a new monogenean and cestode from the deep-sea fish...

Proc. Helminthol. Soc. Wash.49(2), 1982, pp. 169-175

A New Monogenean and Cestode from the Deep-Sea Fish,Macrourus berglax Lacepede, 1802, from theFlemish Cap off Newfoundland

RONALD A. CAMPBELL,1 STEVEN J. CORREIA/ ANDRICHARD L. HAEDRiCH2

1 Department of Biology, Southeastern Massachusetts University,North Dartmouth, Massachusetts 02747 and2 Department of Biology, Memorial University of Newfoundland,St. John's, Newfoundland, Canada, A1B3X9

ABSTRACT: A new trematode, Macruricotyle newfoundlandiae sp. n. (Monogenea: Diclidophoridae),and a new cestode, Parabothriocephalus macruri sp. n. (Cestoda: Parabothriocephalidae), are de-scribed from 46 specimens of the macrourid fish, Macrourus berglax Lacepede, 1802, taken in theNewfoundland region of the North Atlantic Ocean (45°31'-46043'N, 44°08'^8°23'W). Macruricotylenewfoundlandiae is the second species named in the genus, and is distinguished from M. clavipesMamaev and Lyadov, 1975 by its much larger pharynx, smaller first pair of clamps, "callous" on thesecond and third pairs of clamps, and the shape of the distal median sclerite in the posterior clampjaw. Parabothriocephalus macruri sp. n. is differentiated from the three other species in the genusby its narrow scolex and segment shape, 77-112 testes per segment, and lack of a vaginal armatureand sphincter.

During May-June 1981, 218 fishes (21 spp.) were examined off the eastern slopeof the Grand Bank and in the Flemish Cap area off Newfoundland. In this paperwe describe a new species of Macruricotyle (Monogenea) and a new species ofParabothriocephalus (Cestoda) from that collection. Noble et al. (1972) and Zub-chenko (1979, 1981) have reported pseudophyllidean cestodes from Macrourusberglax and other macrourids in the northwest Atlantic, but did not identify them.Specimens of Macruricotyle and Parabothriocephalus are unknown from M. ber-glax or other fishes in this region. Discussion of the entire metazoan parasitefauna of M. berglax and other dominant deep-benthic fishes of this region wil lbe presented in another paper.

Materials and Methods

Forty-six specimens of M. berglax, taken in 12.5-m Gulf of Mexico shrimptrawls and standard survey-type bottom trawls fished at 367-811 m, were ex-amined at sea. A few fish were moribund when obtained, but most had recentlydied. Examinations for parasites began immediately. Fish from large samples thatcould not be examined immediately were refrigerated and examined the followingday. Organs and tissues were observed with the aid of a dissecting microscope.The monogenetic trematodes were fixed in cold alcohol-formalin-acetic acid (AFA)without cover-glass pressure. Cestodes were relaxed in tap water for 10-20 minprior to fixation by immersion in AFA. Al l parasites were later transferred to70% ethanol prior to staining. Trematodes were stained with Mayer's paracarmineand cestodes were stained in Harris' hematoxylin. Whole mounts were dehy-drated in ethanol, cleared in methyl salicylate, and mounted in Canada balsam.Serial transverse sections, cut at 6 /xm, of mature segments of Parabothrio-cephalus were stained in Harris' hematoxylin and counterstained with eosin.

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Copyright © 2011, The Helminthological Society of Washington

170 • PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY

Descriptive measurements are expressed as length by width, and are in microm-eters unless otherwise indicated. The mean is given following the range for somecharacters.

Macruricotyle newfoundlandiae sp. n.(Figs. 1-7)

DESCRIPTION (based on 14 specimens; 10 mature specimens measured): Bodyproper elongate, rather slender, tapering anteriorly, 3.6-8 mm (5.18 mm). Maxi-mum width at ovarian level, 360-1,000 (789). Total length 4.2-9.1 mm (6.8 mm)including opisthaptor. Opisthaptor 824-1,800 (1.15 mm) by 2-4.2 mm (3.16 mm),consisting of 2 symmetrical, palmate lobes, each bearing 4 pedunculated clamps;lobes directed at right angles to body. Origin of lobes marked by inverted V-shapeddepression on ventral body surface (Fig. 1). Terminal lappet about 120 by 160,bearing 1 or 2 pairs of minute hooks. Clamps about equal, wider than long,160-272 by 192-264; anterior pair of clamps often slightly smaller. Clamp cavitysurrounded by 8 sclerites; opening exhibiting well-developed muscular rim (Fig.5). Interior of posterior valve bearing riblike thickenings and smaller, distal, me-dian sclerite with flared lateral wings (Figs. 5, 6). Posterior (dorsal) surfaces ofsecond and third clamp valves (Fig. 1) bearing well-developed pad or "callous"(sic, Mamaev and Lyadov, 1975). Callous slightly bilobed, about same dimensionsas its associated clamp. Muscle bundles traversing opisthaptor to clamps welldeveloped, especially large for the third clamp pair.

