c, caecum; cs, cirrus sac; dm, delimiting membrane; d, dorsal surface; ep, excretory pore; esv, external seminal vesicle; ev, excretory vesicle; gs, glandular sheath; isv, internal seminal vesicle; mt, metraterm; pecs, posterior extent of cirrus sac; sp, stained patches; v, ventral surface; vf, vitelline follicle; vs, ventral sucker. Scale bars: 4, 1,000 μm; 5, 6, 7, 8, 9, 200 μm
Lepidapedon elongatum (Lebour, 1908) sensu stricto is generally considered to be one of the two common members of the genus found in north Atlantic shallow-water gadids, particularly the cod Gadus morhua Linnaeus, 1758 (the other species is Lepidapedon rachion (Cobbold, 1858), which is mostly found in the haddock Melanogrammus aeglefinus (Linnaeus, 1758)). Perdiguero-Alonso et al. (2008) studied cod from six areas in the waters of Iceland, the British Isles and Scandinavia and found cod infected with L. elongatum at
all sites, although prevalences were low in the Baltic Sea. Overall, the prevalence was 60 %. Appy and Burt (1982) found localities off eastern Canada where prevalence reached 100 %, with intensities up to 2,916 and Køie (1984) found over 90 % prevalence in Danish waters. Recent records of L. elongatum (and its synonym L. microcotyleum Odhner in Dollfus, 1953) from morids and macrourids from deep waters off Japan by Kuramochi (2009) should be treated with caution (see Lepidapedon gadi below). Bray and Gibson (1995)
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Table 1 Dimensions and ratios of Lepidapedon sereti n. sp.
Table 1 (continued)
Species Host Locality n
Pre-vitelline distance % Anterior testis length % Posterior testis length %
Length
Lepidapedon sereti Coelorhynchus sereti Vanuatu 2 Holotype Paratype 8,192 8,406
Width Forebody Preoral lobe Oral sucker length Oral sucker width Prepharynx Pharynx length Pharynx width Oesophagus Intestinal bifurcation to ventral sucker Vitellarium to ventral sucker Ventral sucker length Ventral sucker width Cirrus sac length Cirrus sac width External seminal vesicle reach into hindbody Ventral sucker to ovary Ovary length
963 1,765 14 230 249 216 145 121 365 800 636 227 227 325 119 613 2,404 382
1,051 1,675 46 253 249 148 139 117 292 784 729 217 220 289 101 548 2,282 389
Ovary width Ovary to anterior testis Anterior testis length Anterior testis width Distance between testes Posterior testis length Posterior testis width Post-testicular distance Post-caecal distance Egg length Egg width Width % Forebody % Sucker length ratio 1: Sucker width ratio 1: Oral sucker: pharynx width 1: Ventral sucker to ovary % External seminal vesicle reach into hindbody %a Post-testicular distance % Oesophagus % Intestinal bifurcation to ventral sucker % Vitellarium to ventral sucker % Ovary to anterior testis % Distance between testes % Cirrus sac length % Pre-vitelline distance
365 126 474 438 428 390 434 2,166 603 65–70 (67) 30–38 (34) 11.8 21.5 0.99 0.91 2.05 29.3
325 194 339 312 427 482 414 2,434 646 60–71 (65) 29–41 (35) 12.5 19.9 0.86 0.88 2.13 27.2
25.5
24.0
26.4 4.45 9.76 7.76 1.54 5.22 3.97 2,401
29.0 3.47 9.33 8.67 2.30 5.08 3.44 2,403
29.3 5.79 4.77
28.6 4.04 5.73
Percentages are of total body length a
Ventral sucker to ovary distance
redescribed the species based solely on material from north Atlantic cod. The greatest length reported was 3,970 μm, much shorter than that found for L. sereti n. sp. In addition to the size, the terminal position of the excretory pore and the usual presence of a pseudoesophagus distinguish this species from L. sereti n. sp. The forebody is usually relatively longer (21–33 % of body length), and the male terminal genitalia are much less elongate in L. elongatum; the ventral sucker is usually slightly larger than the oral (sucker width ratio mean 1:1.04), the vitelline follicles are fewer but relatively larger, and the post-testicular distance is shorter (10–18 % of body length). Lepidapedon arlenae Bray and Gibson, 1995 is known from the macrourids the roughsnout grenadier Trachyrincus scabrus (Rafinesque, 1810), the roughnose grenadier Trachyrincus murrayi Günther, 1887 and the spearsnouted grenadier Coelorinchus labiatus (Köhler, 1896) found at moderate depths (down to 1,800 m) from the eastern North Atlantic Ocean from the Bay of Biscay to north of Scotland (Bray and Gibson 1995; Bray and Kuchta 2006). This is a relatively small worm, reaching 3,568 μm. The excretory pore is terminal. The intestinal bifurcation is in the posterior forebody. It is said to have no vitelline follicles dorsal to the caeca. L. coelorhynchi Yamaguti 1938 was originally described from Coelorinchus [as Coelorhynchus ] sp. off Japan (Yamaguti 1938). The maximum size (3,600 μm) in the original description is much less than that of L. sereti n. sp. (8,406 μm); it is wider (width 15–16 % of body length), the ventral sucker is larger (sucker width ratio is about 1:1.14), the forebody is longer (about 28 % of the body length), the ventral sucker to ovary distance is shorter (about 24 % of the body length) and the post-testicular distance is shorter (about 22 % of body length). The excretory pore is illustrated as terminal. This species has subsequently been reported several times from the macrourids Coelorinchus gilberti Jordan and Hubbs, 1925; the Mugura grenadier Coelorinchus kishinouyei Jordan and Snyder, 1900; the giant grenadier Albatrossia [as Coryphaenoides] pectoralis (Gilbert, 1892); and the morid Laemonema filodorsale Okamura, 1982 (Kuramochi 2005, 2006, 2009, 2011). There must be some doubt as to the conspecificity of all these forms as Kuramochi (2005) gave a maximum size of 9,430 μm and Kuramochi (2009) gave 14, 600 μm. In neither paper were illustrations included, and in the latter, only the body size was quoted. Kuramochi (2005)
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Table 2 Groups, subgroups, characters and species of Lepidapedon Group
Characters
Rachion group Vitellarium reaches to about the ventral sucker level.
