A New Species of Clistobothrium - University of Connecticut

J. Parasitol., 79(1), 1993, p. 37-43? American Society of Parasitologists 1993A NEW SPECIES OF CLISTOBOTHRIUM(CESTODA: TETRAPHYLLIDEA), WITH AN EVALUATION OF THESYSTEMATIC STATUS OF THE GENUST. R. RuhnkeDepartment of Ecology and Evolutionary Biology, University of Connecticut, 314 TLS,Storrs, Connecticut 06269-3043ABSTRACT: Clistobothrium montaukensis n. sp. is described from the shortfin mako shark, Isurus oxyrinchus.Based on shared characters from the scolex and segment, Phyllobothrium tumidum is transferred to the genusClistobothrium, and the species description is emended. The description of the type species, Clistobothriumcarcharodoni, also is emended, as is the generic diagnosis. Derived characters shared by these 3 species includea dorsomedian longitudinal band of strobilar muscles, a bilobed ovary, and a dorsal L-shaped cirrus sac. Thespined or mammilated egg surface of these 3 species also may be synapomorphic. Although phenetically similar,it is postulated that the foliose bothridial condition shared among members of Phyllobothrium and 2 of thespecies of Clistobothrium is not homologous. The cirruses of C. montaukensis n. sp. and C. carcharodoniare armed with microtriches, but this may be true for other cestodes. Reliable host reports indicate that speciesof Clistobothrium are restricted to sharks of the family Lamnidae (the mackerel sharks).Dailey and Vogelbein (1990) erected Clistobothriumfor Clistobothrium carcharodoni fromthe great white shark, Carcharodon carchariasLinnaeus, 1758. A morphological study of newlycollected material from the shortfin mako shark,Isurus oxyrinchus Rafinesque, 1809, revealed anew species of Clistobothrium. Examination oftype and voucher specimens of Phyllobothriumtumidum Linton, 1922, from the great white sharkindicated that it should be considered congenericwith the above 2 species. The following reportsummarizes taxonomic information for membersof Clistobothrium and emends the genericdiagnosis. The study also allowed for a morphologicalexamination of the cirrus armature forthe new species and C. carcharodoni. A summaryof host reports for members of Clistobothriumalso is presented.MATERIALS AND METHODSDuring the summers of 1988-1990, 5 shortfin makosharks, I. oxyrinchus, were collected from sport fishermenat shark fishing tournaments in Montauk onLong Island, New York, and in Yarmouth, Massachusetts.The spiral intestine was removed from each sharkand opened with a longitudinal incision along the dorsalsurface to expose the internal chambers. Wormswere removed, relaxed in sea water, then placed in avial of alcohol-formalin-acetic acid (AFA) or in hotwater and immediately transferred to AFA. For electronmicroscopical studies, worms were fixed in coldReceived 30 August 1991; revised 14 August 1992;accepted 26 August 1992.372.5% glutaraldehyde in 0.1 M cacodylate buffer, washedin the same concentration of buffer, and postfixed in1% osmium tetroxide. Spiral intestines from some ofthe individuals also were fixed in AFA, and additionalworms were removed from the intestines upon returningto the laboratory. Specimens of P. tumidum wereobtained from the spiral intestine of a great white sharkobtained from fisherman fishing in Atlantic waters offLong Island. Specimens for whole mounts were stainedwith Ehrlich's or Gill's hematoxylin, flattened between2 glass slides, dehydrated in an alcohol series, destainedin acid ethanol (if required), cleared in xylene, andmounted in Canada balsam. Cross sections were preparedaccording to the methods of Caira and Gavarrino(1990). Specimens for scanning electron microscopywere dehydrated in an ethanol series, critical point driedin liquid CO2, mounted on stubs with carbon paint,sputter coated with gold, and examined in a Coatesand Welter field emission scanning electron microscope.Measurements are given in micrometers unlessotherwise stated. The range is given for each numericalcharacter, followed in parentheses by the mean, standarddeviation, number of worms examined (n), andthe total number of observations when more than 1measurement per worm was taken (n). Tapeworm eggswere measured from segments mounted in Canada balsamand from segments opened and examined in 70%ethanol. Cirrus sacs were measured according to themethod used by Caira (1990) for trematodes. Illustrationswere made with the aid of a drawing tube. Paratypesof C. carcharodoni (USNM no. 80985 and HWMLno. 31397) were borrowed from the U.S. National MuseumHelminthological Collection, Beltsville, Maryland,and the H. W. Manter Laboratory, University ofNebraska State Museum. Type specimens of P. tumidum(USNM nos. 2630 and 2631) were borrowed fromthe U.S. National Museum Helminthological Collectionin Beltsville, Maryland. A voucher specimen ofP. tumidum (USNM no. 35802) was borrowed fromthe U.S. National Museum Helminthological Collection.