Mouth ventral, subterminal. Intrabuccal suckers 72-128 (104) in diameter.Pharynx conspicuous, 256-360 (309) by 224-288 (261), containing 2 indistinctmasses of gland cells. Esophagus short. Intestinal bifurcation at level of genitalpore; ceca forming numerous lateral diverticula, terminating in large brancheswithin opisthaptor.

Testes subspherical, about 50-70 in number, in postovarian intercecal space.Cirrus 80-136 (105) in diameter, armed with a corona of 10-14 sickle-shapedhooks. Prostatic vesicle droplet-shaped, immediately posterior to cirrus; prostatecells large but indistinct.

Ovary reverse J-shaped when viewed ventrally, situated at midbody, maximumdimensions 320-600 by 248^400, mature end sinistral. Oviduct passing anteriorlyand across to right side of ovary, then descending beneath immature end of ovary,entering ootype in postovarian space (Fig. 7). Seminal receptacle large, unlobed,overlapping right anterior Vi of ovary. Genito-intestinal canal ventral, recurvinganterolaterally from main vitelline duct, emptying into right cecum. Mehlis' glandsmall, indistinct. Vaginal openings paired, on lateral body margins opposite gen-ital pore. Uterus ascending directly in midline to genital atrium. Vitelline folliclessubspherical to irregular, 42-68 by 38-46, numerous, distributed around ceca fromlevel of prostatic vesicle to end of body proper; linear series of follicles scatteredthrough anterior portion of opisthaptor lobes in direction of first pair of clamps.Eggs not observed.

HOST: Macrourus berglax Lacepede, 1802 (Macrouridae).COLLECTION LOCALITIES AND DEPTHS: 45°38'N, 48°16'W at 715-720 m; 46°31'N,

45°52'W at 425-464 m; 46°35'N, 45°51'W at 367-390 m; 46°43'N, 44°08'W at514-521 m.


OF WASHINGTON, VOLUM E 49, NUMBER 2, JULY 1982 • 171

Figures 1—7. Macruricotyle newfoundlandiae sp. n. 1. Holotype, dorsal view. Note callous (C) onsecond and third clamps. 2. Anterior end, showing pharynx. 3. Detail, male terminalia. Note cirrushooks. 4. Posterior (dorsal) view, second clamp on right side, showing callous (C) of a paratype. Figures4-6 to same scale. 5. Anterior (ventral) view of second clamp on left side (holotype). 6. Detail of distalmedian sclerite in posterior clamp jaw. 7. Detail, female reproductive system. Abbreviations: CP, cirruspouch; GI, genito-intestinal canal; GP, genital pore; MG, Mehlis' gland; OV, ovary; OVD, oviduct; SR,seminal receptacle; T, testis; U, uterus; UD, uterine duct; UP, uterine pore; V, vagina; VD, vas deferens;VTD, vitelline duct.



LOCATION: Gills.PREVALENCE: On 10 of 46 fish examined.INTENSITY: One to 2 worms per host.TYPE SPECIMENS: USNM Helm. Coll. Nos. 77096 (holotype) and 77097 (para-

type); additional paratypes in Harold W. Manter Laboratory, University of Ne-braska State Museum No. 21399, and in the British Museum (Natural History).

ETYMOLOGY: The species is named after Newfoundland, in the geographicalregion of collection.

Remarks

The genus Macruricotyle was created by Mamaev and Lyadov (1975) for M.clavipes found on the gills of Macrourus sp. taken in the southern Indian Ocean.Diagnostic characteristics of the genus are a prostatic vesicle, an armed cirrus,paired vaginae, and clamps with an adhesive (?) callous. Because of its diagnosticcharacters, Mamaev and Lyadov (1975) considered Macruricotyle to occupy anintermediate position among the subfamilies of the Diclidophoridae, with an ad-vanced structural organization above the most primitive subfamily, Diclidopho-ropsinae.