Elongatum group
Subgroup
Characters
Included species
Rachion subgroup
Excretory vesicle not reaching further anterior than about middle of posterior testis
L. rachion (Cobbold, 1858) L. abyssensis McCauley, 1968 L. aljoshkinae Gaevskaja, 1983 L. cambrensis Srivastava, 1966 L. cascadensis McCauley, 1968 L. desotoensis Blend, Dronen and Armstrong, 2000 L. genge Yamaguti, 1938 L. lebouri Manter, 1934 L. luteum Yamaguti, 1938 L. paralebouri Zdzitowiecki, 1990 L. zaniophori Blend, Dronen and Armstrong, 2000 L. sommervillae Bray and Gibson, 1995
Sommervillae Excretory vesicle reaches subgroup to the anterior testis Vitellarium not reaching Elongatum subgroup Excretory vesicle reaches to ventral sucker to about the level of posterior margin of the anterior testes
Desclersae subgroup Excretory vesicle reaches to about level of posterior margin of posterior testis
Ostorhinchi subgroup
Subgroup IV
L. elongatum (Lebour, 1908) L. arlenae Bray and Gibson, 1995 L. coelorhynchi Yamaguti, 1938 L. discoveryi Bray and Gibson, 1995 L. gadi (Yamaguti, 1934) L. gaevskayae Campbell and Bray, 1993 L. mariannae Bray and Gibson, 1995 L. merretti Campbell and Bray, 1993 L. mexicanensis Blend, Dronen and Armstrong, 2000 L. ninae Zdzitowiecki and Cielecka, 1997 L. sereti n. sp. L. desclersae Bray and Gibson, 1995 L. antimorae McCauley, 1968 L. australis Manter, 1954 L. blairi Bray and Jones, 1993 L. brayi Zdzitowiecki and Cielecka, 1997
L. filiformis McCauley, 1968 L. lepidum Gaevskaja and Rodyuk, 1988 L. nezumiatis Blend, Dronen and Armstrong, 2000 L. oregonensis MeCauley, 1968 L. taeniatum Gaevskaja and Rodyuk, 1988 L. yaquina McCauley, 1968 L. megalaspi Parukhin, 1966 incertae sedis L. sphyraenae Shen, 1990 incertae sedis Excretory vesicle reaches The only species placed in this subgroup, to about level of ovary L. ostorhinchi Korotaeva, 1974, is now considered a member of the genus Paralepidapedon Shimazu and Shimura, 1984 by Bray and Cribb (1997) Excretory vesicle not described L. alvigae Tkachuk, 2002 L. clavatum Linton, 1940 L. gymnacanthi (Issaitschikov, 1928) L. sammari Abdel Aal, Banaja and Al Zanbagi, 1985 incertae sedis L. spiniferi Abdel Aal, Banaja and Al Zanbagi, 1985 incertae sedis
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Table 2 (continued) Group
Characters
Garrardi group Vitellarium reaches at least to intestinal bifurcation
Subgroup
Characters
Included species
Garrardi subgroup
Excretory vesicle reaching close to the level of the posterior margin of the posterior testis
L. garrardi (Leiper and Atkinson, 1914) L. calli Acena, 1947 L. carcini Mordvinova, 1985
Beveridgei subgroup
Congeri subgroup
Subgroup IV
L. guevarai Lopez-Roman and Maillard, 1973 L. zubchenkoi Campbell and Bray, 1993 Excretory vesicle reaches L. beveridgei Campbell and Bray, 1993 to the level of the posterior L. balgueriasi Zdzitowiecki and margin of the anterior testis Cielecka, 1997 or further into the region L. notogeorgianus Zdzitowiecki, 1990 between the testes L. tertius Zdzitowiecki, 1990 Excretory vesicle reaching L. congeri Manter, 1954 into the forebody to about L. caribbaei Blend, Dronen and the level of the intestinal Armstrong, 2000 bifurcation L. longivesicula Blend, Dronen and Armstrong, 2000 Excretory vesicle not described L. golphick Oshmarin, 1968
described the excretory pore as subterminal but did not mention the extent of the vesicle. Using the body-size data in these two papers, the width is 13–19 % of the body length, somewhat greater than that of L. sereti n. sp. L. discoveryi Bray and Gibson, 1995 is known only from the macrourid abyssal grenadier Coryphaenoides armatus (Hector, 1875) from the eastern North Atlantic and is found over a wide range of depths, from 2,550 to 4, 850 m, i.e. it can be abyssal (Bray and Gibson 1995). This is a large worm, of similar dimensions to L. sereti n. sp., known to attain a length of 9,304 μm. The excretory pore is terminal. The excretory vesicle is rather shorter than is usual in this subgroup (although not short enough to fit the species into the Desclersae subgroup). It ‘usually reaches to level of middle of posterior testis, occasionally may reach just anterior to posterior margin of posterior testis or just anterior to anterior margin of posterior testis (not reaching close to anterior testis)’ (Bray and Gibson 1995). L. gadi (Yamaguti, 1934) Yamaguti 1938 sensu stricto was considered to be restricted to the Pacific cod Gadus macrocephalus Tilesius, 1810 from the North Pacific Ocean by Bray and Gibson (1995). If this is the case, then only the original description can be considered for comparison (Yamaguti 1934). The worm is of moderate size, reaching a maximum length of 5,800 μm, but the excretory pore is terminal, the forebody is longer (about 27 % of the body length) and the post-testicular distance is shorter (about 16 % of the body length). A pseudoesophagus is reported as ‘posterior part [of the oesophagus] lined by the intestinal epithelium’ (Yamaguti 1934). This appears to be a shallowwater form. This name has been used for worms from G.
morhua in northern European waters, which were considered L. elongatum by Bray and Gibson (1995). Lepidapedon gaevskayae Campbell and Bray, 1993 is known only from C. armatus from the western and eastern North Atlantic (Campbell and Bray 1993; Bray and Gibson 1995). Its maximum known length is 4,300 μm, and the excretory pore is terminal. The worm is narrower (width 7– 10 % body length), with a shorter post-testicular distance (11– 20 % of body length). The intestinal bifurcation is well into the posterior part of the forebody. The ventral sucker is smaller, with a sucker width ratio of 1:0.68–0.86. Although this species is reported from a fish species which is often recovered from abyssal depths, it has only been reported to 2,890 m (cf. L. discoveryi from the same host species). Lepidapedon mariannae Bray and Gibson, 1995 is known only from the lotid Arctic rockling Gaidropsarus argentatus (Reinhardt, 1837), from moderate depths (to 1,110 m) in waters to the north of Scotland to the Faroes (Bray and Gibson 1995; Køie 2000). It is a moderately sized worm, up to 4, 960 μm long. The excretory pore is terminal. The anterior extent of the vitellarium overlaps the posterior margin of the external seminal vesicle, occasionally reaching to the ventral sucker. A pseudoesophagus may be present. Lepidapedon merretti Campbell and Bray, 1993 is known only from the phycid longfin hake Phycis chesteri Goode and Bean, 1878, from relatively shallow depths (to 786 m) in the Hudson Canyon, western North Atlantic (Campbell and Bray 1993). It is a small worm, only reaching 2,780 μm in length. It is broader (width 14–27 % of body length); the forebody is longer (18–31 % of body length), and the ventral sucker to ovary distance is smaller (14–23 % of body length), as is the post-testicular distance (10–22 % of body length). The
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excretory pore is terminal, and the vitellarium may reach virtually to the ventral sucker. L. mexicanensis Blend, Dronen and Armstrong, 2000 is known from the macrourids the hollowsnout grenadier Coelorinchus caelorhincus (Risso, 1810), the carmine grenadier Coryphaenoides carminifer (Garman, 1899) and the thickbeard grenadier Coryphaenoides zaniophorus (Vaillant, 1888) from the northern Gulf of Mexico (Blend et al. 2000). This is a small worm, reaching only 1,809 μm in length, and the excretory pore is terminal. It is wider (width 14–33 % of body length) and has a shorter ventral sucker to ovary distance (11–26 % of body length). The intestinal bifurcation is in the posterior forebody. L. ninae Zdzitowiecki and Cielecka, 1997 is known only from Whitson's grenadier Macrourus whitsoni (Regan, 1913) from the Weddell Sea in western Antarctica (Zdzitowiecki and Cielecka 1997). The species is based on one specimen of 3, 310 μm in length. The original authors pointed out that, in some characteristics, it resembles the Rachion group worms (long prepharynx, short oesophagus). The excretory pore is terminal. Its eggs are larger (91–102 × 40–46 μm), the forebody is longer (33 % of body length), and the distance from the ventral sucker to ovary is shorter (about 17 % of body length). Several other Lepidapedon species have been reported from Coelorinchus spp. (under various spellings of the host generic name). These are L. rachion (Cobbold, 1858), L. alvigae Tkachuk, 2002, Lepidapedon australis Manter, 1954, Lepidapedon blairi Bray and Jones, 1993, Lepidapedon caribbaei Blend, Dronen and Armstrong, 2000 and Lepidapedon longivesicula Blend, Dronen and Armstrong, 2000. L. rachion (Cobbold, 1858) was reported in Coelorinchus sp. from Tortugas, Florida (Manter 1931), and the longnose grenadier Coelorinchus carminatus (Goode, 1880) from the same locality at 200–315 fathoms (366–576 m) by Manter (1934). L. rachion is the type species of the genus and is considered by Bray and Gibson (1995) to be a shallowwater species with a distinct predilection for the haddock M. aeglefinus . Manter's records were not included amongst those of L. rachion sensu stricto by Bray and Gibson (1995). This form is easily distinguished from of L. sereti n. sp. by its broad shape and the vitellarium reaching into the forebody. L. alvigae Tkachuk 2002 (syn. T. coelorhynchi GavrilyukTkachuk, 1979) was reported from the banded whiptail Coelorinchus fasciatus (Günther, 1878) from the Agulhas Bank in the Indian Ocean (Gavrilyuk-Tkachuk 1979). The worm is of moderate size, reaching a maximum of 4,140 μm in length. The excretory vesicle is not described, but the pore appears terminal in the illustration. The forebody is longer (about 31 % of body length), and the post-testicular distance is shorter (about 17 % of body length). Nevertheless, the worm clearly belongs in Lepidapedon.