38 THE JOURNAL OF PARASITOLOGY, VOL. 79, NO. 1, FEBRUARY 19937X4 0 Ii- : ':;'0FIGURES 1-8. Line drawings of Clistobothrium carcharodoni, Clistobothrium tumidum, and Clistobothriummontaukensis. 1. Cirrus microtriche from partially everted cirrus of paratype (HWML no. 31397) of C carcharodoni.2. Cirrus sac from end segment of lectotype (USNM no. 7631) of C. tumidum n. comb. 3. Scolex ofholotype (USNM no. 82490) of C. montaukensis. 4. Mature segment, ventral view of paratype (USNM no.82490) of C. montaukensis. 5. Dorsomedian muscle band of paratype (USNM no. 82490) of C. montaukensis.6. Cross section through segment posterior to cirrus sac and anterior to ovary of paratype (HWML no. 35289)of C. montaukensis. 7. Cross section through segment at ovary of paratype (HWML no. 35289) of C. montaukensis.8. Cirrus microtriche from cross section through cirrus of voucher (HWML no. 35289) of C. montaukensis.DE, dorsal excretory duct; MB, dorsomedian longitudinal muscle band; NC, nerve cord; 0, ovary; T, testes; U,uterus; V, vagina; VE, ventral excretory duct.

RUHNKE-NEW SPECIES OF CLISTOBOTHRIUM 39DESCRIPTIONSClistobothrium carcharodoniDailey and Vogelbein, 1990(Fig. 1)The following information from 4 paratype specimensis provided to emend the description of Daileyand Vogelbein (1990) for C. carcharodoni. Only characteristicsrequiring emendation are given: Wormsapolytic. Maximum width 1,500-1,950 (1,733 + 225;n = 3) at scolex. Strobila with a distinct band of dorsomedianlongitudinal muscles 70-85 (76 ? 6; n = 4)wide in anterior and 50-73 (63 ? 11; n = 4) wide inposterior segments. Cirrus sac L-shaped, 408-670 (564? 91; n = 4; n = 13) long by 145-229 (198 ? 37; n =4; n = 13) wide, containing cirrus. Cirrus coiled, expandedproximally, and armed with spiniform microtriches(Fig. 1). Genital pores lateral, irregularly alternating,positioned in the anterior 60-68% (65 ? 3; n= 5; n = 13) of mature segments; genital atrium present.Vagina medial, extending from ovary anteriorly andcrossing ventrally the proximal portion of cirrus sac,extending laterally to genital atrium, 30-135 (72 ? 34;n = 5; n = 10) wide above cirrus sac in mature segments.Ovary posterior to testes, H-shaped, 210-420(295 + 68; n = 5; n = 11) long by 320-500 (425 +63; n = 5; n = 11) wide. Vitelline follicles 12-30 (21+ 6; n = 4; n = 8) long by 40-80 (59 + 15; n = 4; n=8) wide. Eggs round, 21-24 (23 ? 1; n = 4; n = 9)in diameter, found in terminal and free segments.Taxonomic summaryType host: Carcharodon carcharias Linnaeus, 1758,the great white shark.Type locality: Off Pt. Dume, Los Angeles County,California, 33?55'N, 118?48'W.Site of infection: Spiral intestine.Specimens examined: Paratype specimens USNMno. 80895 and HWML no. 31397.RemarksThe description of C. carcharodoni is emended forseveral reasons. Apparently, Dailey and Vogelbein(1990) were mistaken in their estimation of the size ofthe egg and the width of the scolex in this species.Quantitative values have been added for some of themorphological features of this species and informationalso has been added concerning the dorsomedian bandof longitudinal muscles extending throughout the lengthof the strobila. The length of the cirrus sac has beenremeasured according to the methods used by Caira(1990) to reflect the total length of the structure. Inaddition, Dailey and Vogelbein (1990) described C.carcharodoni as anapolytic. However, an apolytic (free)segment was observed in the paratype series, and theposterior segments of some of the specimens, althoughcontaining eggs, were not completely gravid. Thus, myobservations indicate that the species should be consideredapolytic.Clistobothrium tumidum(Linton, 1922) n. comb.