Macruricotyle newfoundlandiae may be differentiated from M. clavipes, theonly other species described in the genus, by the following combination of char-acters: (1) a much larger pharynx (256-360 by 224-288 versus 140-160 by 120-150for M. clavipes}; (2) the first pair of clamps smallest (fourth pair of clamps smallestin M. clavipes); (3) a callous present on both the second and third clamp pairs(on only the third clamp pair of M. clavipes); and (4) shape of the distal mediansclerite of the posterior clamp jaw (compare Fig. 6 with figures of Mamaev andLyadov, 1975).

Parabothriocephalm macruri sp. n.(Figs. 8-12)

DESCRIPTION (based upon 3 complete specimens with mature segments): Stro-bila filiform , delicate, tapering to maximum width of 2.34 mm. Total length14.5-26.9 cm; 840 segments in largest specimen. Scolex elongate, pointed,1,460-2,240 by 340-380. Bothria shallow. Neck absent. Segments craspedote;first segment merging with scolex, succeeding segments elongate, about 400 by280, rapidly becoming wider than long, about 200 by 600. Genital primordia firstapparent in segments measuring 280 by 2,000; testes apparent in segments mea-suring 380 by 2,100, segments elongating to 860 by 2,340 with further maturation.Secondary division of segments apparent throughout strobila; segments up to 540by 1,840 still dividing. Fully mature primary segments 460-560 by 1,960-2,340,segments resulting from secondary division narrower, up to 240 by 2,080. Genital

Figures 8-12. Parabothriocephalus macruri sp. n. 8. Scolex (holotype). 9. Transverse section throughgenital pore, vagina, and uterine pore of mature segment. Figures 9-10 to same scale. 10. Transversesection of mature segment. Note disposition of testes, vitelline follicles, and osmoregulatory ducts. 11.Mature segment. 12. Detail of reproductive system (vitellaria not shown). Abbreviations as in Figures1-7.


OF WASHINGTON, VOLUM E 49, NUMBER 2, JULY 1982 173

0.5mm

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pores dorsosubmarginal, above nerve cords, irregularly alternating. Testes spher-ical to subspherical, 56-88 in diameter, 77-112 (90) per segment, encircling re-productive organs within medullary zone, continuous from segment to segment.Cirrus sac pyriform, thick-walled, 352^40 by 96-184, oriented transversely orslightly anteromedially. Cirrus armed with small spines. Vas deferens tightly coiledat proximal end of cirrus sac.

Ovary bilobed, maximum dimensions 80-208 by 520-624, submedian, imme-diately posterior to cirrus sac. Ovarian lobes asymmetrical, subdivided into lob-ules; antiporal lobe 240-336 by 104-208; poral lobe 88-236 by 80-184. Ootypeand Mehlis' gland form a globular complex, 106-208 by 112-152, posterior toovarian isthmus. Vagina divided into 2 parts of about equal length; proximalportion tubular, not coiled, surrounded by gland cells; distal portion thin-walled,saccate, 320-360 by 48-120, reaching maximum dimensions in oldest segments.No vaginal armature, vaginal sphincter, or seminal receptacle. Uterus extendinganterolaterally to uterine pore, tightly coiled, surrounded by gland cells. Uterinepore ventral, near anterior margin of segment, submedian to antiporal side by6-8% of segment width. Vitelline follicles spherical to subspherical, 56-80 indiameter, fillin g entire circumcortical zone; some follicles in medullary zone. Eggsnot observed. Osmoregulatory ducts in a longitudinal series across dorsal medulla(Fig. 9).

HOST: Macrourus berglax Lacepede, 1802 (Macrouridae).COLLECTION LOCALITIES AND DEPTHS: 46°31'N, 46°52'W at 425-464 m; 46°35'N,

45°51'Wat 367-390 m.LOCATION: Scolex in pyloric cecum, strobila in intestinal lumen.PREVALENCE: In 3 of 46 fish examined.INTENSITY: One worm per host.TYPE SPECIMENS: USNM Helm. Coll. Nos. 77098 (holotype) arid 77099 (para-

type).