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L. australis Manter, 1954 is known only from the javelin Coelorinchus australis (Richardson, 1839) off Wellington in the North Island of New Zealand (Manter 1954). This is a fairly large worm reaching up to 6,536 μm in length. Its excretory vesicle is short, extending only to the posterior testis, causing it to be placed in the Desclersae subgroup by Bray and Gibson (1995). It has a long forebody, originally described as a little less than half the body length (about 36– 39 % of body length using the data given in the description). The distance of the ventral sucker to ovary is shorter (about 19 % of body length), the post-testicular distance is shorter (18–19 % of body length), and the eggs are larger (80–92× 55–65 μm). The ventral sucker is always slightly larger than the oral sucker (sucker width ratio 1:1.03–1.30). L. blairi Bray and Jones, 1993 is known from Bollons' rattail Coelorinchus bollonsi McCann and McKnight, 1980 at a relatively shallow depth (570 m) from Chatham Rise off New Zealand (Bray and Jones 1993) and from the rough-head whiptail Coelorinchus aspercephalus Waite, 1911 in relatively shallow (495 m) waters just off the southern end of New Zealand (Bray and Gibson 1995). It is a moderately sized worm (up to 5,000 μm in length). Its short excretory vesicle places this species in the Desclersae subgroup. It is easily distinguished from most Lepidapedon species by the anterior extent of the vitellarium which reaches only slightly anterior to the ovary. L. caribbaei Blend, Dronen and Armstrong, 2000 is reported from the blackfin grenadier Coelorinchus caribbaeus (Goode and Bean, 1885) from relatively shallow waters (down to 393 m) at various sites in the northern Gulf of Mexico (Blend et al. 2000). It belongs to the Garrardi group, Congeri subgroup, based on its vitellarium and excretory vesicle reaching into the forebody. These features serve to easily distinguish this species from L. sereti. L. longivesicula Blend, Dronen and Armstrong, 2000 was also reported from C. caribbaeus from relatively shallow waters (down to 393 m) at various sites in the north Gulf of Mexico (Blend et al. 2000). As with L. caribbaei, this species belongs to the Garrardi group, Congeri subgroup, based on its vitellarium and excretory vesicle reaching into the forebody, features which serve to easily distinguish this species from L. sereti. Blend et al. (2000) drew attention to a report on an unpublished description (in a thesis by Heath 1989) of a Lepidapedon sp. from the gargoyle fish Coelorinchus mirus McCulloch, 1926 and Coelorinchus sp. off southeastern Australia. This species is, according to Blend et al. (2000), clearly a member of the Elongatum group, Desclersae subgroup. As far as we are aware, this is the first report on a Lepidapedon sensu stricto species from the ‘Pacific, Western Central’ region (no. 71) of the FAO major fishing areas. The nearby ‘Pacific, Southwest’ region (no. 81) includes only the species L. australis , L. blairi , the unpublished report
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mentioned above, and L congeri Manter, 1954, a member of the Garrardi group, Congeri subgroup (based on its vitellarium and excretory vesicle reaching into the forebody) from the ‘Leptocephalus conger’ (presumably Conger verreauxi Kaup, 1856) off Wellington, New Zealand. The observation that this is the first report on Lepidapedon from the Pacific Western Central region is probably not an indication of the scarcity of this genus in this region, but merely a reflection of the lack of observations of deep-sea parasites in this part of the tropical ocean. Acknowledgments We are grateful to B. Richer de Forges (IRD, Nouméa, New Caledonia), Bernard Séret (Museum National d'Histoire Naturelle, Paris France), and the crew members of the NO Alis for their help in collecting and/or identifying the fish species.