(Fig. 2)The following information is provided to emendLinton's (1922) decription of this species: Wormsslightly craspedote, apolytic. Scolex with dome-shapedapical region and dorsal and ventral pairs ofbothridia.Each bothridium with a single anterior apical sucker,measuring 280-360 (307 ? 35; n = 4; n = 12) and asingle foliose posterior loculus. Strobila with more than100 segments. Strobila with a distinct dorsomedianmuscle band 75-120 (98 ? 32; n = 2) wide in anteriorsegments, 33-62 (49 ? 12; n = 4) wide in posteriorsegments. Mature segments 1,625-1,925 (1,761 ? 106;n = 4; n = 7) long by 1,025-1,800 (1,457 ? 231; n =4; n = 7) wide. Testes 234-307 (282 ? 33; n = 4) innumber in mature segments in dorsal or ventral view,distributed in 2 irregular fields, intravascular. Maturesegments with thin-walled, L-shaped, dorsal cirrus sac(Fig. 2), 316-411 (376 ? 41; n = 4) long by 105-168(126 ? 30; n = 4) wide, opening into genital atrium.Cirrus armed, coiled inside cirrus sac, expanded proximally.Genital pores lateral, irregularly alternating,positioned in the anterior 61-76% (67 ? 4; n = 5; n= 9) of mature segments. Vagina medial, extendinganteriorly, then laterally and anteriorly over proximalportion of cirrus sac (Fig. 2) to genital atrium. Ovaryposterior, H-shaped, 420-520 (477 ? 37; n = 3; n =6) long by 470-600 (538 + 47; n = 3; n = 6) wide inmature segments, bilobed in cross section. Uterus ventral,extending to posterior margin of cirrus sac in maturesegments, extending to anterior margin of cirrussac in gravid free segments. Some free segments witha midventral uterine pore. Eggs round, 20-27 (24 + 2;n = 3; n = 8) in diameter in free segments, surfacemammilated.Taxonomy summarySynonym: Phyllobothrium tumidum Linton, 1922.Type host: Carcharodon carcharias Linnaeus, 1758,the great white shark.Type locality: Woods Hole, Massachusetts.Additional locality: Moriches, Long Island, New York.Site of infection: Spiral intestine.Specimens examined: Lectotype (USNM no. 7631);paralectotypes (USNM nos. 7630 and 7631); voucherspecimen (USNM no. 35802).Specimens deposited: Three voucher specimens(USNM no. 82491) deposited in the U.S. NationalMuseum Helminthological Collection in Beltsville,Maryland, and 3 voucher specimens (HWML no.35290) deposited in the Harold W. Manter Laboratoryof Parasitology, Lincoln, Nebraska.RemarksLinton (1922) described this species as P. tumidumfrom the great white shark. He included an additionalspecimen from the shortfin mako shark in the typeseries (USNM no. 7632), but the specimen is immatureand its conspecificity with C. tumidum cannot be determined.A holotype was not designated by Linton(1922) for this species. I hereby designate as the lectotype1 of the partial worms on the "type" slide cataloguedUSNM no. 7631. This strobila was drawn byLinton and most clearly depicts the segment structureof the specimens in the type series. The remainingspecimens on slides catalogued USNM nos. 7630 and7631 should be considered paralectotypes. Clistobothriumtumidum differs from C. carcharodoni in the shapeof the posterior loculus, diameter of the apical sucker,