Remarks

Yamaguti (1934) created Parabothriocephalus for a cestode commonly foundin a shallow-water teleost, Psenopsis anomala (Temminck and Schlegel, 1850),from the Inland Sea of Japan. The type species, P. gracilis, is unusual in havinga vaginal armature. Since the creation of the genus, that feature has not beenfound in the two species added to the genus. A vaginal armature is also absentin P. macruri sp. n. Other differences distinguishing P. macruri from P. gracilisYamaguti, 1934 are its larger size (14-26 cm versus 6 cm) and its consistentlywider-than-long mature segments (longer than broad in P. gracilis).

The two remaining species in the genus are P. sagitticeps (Sleggs, 1927) andP.johnstoni Prudhoe, 1969. Jensen (1976) correctly reassigned Dibothrium sag-itticeps Sleggs, 1927 to Parabothriocephalus. Parabothriocephalus sagitticeps,from the California rockfish, Sebastes paucispinis Ay res, 1854, is the largestspecies in the genus to date (up to 42 cm by 8 mm). Other characteristics sepa-rating P. sagitticeps from P. macruri are its testes number (135-384 versus 77-112in P. macruri), a large scolex with projecting bothria, a centered uterine pore, asharply recurved distal portion of the uterus, and smooth ovarian lobes. The lastthree characters were determined by examining Jensen's specimens (USNM Helm.Coll. Nos. 73463-73467).


OF WASHINGTON, VOLUM E 49, NUMBER 2, JULY 1982 • 175

Parabothriocephalusjohnstoni described by Prudhoe (1969), was discovered in adeep-sea fish, Coryphaenoides whitsoni Regan, 1913. The specimens were col-lected northeast of Cape Ann, Antarctica, during the B.A.N.Z. Antarctic Expe-dition of 1929-1931. After examining the type specimens of P. johnstoni (wholemounts and serial sections), we found that it possesses a very large vaginalsphincter, about 50 testes per segment, a rather powerful longitudinal muscula-ture, and has the Mehlis' gland situated dorsal to the ovarian isthmus. Thosefeatures clearly differ from our species, P. macruri sp. n., which lacks a vaginalsphincter, possesses 77-112 (90) testes per segment, has smaller longitudinal mus-cle bundles, and has the Mehlis' gland situated posterior to the ovarian isthmus.

Acknowledgments

Thanks are due to Dr. John Anderson, Scientist-in-Charge, Northwest AtlanticFisheries Centre, St. John's, Newfoundland, for providing research space aboardF-V Gadus Atlantica for R. Campbell; and to Dr. Richard L. Haedrich, MemorialUniversity of Newfoundland, for supplying equipment and fish for examination.This work was supported, in part, by National Sciences and Engineering ResearchCouncil of Canada Grant A-7230 to R. L. Haedrich.

Literature Cited

Jensen, L. A. 1976. Parabothriocephalus sagitticeps (Sleggs, 1927) comb. n. (Cestoda: Paraboth-riocephalidae) from Sebastes paucispinis of southern and central California. J. Parasitol. 62:560-562.

Mamaev, Yu. L., and V. N. Lyadov. 1975. Monogeneans of the subfamily Diclidophoropsinae(Monogenoidea: Diclidophoridae). Proc. Inst. Biol. Pedol., Vladivostok, New Ser. 26:115-125.(In Russian)

Noble, E. R., J. D. Orias, and T. D. Rodella. 1972. Parasitic fauna of the deep-sea fish, Macrourusrupestris (Gunnerus) from Korsfjorden, Norway. Sarsia 50:47-50.

Prudhoe, S. 1969. Cestodes from fish, birds and whales. B.A.N.Z.A.R.E. Rep., Br. Mus. (Nat.Hist.), Ser. B 8:171-193.

Yamaguti, S. 1934. Transactions I. Studies on the helminth fauna of Japan. Part 4. Cestodes offishes. Jpn. J. Zool. 6:1-112.

Zubchenko, A. V. 1979. The parasite fauna of macrourids in the North Atlantic. Tr. Polyarn.Nauchno-Issled. Proektn. Inst. Morsk. Rybn. Khoz. Okeanogr. 35:234-238. (In Russian)

Zubchenko, A. V. 1981. Parasitic fauna of some Macrouridae in the Northwest Atlantic. J. North-west. Atl . Fish. Sci. 2:67-72.


a new monogenean and cestode from the deep-sea fish...

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