References Appy RG, Burt MDB (1982) Metazoan parasites of cod, Gadus morhua L., in Canadian Atlantic waters. Can J Zool 60:1573–1579 Blend CK, Dronen NO, Armstrong HW (2000) Six new species of Lepidapedon Stafford, 1904 (Digenea: Lepocreadiidae) from deep-sea macrourid fishes from the Gulf of Mexico and Caribbean Sea, with revised keys to the species of the genus. Syst Parasitol 45: 29–51 Bray RA (1995) Annotated checklist of digenean parasites of Macrouridae (Teleostei, Gadiformes). Acta Parasitol 40:168–192 Bray RA (2004) The bathymetric distribution of the digenean parasites of deep-sea fishes. Folia Parasitol 51:268–274 Bray RA, Cribb TH (1997) Paralepidapedon ostorhinchi (Korotaeva, 1974) n. comb. (Digenea: Lepocreadiidae) in Oplegnathus woodwardi (Waite) (Teleostei: Perciformes: Oplegnathidae) from off Rottnest Island, Western Australia. Syst Parasitol 36:229–233 Bray RA, Cribb TH (2012) Reorganisation of the superfamily Lepocreadioidea Odhner, 1905 based on an inferred molecular phylogeny. Syst Parasitol 83:169–177. doi:10.1007/s11230-0129386-3 Bray RA, des Clers SA (1992) Multivariate analyses of metrical features in the Lepidapedon elongatum (Lebour, 1908) species-complex (Digenea, Lepocreadiidae) in deep and shallow water gadiform fishes of the NE Atlantic. Syst Parasitol 21:223–232 Bray RA, Gibson DI (1995) The Lepocreadiidae (Digenea) of fishes from the north-east Atlantic: a review of the genus Lepidapedon Stafford, 1904. Syst Parasitol 31:81–132 Bray RA, Jones JB (1993) A new species of Lepidapedon Stafford, 1904 (Digenea: Lepocreadiidae) in the gadiform fish Coelorhinchus bollonsi McCann & McKnight (Macrouridae) from Chatham Rise, New Zealand. Syst Parasitol 26:69–73 Bray RA, Kuchta R (2006) Digeneans from deep-sea marine teleosts off the Outer Hebrides, Scotland, including the description of Brachyenteron helicoleni sp. nov. (Zoogonidae). Acta Parasitol 51:169–175 Bray RA, Littlewood DTJ, Herniou EA, Williams B, Henderson RE (1999) Digenean parasites of deep-sea teleosts: a review and case
3989 studies of intrageneric phylogenies. Parasitology 119(Supplement): S125–S144 Bray RA, Waeschenbach A, Cribb TH, Weedall GD, Dyal P, Littlewood DTJ (2009) The phylogeny of the Lepocreadioidea (Platyhelminthes: Digenea) inferred from nuclear and mitochondrial genes: implications for their systematics and evolution. Acta Parasitol 54:310–329. doi:10.2478/s11686-009-0045-z Campbell RA, Bray RA (1993) Lepidapedon spp. (Digenea: Lepocreadiidae) from deep-sea gadiform fishes of the NW Atlantic Ocean, including four new species. Syst Parasitol 24:99–110 Gavrilyuk-Tkachuk LD (1979) New species of trematodes from commercial fishes of the Indian Ocean. Biol Morya Vladivostok 3: 83–86 (In Russian) Heath BM (1989) A study of the endoparasitic helminths of deep sea fishes from southeastern Australia: taxonomy, zoogeography and host-parasite ecology. PhD thesis. Armidale: University of New England, pp. 360. [n. v.] Heidenhain M (1915) Über die mallorysche bindegewebsfärbjung mit karmin und azokarmin als vorfarben. Z Wiss Mikrosk 32:361–372 Køie M (1984) Digenetic trematodes from Gadus morhua L. (Osteichthyes, Gadidae) from Danish and adjacent waters, with special reference to their life-histories. Ophelia 23:195–222 Køie M (2000) Metazoan parasites of teleost fishes from Atlantic waters off the Faroe Islands. Ophelia 52:25–44 Kuramochi T (2005) Digenean trematodes of fishes from deep-sea areas off Ryukyu Islands, Southern Japan. In: Hasegawa M, Shinohara G, Takeda M (eds) Deep-sea Fauna and Pollutants in Nansei Islands, vol 29. National Science Museum Monographs, Tokyo, pp 23–35 Kuramochi T (2006) Digenean trematodes of fishes caught in the Sagami Sea, central Japan. Mem Natl Sci Mus Tokyo 40:175–186 Kuramochi T (2009) Digenean trematodes of fishes from deep-sea areas off the Pacific Coast of Northern Honshu, Japan. In: Fujita T (ed) Deep-sea fauna and pollutants off Pacific coast of Northern Japan, vol 39. National Museum of Nature and Science Monographs, Tokyo, pp 25–37 Kuramochi T (2011) Digenean trematodes of fishes caught in Sagami Bay, off Izu Islands and off Ogasawara Islands. Mem Natl Mus Nat Sci Tokyo 47:51–63 Langeron M (1949) Précis de microscopie. Masson & Cie, Paris Manter HW (1931) Further studies on trematodes of Tortugas fishes. Carnegie Inst Wash Yearb 30:386–388 Manter HW (1934) Some digenetic trematodes from deep-water fish of Tortugas, Florida. Pap Tortugas Lab 28:257–345 Manter HW (1954) Some digenetic trematodes from fishes of New Zealand. Trans R Soc NZ 82:475–568 Perdiguero-Alonso D, Montero FE, Raga JA, Kostadinova A (2008) Composition and structure of the parasite faunas of cod, Gadus morhua L. (Teleostei: Gadidae), in the North East Atlantic. Parasite Vector 1(23):1–18. doi:10.1186/1756-3305-1-23 Tkachuk LP (2002) Lepidapedon alvigae is a new name for Tormopsolus coelorhynchi Gavrilyuk-Tkachuk, 1979. Ekol Morya 61:44 (In Russian) Yamaguti S (1934) Studies on the helminth fauna of Japan. Part 2. Trematodes of fishes, I. Jpn J Zool 5:249–541 Yamaguti S (1938) Studies on the helminth fauna of Japan. Part 21. Trematodes of fishes, IV. Satyû Yamaguti, Kyoto Zdzitowiecki K, Cielecka D (1997) Digenea of fishes of the Weddell Sea. I. Parasites of Macrourus whitsoni (Gadiformes, Macrouridae). Acta Parasitol 42:23–30
ORIGINAL PAPER
Lepidapedon sereti n. sp. (Digenea: Lepidapedidae) in Coelorinchus sereti (Gadiformes: Macrouridae) from deep waters off Vanuatu Rodney A. Bray & Elisabeth Faliex & Jean François Allienne & Gabriel Mouahid
Received: 30 May 2013 / Accepted: 7 August 2013 / Published online: 8 November 2013 # Springer-Verlag Berlin Heidelberg 2013
Abstract Lepidapedon sereti n. sp. is described from the macrourid Coelorinchus sereti from the deep water off Vanuatu. It is placed in the Elongatum group and Elongatum subgroup. It differs from the other species described in this subgroup by the distinctly dorsally subterminal excretory pore. It also differs from other species in combinations of size, excretory vesicle length, proportions of forebody, posttesticular region and other metric features. This constitutes the first record of a Lepidapedon (sensu stricto) from the Central Western Pacific Ocean.
Introduction Lepidapedon Stafford, 1904 is a large genus, mainly of deepwater fish parasites, with a distinct predilection for gadiforms. According to Bray and Gibson (1995), 61 % of records were from gadiforms, with the families Gadidae (35 %) and Macrouridae (22 %) as the most frequently reported host families. Most of the gadid records are of a few relatively shallow-water species, but the macrourids harbour many distinct species. Bray et al. (1999) presented phylogenetic R. A. Bray (*) Department of Life Sciences, Natural History Museum, Cromwell Road, SW7 5BD London, UK e-mail: [email protected] E. Faliex : J. F. Allienne : G. Mouahid Université de Perpignan, Via Domitia, 52, Avenue Paul Alduy, 66860 Perpignan Cedex, France E. Faliex UMR 5110, CEFREM, CNRS, 52, Avenue Paul Alduy, 66860 Perpignan Cedex, France J. F. Allienne UMR 5244, Ecologie et Evolution des Interactions, CNRS, 52, Avenue Paul Alduy, 66860 Perpignan Cedex, France
estimates inferred from LSU rDNA and ND1 mtDNA sequences, indicating that this genus probably radiated in the deep sea and has encroached into shallower waters in relatively few cases. They considered Lepidapedon to be ‘the most common deep-water digenean genus’, a conclusion which Blend et al. (2000) found to be supported by their findings. Bray (2004) illustrated the bathymetry of deep-water digeneans and showed further data to support this assertion, pointing out that two species, namely Lepidapedon discoveryi Bray and Gibson, 1995 and Lepidapedon beveridgei Campbell and Bray, 1993 had been reported from the northeastern Atlantic abyssal plain at nearly 5,000 m in depth. Lepidapedon has, until recently, been considered a member of the family Lepocreadiidae Odhner, 1905, but molecular estimates of its relationships by Bray et al. (2009) have shown that the family is polyphyletic and Bray and Cribb (2012) suggested that the subfamily Lepidapedinae Yamaguti, 1958 should be raised to family level to better reflect the relationships in the superfamily. This is supported not only by molecular results but also by morphology and biology (Bray et al. 2009; Bray and Cribb 2012).