40 THE JOURNAL OF PARASITOLOGY, VOL. 79, NO. 1, FEBRUARY 1993and number of testes in mature segments. The 2 speciesalso differ in the length of the cirrus sac and in theposition of the proximal portion of the cirrus sac relativeto the vagina. The description is emended tofacilitate future comparisons with this species. A morecomplete description of this species must await additionalcollections from the type host, C. carcharias.Clistobothrium montaukensis n. sp.(Figs. 3-15)The description is based on 4 whole worms, 13 partialworms, 2 critically point dried scolices with strobilae,eggs from 3 critically point dried free segments,5 free segments, and eggs from 5 free segments: Worms38.5-119.5 mm (73.5 + 34.3; n = 4) long, maximumwidth 2,475-3,750 (3,000 + 522; n = 7) at scolex,apolytic, slightly craspedote. Scolex with large, domeshapedapical region (Figs. 3, 9), apical region coveredwith filiform microtriches (Fig. 10). Scolex 2,100-3,650(3,000 + 544; n = 7) long by 2,475-3,750 (3,000 +522; n = 7) wide, with 2 ventral and 2 dorsal large,foliose bothridia (Fig. 11) each with 1 circular, muscular,anterior accessory sucker 310-500 (372 + 52; n= 9; n = 18) in diameter. Bothridia 1,750-2,125 (1,970+ 159; n = 5) long by 1,350-1,500 (1,465 + 89; n =5) wide. Proximal surface of bothridia covered withslender spiniform microtriches (Fig. 12); distal bothridialsurface not observed. Neck short, 950-3,700(2,110 + 1,125; n = 5) long, covered with filiformmicrotriches (Fig. 13). Strobila with more than 100segments, with distinct dorsomedian muscle band (Figs.4, 5, 14), 63-160 (91 + 33; n = 8) wide in anteriorsegments, 30-58 (45 + 8; n = 9) wide in posteriorsegments. Anterior segments much wider than long,immature segments at midworm 525-800 (669 + 86;n = 4; n = 8) long by 1,050-1,300 (1,191 + 92; n -4; n = 8) wide, mature segments 1,400-3,200 (2,122+ 569; n = 6; n = 13) long by 865-1,212 (1,035 +127; n = 6; n = 13) wide, generally twice as long aswide, with a dorsal and ventral pair of lateral excretoryducts and a pair of lateral nerve cords in cross section(Figs. 6, 7). Testes round, 33-72 (56 + 12; n = 5; n =17) in diameter, numbering 198-263 (242 + 28; n =6; n = 8) in dorsal or ventral view, distributed in 2irregular fields between the ventral excretory ducts incross section (Fig. 6). Vas deferens coiled, medial, inanterior third of segment. Cirrus sac dorsal, L-shaped,proximal portion of cirrus sac immediately posteriorto vas deferens (Fig. 4), 519-737 (638 + 66; n = 4; n10) long by 123-251 (173 ? 39; n = 4; n = 10) wide,opening into a genital atrium. Cirrus long, coiled insidecirrus sac, expanded proximally, covered with slenderspiniform microtriches (Fig. 8). Genital pores lateral,irregularly alternating, positioned in the anterior 57-64% (61 + 3; n = 8; n = 14) of mature segments. Vaginamedial, extending from ovary anteriorly and crossingproximal portion of cirrus sac ventrally and extendinglaterally to genital atrium, 28-170 (78 + 45; n = 6; n=12) wide anterior to cirrus sac. Ovary posterior,H-shaped with conspicuous lateral lobes (Fig. 4), positionedbetween ventral excretory ducts, 330-550 (409+ 83; n = 3; n = 5) long by 375-500 (429 + 48; n =3; n = 5) wide; bilobed and dorsal in cross section (Fig.7). Mehlis' gland posterior to ovary.Uterus ventral (Fig.6), beginning anterior to ovary and extending to pos-terior margin of cirrus sac in mature segments; no uterineduct observed. Uterus extending to