Material and methods Material was collected in October 1994 during a trawling operation in Vanuatu near the islands of Espiritu Santo (sampling site 15°48.42′S; 167°24.27′E; depth of 775– 798 m). Digenean (a total of three worms) were removed from the digestive tract of a single female specimen of macrourid (female Coelorinchus sereti Iwamoto and Merrett, 1997; standard length 470 mm) and fixed in Bouin's solution (Langeron 1949). Whole mounts (two specimens) were stained with Grenacher's boric acid alcohol-based carmine solution (Langeron 1949) and mounted in Canada balsam. Sections (from one specimen) were cut using a manual
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microtome at 6 μm and stained with Heidenhain's azan (Heidenhain 1915). 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.
posterior extremity of external seminal vesicle or just posterior, confluent in post-testicular region; fields may be slightly interrupted at level of gonads, but not on both sides and not consistently; lateral, ventral and dorsal to caeca. Excretory pore on dorsal surface (Figs. 6 and 7); vesicle reaches dorsally to posterior testis and to posterior edge of anterior testis.
Results
Taxonomic summary
Superfamily Lepocreadioidea Odhner, 1905 Family Lepidapedidae Yamaguti, 1958 Genus Lepidapedon Stafford, 1904 urn:lsid:zoobank.org:act:CBDC3DD9-F745-4CE1-B752955EA2C97B80 Syn. Lepodora Odhner, 1905
Type host: Coelorinchus sereti Iwamoto and Merrett, 1997, female Type locality: Vanuatu, island of Espiritu Santo (15°48.42′S; 167°24.27′E) Deposition of specimens: Museum National d'Histoire Naturelle Paris, France. Holotype MNHN HEL346, paratype MNHN HEL347–357 (11 slides of serial sections); Natural History Museum, London, England, paratype 2013.8.22.1. Etymology: The specific name refers to Dr Bernard Séret (Institut de Recherche pour le Développement (IRD), Museum National d'Histoire Naturelle, Paris, France), in recognition of his expertise in fish taxonomy.
Lepidapedon sereti n. sp. (Figs. 1, 2, 3, 4, 5, 6, 7, 8, and 9; Table 1) urn:lsid:zoobank.org:act:FB9E1567-8787-4EB3-A6ECC53519017F20 Description is based on two whole-mounted specimens and one set of serial sections; the measurements are shown in Table 1. Body elongate linguiform (Figs. 1 and 4). Tegument finely spined, becoming sparser in hindbody, none beyond level of testes. Neither eye spots nor eye-spot pigment seen. Oral sucker small, subglobular, subterminal. Ventral sucker oval, slightly smaller than oral sucker, in anterior quarter of body. Prepharynx long. Pharynx small, oval. Oesophagus long, narrow. Intestinal bifurcation in mid forebody. Caeca narrow, end blindly anterior to excretory pore (Fig. 6), termination may be amongst dense patches of vitelline follicles. Testes two, oval, entire, tandem, separated, in anterior part of posterior half of hindbody. External seminal vesicle elongate sigmoid, reaches about quarter of distance to ovary; surrounded by membrane-bound gland cell mass which narrows anteriorly forming narrow neck before male duct enters cirrus sac (Figs. 2, 5 and 9). Cirrus sac narrow claviform, mainly dorsal to ventral sucker. Internal seminal vesicle gently undulating, narrow. Pars prostatica oval, vesicular (Figs. 2, 5 and 8). Ejaculatory duct short, extended to form short cirrus. Genital atrium distinct. Genital pore sinistral, submedian, at level just anterior to ventral sucker. Ovary oval to weakly trilobate, pretesticular with distinct gap. Laurer's canal long, opens dorsally lateral to left caecum at level of anterior part of ovary (Fig. 3). Seminal receptacle elongate saccular, mainly postero-dorsal to ovary. Mehlis' gland dorsal to ovary. Uterus mainly intercaecal, preovarian, almost entirely in hindbody, runs ventrally to external seminal vesicle. Eggs tanned operculate. Metraterm of similar length to cirrus sac, wall weakly muscular. Vitellarium follicular, anterior extent of follicular field in hindbody, at about 26– 31 % of distance from ventral sucker to ovary, at level of
Discussion This species is a fairly typical member of the genus but is particularly large, and the excretory pore is distinctly dorsal. Initial observations on whole mounts suggested that a cyclocoel (i.e. the caeca unite close to the posterior end of the body) might be present, but sections showed that the caeca terminate blindly. In the whole mounts, the terminations are not easy to see as they occur amongst dense bunches of vitelline follicles. The feature giving the superficial appearance of a cyclocoel is two concentric irregular patches of stained tissue (Fig. 7). The genus Lepidapedon now has over 50 recognised species, although the status of some is doubtful. Bray and Gibson (1995) and Blend et al. (2000) have summarised our knowledge on the genus, with only one species, Lepidapedon alvigae Tkachuk, 2002, having been named since. This latter species is a renaming by Tkachuk (2002) of Tormopsolus coelorhynchi Gavrilyuk-Tkachuk, 1979, which, if considered a Lepidapedon, as suggested by Bray (1995), is preoccupied by Lepidapedon coelorhynchi Yamaguti, 1938. Multivariate analysis of measurements (Bray and des Clers 1992) and molecular studies (Bray et al. 1999, 2009) indicate that although many species are similar morphologically, there are numerous species, particularly in the deep sea. Bray and Gibson (1995) divided the genus into three groups, each separated into subgroups, for some of which they supplied keys. These keys were extended and updated by Blend et al. (2000). The characters of these groups and
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Figs. 1–3 L. sereti n. sp. 1 Ventral view of holotype, uterus in outline. 2 Terminal genitalia, viewed from ventral plane. 3 Proximal female genitalia, viewed from ventral plane. ca, caecum; cs, cirrus sac; e, egg; esv, external seminal vesicle; gp, Genital pore; gs, glandular sheath; isv, internal seminal vesicle; Lc, Laurer's canal; Mg, Mehlis' gland; od, oviduct; ov, ovary; pecs, posterior extent of cirrus sac; pp, pars prostatica; sr, seminal receptacle; ut, uterus; vr, vitelline reservoir; vs, outline of ventral sucker. Scale bars: 1, 1,000 μm; 2, 3, 200 μm
subgroups and the currently recognised species in these groups are summarised in Table 2. The species L. sereti n. sp. fits into the ‘Elongatum group’, where the vitellarium does not reach to the ventral sucker. It fits into the Subgroup i (Elongatum subgroup) in which the excretory vesicle reaches to about the level of posterior margin of the anterior testes. Unfortunately, due to the morphological similarity of many of the species in this subgroup, a key was not produced. The subgroup was considered by Bray and Gibson (1995) to contain eight species, and two have been added subsequently, Lepidapedon ninae Zdzitowiecki and Cielecka, 1997 and Lepidapedon mexicanensis Blend, Dronen and Armstrong, 2000.