anterior marginof cirrus sac in free segments. Free segments 6-7 mm(6.7 + 0.6; n = 5) long by 2-3 mm (2.5 + 0.4; n = 5)wide. Eggs round 21-28 (26 + 1.4; n = 6; n = 35) indiameter, surface covered with small spinose projections(Fig. 15), found only in free segments. Vitellariafollicular, distributed dorsally and ventrally, extendingto median third of segment in cross section (Figs. 6,7), follicles 20-30 (26 + 3; n = 4; n = 11) long by 22-42 (31 + 5; n = 4; n = 11) wide, interrupted by thecirrus sac.Taxonomic summaryType host: Isurus oxyrinchus Rafinesque, 1809, theshortfin mako shark.Type locality: Montauk, Long Island, New York.Additional locality: Yarmouth, Massachusetts.Site of infection: Spiral intestine.Specimens deposited: Holotype (USNM no. 82489)and 8 paratype specimens (USNM no. 82490) depositedin the U.S. National Museum HelminthologicalCollection, Beltsville, Maryland. Additional 9 paratypespecimens (HWML no. 35289) deposited in the HaroldW. Manter Laboratory, University of Nebraska StateMuseum, Lincoln, Nebraska. Remaining paratypespecimens are in the collection of the author.Etymology: The species is named for the type locality.RemarksClistobothrium montaukensis is most similar to C.tumidum in testes number and anterior and posteriorwidth of the dorsomedian band of strobilar muscles.Both species have foliose bothridia. Clistobothriummontaukensis differs from C. tumidum in having alonger cirrus sac (x = 638 vs. x = 376, respectively).In C. montaukensis and C. carcharodoni, the proximalportion of the cirrus sac crosses and lies dorsal to theanterior portion of the vagina, but the cirrus sac doesnot cross the vagina in C. tumidum (Figs. 2, 4). Clistobothriummontaukensis differs from C. carcharodoniin testes number (x = 236 vs. x = 107) and in thefoliose versus lappetlike nature of the posterior bothridialloculus.Clistobothrium Dailey and Vogelbein, 1990Emended generic diagnosis: Phyllobothriidae. Wormsapolytic. Scolex with 2 dorsal and 2 ventral pedunculatebothridia and dome-shaped or cruciform apicalregion. Myzorhynchus absent. Each bothridium withsingle apical, muscular, round sucker. Posterior loculusfoliose or folding flap of tissue. Neck short; immaturesegments wider than long; mature segments at leasttwice as long as wide. Strobila with distinct longitudinaldorsomedian band of muscles. Testes numerous, intervascular,in 2 irregular fields. Cirrus sac extends mediallywith proximal portion directed anteriorly (Lshaped).Cirrus armed with spiniform microtriches.Genital atrium present. Vagina ventral to, and openinganterior to, cirrus sac. Ovary posterior, bilobed in crosssection. Uterus ventral, reaching only to posterior marginof cirrus sac in mature segments; reaching anterior

RUHNKE-NEW SPECIES OF CLISTOBOTHRIUM 41,r *. I., " I;'6t ~ X .. ,v .IB.*:"r"?->^K>FIGURES 9-15. Scanning electron micrographs of Clistobothrium montaukensis. 9. Apical region. 10. Enlargedview of region indicated by triangle in Figure 9. 11. Two bothridia in lateral contraction. 12. Enlarged view ofregion indicated by circle of Figure 11. 13. Enlarged view of region indicated by square of Figure 11. 14. Crosssection of strobila. 15. Egg. ED, excretory duct; LMB, dorsomedian longitudinal muscle band. Scale bar in Figure9, 250 Aum; scale bar in Figure 11, 500 ,im; scale bars in Figures 12 and 13, 2 um; scale bars in Figures 10 and15, 5 ium; scale bar in Figure 14, 100 Aim.