L. sereti n. sp. is distinguished from other members of the subgroup and possibly from all described species by its dorsally situated excretory pore. In addition, it is unusually large; only L. discoveryi and, possibly, L. coelorhynchi grow to a similar size. Species in the ‘Elongatum group, Elongatum subgroup’ category are all superficially similar, such that, as stated above, a key to them was not produced by Bray and Gibson (1995). Also two new species have been added since, making it necessary to compare all of the species in this subgroup with L. sereti n. sp. The differentiating features of biology and morphology are discussed below.
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Figs. 4–9 L. sereti n. sp. 4 Whole mount of holotype. 5 Ventral view of terminal genitalia. 6 Sagittal section of posterior part of worm showing caecal extent and dorsal position of excretory pore. 7 Posterior extremity of worm showing posterior vitelline follicles, excretory pore and concentric stained patches of tissue around excretory pore. 8 Sagittal section showing cirrus sac. 9 Sagittal section showing external seminal vesicle and membrane-bound glandular sheath. c, caecum; cs, cirrus sac; dm, delimiting membrane; d, dorsal surface; ep, excretory pore; esv, external seminal vesicle; ev, excretory vesicle; gs, glandular sheath; isv, internal seminal vesicle; mt, metraterm; pecs, posterior extent of cirrus sac; sp, stained patches; v, ventral surface; vf, vitelline follicle; vs, ventral sucker. Scale bars: 4, 1,000 μm; 5, 6, 7, 8, 9, 200 μm
Lepidapedon elongatum (Lebour, 1908) sensu stricto is generally considered to be one of the two common members of the genus found in north Atlantic shallow-water gadids, particularly the cod Gadus morhua Linnaeus, 1758 (the other species is Lepidapedon rachion (Cobbold, 1858), which is mostly found in the haddock Melanogrammus aeglefinus (Linnaeus, 1758)). Perdiguero-Alonso et al. (2008) studied cod from six areas in the waters of Iceland, the British Isles and Scandinavia and found cod infected with L. elongatum at
all sites, although prevalences were low in the Baltic Sea. Overall, the prevalence was 60 %. Appy and Burt (1982) found localities off eastern Canada where prevalence reached 100 %, with intensities up to 2,916 and Køie (1984) found over 90 % prevalence in Danish waters. Recent records of L. elongatum (and its synonym L. microcotyleum Odhner in Dollfus, 1953) from morids and macrourids from deep waters off Japan by Kuramochi (2009) should be treated with caution (see Lepidapedon gadi below). Bray and Gibson (1995)
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Table 1 Dimensions and ratios of Lepidapedon sereti n. sp.
Table 1 (continued)
Species Host Locality n
Pre-vitelline distance % Anterior testis length % Posterior testis length %
Length
Lepidapedon sereti Coelorhynchus sereti Vanuatu 2 Holotype Paratype 8,192 8,406
Width Forebody Preoral lobe Oral sucker length Oral sucker width Prepharynx Pharynx length Pharynx width Oesophagus Intestinal bifurcation to ventral sucker Vitellarium to ventral sucker Ventral sucker length Ventral sucker width Cirrus sac length Cirrus sac width External seminal vesicle reach into hindbody Ventral sucker to ovary Ovary length
963 1,765 14 230 249 216 145 121 365 800 636 227 227 325 119 613 2,404 382
1,051 1,675 46 253 249 148 139 117 292 784 729 217 220 289 101 548 2,282 389
Ovary width Ovary to anterior testis Anterior testis length Anterior testis width Distance between testes Posterior testis length Posterior testis width Post-testicular distance Post-caecal distance Egg length Egg width Width % Forebody % Sucker length ratio 1: Sucker width ratio 1: Oral sucker: pharynx width 1: Ventral sucker to ovary % External seminal vesicle reach into hindbody %a Post-testicular distance % Oesophagus % Intestinal bifurcation to ventral sucker % Vitellarium to ventral sucker % Ovary to anterior testis % Distance between testes % Cirrus sac length % Pre-vitelline distance
365 126 474 438 428 390 434 2,166 603 65–70 (67) 30–38 (34) 11.8 21.5 0.99 0.91 2.05 29.3
325 194 339 312 427 482 414 2,434 646 60–71 (65) 29–41 (35) 12.5 19.9 0.86 0.88 2.13 27.2
25.5
24.0
26.4 4.45 9.76 7.76 1.54 5.22 3.97 2,401
29.0 3.47 9.33 8.67 2.30 5.08 3.44 2,403
29.3 5.79 4.77
28.6 4.04 5.73
Percentages are of total body length a
Ventral sucker to ovary distance
redescribed the species based solely on material from north Atlantic cod. The greatest length reported was 3,970 μm, much shorter than that found for L. sereti n. sp. In addition to the size, the terminal position of the excretory pore and the usual presence of a pseudoesophagus distinguish this species from L. sereti n. sp. The forebody is usually relatively longer (21–33 % of body length), and the male terminal genitalia are much less elongate in L. elongatum; the ventral sucker is usually slightly larger than the oral (sucker width ratio mean 1:1.04), the vitelline follicles are fewer but relatively larger, and the post-testicular distance is shorter (10–18 % of body length). Lepidapedon arlenae Bray and Gibson, 1995 is known from the macrourids the roughsnout grenadier Trachyrincus scabrus (Rafinesque, 1810), the roughnose grenadier Trachyrincus murrayi Günther, 1887 and the spearsnouted grenadier Coelorinchus labiatus (Köhler, 1896) found at moderate depths (down to 1,800 m) from the eastern North Atlantic Ocean from the Bay of Biscay to north of Scotland (Bray and Gibson 1995; Bray and Kuchta 2006). This is a relatively small worm, reaching 3,568 μm. The excretory pore is terminal. The intestinal bifurcation is in the posterior forebody. It is said to have no vitelline follicles dorsal to the caeca. L. coelorhynchi Yamaguti 1938 was originally described from Coelorinchus [as Coelorhynchus ] sp. off Japan (Yamaguti 1938). The maximum size (3,600 μm) in the original description is much less than that of L. sereti n. sp. (8,406 μm); it is wider (width 15–16 % of body length), the ventral sucker is larger (sucker width ratio is about 1:1.14), the forebody is longer (about 28 % of the body length), the ventral sucker to ovary distance is shorter (about 24 % of the body length) and the post-testicular distance is shorter (about 22 % of body length). The excretory pore is illustrated as terminal. This species has subsequently been reported several times from the macrourids Coelorinchus gilberti Jordan and Hubbs, 1925; the Mugura grenadier Coelorinchus kishinouyei Jordan and Snyder, 1900; the giant grenadier Albatrossia [as Coryphaenoides] pectoralis (Gilbert, 1892); and the morid Laemonema filodorsale Okamura, 1982 (Kuramochi 2005, 2006, 2009, 2011). There must be some doubt as to the conspecificity of all these forms as Kuramochi (2005) gave a maximum size of 9,430 μm and Kuramochi (2009) gave 14, 600 μm. In neither paper were illustrations included, and in the latter, only the body size was quoted. Kuramochi (2005)
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Table 2 Groups, subgroups, characters and species of Lepidapedon Group
Characters
Rachion group Vitellarium reaches to about the ventral sucker level.
Elongatum group
Subgroup
Characters
Included species
Rachion subgroup
Excretory vesicle not reaching further anterior than about middle of posterior testis
L. rachion (Cobbold, 1858) L. abyssensis McCauley, 1968 L. aljoshkinae Gaevskaja, 1983 L. cambrensis Srivastava, 1966 L. cascadensis McCauley, 1968 L. desotoensis Blend, Dronen and Armstrong, 2000 L. genge Yamaguti, 1938 L. lebouri Manter, 1934 L. luteum Yamaguti, 1938 L. paralebouri Zdzitowiecki, 1990 L. zaniophori Blend, Dronen and Armstrong, 2000 L. sommervillae Bray and Gibson, 1995
Sommervillae Excretory vesicle reaches subgroup to the anterior testis Vitellarium not reaching Elongatum subgroup Excretory vesicle reaches to ventral sucker to about the level of posterior margin of the anterior testes
Desclersae subgroup Excretory vesicle reaches to about level of posterior margin of posterior testis
Ostorhinchi subgroup
Subgroup IV
L. elongatum (Lebour, 1908) L. arlenae Bray and Gibson, 1995 L. coelorhynchi Yamaguti, 1938 L. discoveryi Bray and Gibson, 1995 L. gadi (Yamaguti, 1934) L. gaevskayae Campbell and Bray, 1993 L. mariannae Bray and Gibson, 1995 L. merretti Campbell and Bray, 1993 L. mexicanensis Blend, Dronen and Armstrong, 2000 L. ninae Zdzitowiecki and Cielecka, 1997 L. sereti n. sp. L. desclersae Bray and Gibson, 1995 L. antimorae McCauley, 1968 L. australis Manter, 1954 L. blairi Bray and Jones, 1993 L. brayi Zdzitowiecki and Cielecka, 1997
L. filiformis McCauley, 1968 L. lepidum Gaevskaja and Rodyuk, 1988 L. nezumiatis Blend, Dronen and Armstrong, 2000 L. oregonensis MeCauley, 1968 L. taeniatum Gaevskaja and Rodyuk, 1988 L. yaquina McCauley, 1968 L. megalaspi Parukhin, 1966 incertae sedis L. sphyraenae Shen, 1990 incertae sedis Excretory vesicle reaches The only species placed in this subgroup, to about level of ovary L. ostorhinchi Korotaeva, 1974, is now considered a member of the genus Paralepidapedon Shimazu and Shimura, 1984 by Bray and Cribb (1997) Excretory vesicle not described L. alvigae Tkachuk, 2002 L. clavatum Linton, 1940 L. gymnacanthi (Issaitschikov, 1928) L. sammari Abdel Aal, Banaja and Al Zanbagi, 1985 incertae sedis L. spiniferi Abdel Aal, Banaja and Al Zanbagi, 1985 incertae sedis
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Table 2 (continued) Group
Characters
Garrardi group Vitellarium reaches at least to intestinal bifurcation
Subgroup
Characters
Included species
Garrardi subgroup
Excretory vesicle reaching close to the level of the posterior margin of the posterior testis
L. garrardi (Leiper and Atkinson, 1914) L. calli Acena, 1947 L. carcini Mordvinova, 1985
Beveridgei subgroup
Congeri subgroup
Subgroup IV
L. guevarai Lopez-Roman and Maillard, 1973 L. zubchenkoi Campbell and Bray, 1993 Excretory vesicle reaches L. beveridgei Campbell and Bray, 1993 to the level of the posterior L. balgueriasi Zdzitowiecki and margin of the anterior testis Cielecka, 1997 or further into the region L. notogeorgianus Zdzitowiecki, 1990 between the testes L. tertius Zdzitowiecki, 1990 Excretory vesicle reaching L. congeri Manter, 1954 into the forebody to about L. caribbaei Blend, Dronen and the level of the intestinal Armstrong, 2000 bifurcation L. longivesicula Blend, Dronen and Armstrong, 2000 Excretory vesicle not described L. golphick Oshmarin, 1968
described the excretory pore as subterminal but did not mention the extent of the vesicle. Using the body-size data in these two papers, the width is 13–19 % of the body length, somewhat greater than that of L. sereti n. sp. L. discoveryi Bray and Gibson, 1995 is known only from the macrourid abyssal grenadier Coryphaenoides armatus (Hector, 1875) from the eastern North Atlantic and is found over a wide range of depths, from 2,550 to 4, 850 m, i.e. it can be abyssal (Bray and Gibson 1995). This is a large worm, of similar dimensions to L. sereti n. sp., known to attain a length of 9,304 μm. The excretory pore is terminal. The excretory vesicle is rather shorter than is usual in this subgroup (although not short enough to fit the species into the Desclersae subgroup). It ‘usually reaches to level of middle of posterior testis, occasionally may reach just anterior to posterior margin of posterior testis or just anterior to anterior margin of posterior testis (not reaching close to anterior testis)’ (Bray and Gibson 1995). L. gadi (Yamaguti, 1934) Yamaguti 1938 sensu stricto was considered to be restricted to the Pacific cod Gadus macrocephalus Tilesius, 1810 from the North Pacific Ocean by Bray and Gibson (1995). If this is the case, then only the original description can be considered for comparison (Yamaguti 1934). The worm is of moderate size, reaching a maximum length of 5,800 μm, but the excretory pore is terminal, the forebody is longer (about 27 % of the body length) and the post-testicular distance is shorter (about 16 % of the body length). A pseudoesophagus is reported as ‘posterior part [of the oesophagus] lined by the intestinal epithelium’ (Yamaguti 1934). This appears to be a shallowwater form. This name has been used for worms from G.
morhua in northern European waters, which were considered L. elongatum by Bray and Gibson (1995). Lepidapedon gaevskayae Campbell and Bray, 1993 is known only from C. armatus from the western and eastern North Atlantic (Campbell and Bray 1993; Bray and Gibson 1995). Its maximum known length is 4,300 μm, and the excretory pore is terminal. The worm is narrower (width 7– 10 % body length), with a shorter post-testicular distance (11– 20 % of body length). The intestinal bifurcation is well into the posterior part of the forebody. The ventral sucker is smaller, with a sucker width ratio of 1:0.68–0.86. Although this species is reported from a fish species which is often recovered from abyssal depths, it has only been reported to 2,890 m (cf. L. discoveryi from the same host species). Lepidapedon mariannae Bray and Gibson, 1995 is known only from the lotid Arctic rockling Gaidropsarus argentatus (Reinhardt, 1837), from moderate depths (to 1,110 m) in waters to the north of Scotland to the Faroes (Bray and Gibson 1995; Køie 2000). It is a moderately sized worm, up to 4, 960 μm long. The excretory pore is terminal. The anterior extent of the vitellarium overlaps the posterior margin of the external seminal vesicle, occasionally reaching to the ventral sucker. A pseudoesophagus may be present. Lepidapedon merretti Campbell and Bray, 1993 is known only from the phycid longfin hake Phycis chesteri Goode and Bean, 1878, from relatively shallow depths (to 786 m) in the Hudson Canyon, western North Atlantic (Campbell and Bray 1993). It is a small worm, only reaching 2,780 μm in length. It is broader (width 14–27 % of body length); the forebody is longer (18–31 % of body length), and the ventral sucker to ovary distance is smaller (14–23 % of body length), as is the post-testicular distance (10–22 % of body length). The
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excretory pore is terminal, and the vitellarium may reach virtually to the ventral sucker. L. mexicanensis Blend, Dronen and Armstrong, 2000 is known from the macrourids the hollowsnout grenadier Coelorinchus caelorhincus (Risso, 1810), the carmine grenadier Coryphaenoides carminifer (Garman, 1899) and the thickbeard grenadier Coryphaenoides zaniophorus (Vaillant, 1888) from the northern Gulf of Mexico (Blend et al. 2000). This is a small worm, reaching only 1,809 μm in length, and the excretory pore is terminal. It is wider (width 14–33 % of body length) and has a shorter ventral sucker to ovary distance (11–26 % of body length). The intestinal bifurcation is in the posterior forebody. L. ninae Zdzitowiecki and Cielecka, 1997 is known only from Whitson's grenadier Macrourus whitsoni (Regan, 1913) from the Weddell Sea in western Antarctica (Zdzitowiecki and Cielecka 1997). The species is based on one specimen of 3, 310 μm in length. The original authors pointed out that, in some characteristics, it resembles the Rachion group worms (long prepharynx, short oesophagus). The excretory pore is terminal. Its eggs are larger (91–102 × 40–46 μm), the forebody is longer (33 % of body length), and the distance from the ventral sucker to ovary is shorter (about 17 % of body length). Several other Lepidapedon species have been reported from Coelorinchus spp. (under various spellings of the host generic name). These are L. rachion (Cobbold, 1858), L. alvigae Tkachuk, 2002, Lepidapedon australis Manter, 1954, Lepidapedon blairi Bray and Jones, 1993, Lepidapedon caribbaei Blend, Dronen and Armstrong, 2000 and Lepidapedon longivesicula Blend, Dronen and Armstrong, 2000. L. rachion (Cobbold, 1858) was reported in Coelorinchus sp. from Tortugas, Florida (Manter 1931), and the longnose grenadier Coelorinchus carminatus (Goode, 1880) from the same locality at 200–315 fathoms (366–576 m) by Manter (1934). L. rachion is the type species of the genus and is considered by Bray and Gibson (1995) to be a shallowwater species with a distinct predilection for the haddock M. aeglefinus . Manter's records were not included amongst those of L. rachion sensu stricto by Bray and Gibson (1995). This form is easily distinguished from of L. sereti n. sp. by its broad shape and the vitellarium reaching into the forebody. L. alvigae Tkachuk 2002 (syn. T. coelorhynchi GavrilyukTkachuk, 1979) was reported from the banded whiptail Coelorinchus fasciatus (Günther, 1878) from the Agulhas Bank in the Indian Ocean (Gavrilyuk-Tkachuk 1979). The worm is of moderate size, reaching a maximum of 4,140 μm in length. The excretory vesicle is not described, but the pore appears terminal in the illustration. The forebody is longer (about 31 % of body length), and the post-testicular distance is shorter (about 17 % of body length). Nevertheless, the worm clearly belongs in Lepidapedon.
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L. australis Manter, 1954 is known only from the javelin Coelorinchus australis (Richardson, 1839) off Wellington in the North Island of New Zealand (Manter 1954). This is a fairly large worm reaching up to 6,536 μm in length. Its excretory vesicle is short, extending only to the posterior testis, causing it to be placed in the Desclersae subgroup by Bray and Gibson (1995). It has a long forebody, originally described as a little less than half the body length (about 36– 39 % of body length using the data given in the description). The distance of the ventral sucker to ovary is shorter (about 19 % of body length), the post-testicular distance is shorter (18–19 % of body length), and the eggs are larger (80–92× 55–65 μm). The ventral sucker is always slightly larger than the oral sucker (sucker width ratio 1:1.03–1.30). L. blairi Bray and Jones, 1993 is known from Bollons' rattail Coelorinchus bollonsi McCann and McKnight, 1980 at a relatively shallow depth (570 m) from Chatham Rise off New Zealand (Bray and Jones 1993) and from the rough-head whiptail Coelorinchus aspercephalus Waite, 1911 in relatively shallow (495 m) waters just off the southern end of New Zealand (Bray and Gibson 1995). It is a moderately sized worm (up to 5,000 μm in length). Its short excretory vesicle places this species in the Desclersae subgroup. It is easily distinguished from most Lepidapedon species by the anterior extent of the vitellarium which reaches only slightly anterior to the ovary. L. caribbaei Blend, Dronen and Armstrong, 2000 is reported from the blackfin grenadier Coelorinchus caribbaeus (Goode and Bean, 1885) from relatively shallow waters (down to 393 m) at various sites in the northern Gulf of Mexico (Blend et al. 2000). It belongs to the Garrardi group, Congeri subgroup, based on its vitellarium and excretory vesicle reaching into the forebody. These features serve to easily distinguish this species from L. sereti. L. longivesicula Blend, Dronen and Armstrong, 2000 was also reported from C. caribbaeus from relatively shallow waters (down to 393 m) at various sites in the north Gulf of Mexico (Blend et al. 2000). As with L. caribbaei, this species belongs to the Garrardi group, Congeri subgroup, based on its vitellarium and excretory vesicle reaching into the forebody, features which serve to easily distinguish this species from L. sereti. Blend et al. (2000) drew attention to a report on an unpublished description (in a thesis by Heath 1989) of a Lepidapedon sp. from the gargoyle fish Coelorinchus mirus McCulloch, 1926 and Coelorinchus sp. off southeastern Australia. This species is, according to Blend et al. (2000), clearly a member of the Elongatum group, Desclersae subgroup. As far as we are aware, this is the first report on a Lepidapedon sensu stricto species from the ‘Pacific, Western Central’ region (no. 71) of the FAO major fishing areas. The nearby ‘Pacific, Southwest’ region (no. 81) includes only the species L. australis , L. blairi , the unpublished report
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mentioned above, and L congeri Manter, 1954, a member of the Garrardi group, Congeri subgroup (based on its vitellarium and excretory vesicle reaching into the forebody) from the ‘Leptocephalus conger’ (presumably Conger verreauxi Kaup, 1856) off Wellington, New Zealand. The observation that this is the first report on Lepidapedon from the Pacific Western Central region is probably not an indication of the scarcity of this genus in this region, but merely a reflection of the lack of observations of deep-sea parasites in this part of the tropical ocean. Acknowledgments We are grateful to B. Richer de Forges (IRD, Nouméa, New Caledonia), Bernard Séret (Museum National d'Histoire Naturelle, Paris France), and the crew members of the NO Alis for their help in collecting and/or identifying the fish species.
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