42 THE JOURNAL OF PARASITOLOGY, VOL. 79, NO. 1, FEBRUARY 1993margin of cirrus sac in gravid segments. Egg surfacemammilated or spinose. Parasites of elasmobranchs.RemarksDailey and Vogelbein (1990) considered Clistobothriumto be different from all phyllobothriid genera basedprimarily on its unique scolex structure. The genericdiagnosis is expanded here to include the foliose bothridiaof C. montaukensis and C. tumidum. Clistobothriumdiffers from all other phyllobothriid genera in itspossession of a longitudinal band ofdorsomedian musclesextending throughout the strobila. The L-shapedcirrus sac of these species is also apparently uniqueamong the phyllobothriids.DISCUSSIONOne of the primary aims of systematics is toproduce a taxonomy that is consistent with thephylogenetic relationships of the organisms inquestion, such that taxa are monophyletic sensuHennig (1966). The morphological evidence presentedhere suggests that C. carcharodoni, C.montaukensis, and C. tumidum are members ofsuch a monophyletic group. These species possessa dorsomedian band of muscles that runslongitudinally throughout the strobila. This conditionhas not been described in other tetraphyllideanspecies and is therefore hypothesizedto be synapomorphic for these 3 species. In additionat least 8 other features support the groupingof these species. The worms are of similarsize, have cirrus sacs of similar size and shape(L-shaped), have genital pores similar in positionand eggs of similar size and surface structure,testes in more than 1 dorsoventral field (in crosssection), bilobed ovaries in cross section, and theuterus in these 3 species extends only to the posteriorregion of the cirrus sac in mature, strobilatedsegments. Although the bothridia of C.tumidum and C. montaukensis are similar pheneticallyto the type species of Phyllobothrium,Phyllobothrium lactuca Van Beneden, 1850 (thebothridia are extensively foliose), the structureand nature of the folding and contraction of thebothridia are different. In P. lactuca, the posteriorportions of the bothridia contract anteriorlyfrom a relaxed condition in which the bothridiaare posteriorly bifid (see Euzet, 1959: figs. 46,49). The bothridia of Clistobothrium species contractlaterally (Figs. 3, 11) in a fashion that coversmost of the distal surface of the bothridium, obscuringthe view of the apical sucker, and thebothridia in these 2 species are not posteriorlybifid. Hence, the foliose bothridia of C. tumidumand C. montaukensis cannot be considered homologousto those in species of Phyllobothrium.The cirruses of C. carcharodoni and C. montaukensisare armed with structures that are morphologicallyconsistent with the definition of amicrotriche (Figs. 1, 8), which is an extension ofthe cestode syncytial tegument consisting of acytoplasmic base and a distal electron-dense shaftseparated from the base by a base plate (Thompsonet al., 1980). Previously, tapeworm cirruseshave been described as being spinose or armedwith spines (e.g., Euzet, 1959). Microtriches havebeen described with a bladelike electron-denseshaft that extends proximally to the tegumentarysurface of the worm with no observable cytoplasmicbase. For example, Thompson et al.(1980) described microtriche types ranging fromspiniform to filiform in Proteocephalus tidswelli(Johnston, 1909). These spiniform microtrichesmay appear to be spines at the light microscopicallevel. Future transmission electron microscopicalinvestigations will be needed to confirmwhether microtriches are a general feature of thetapeworm cirrus.With the exception of Dailey and Vogelbein's(1990) description of C. carcharodoni and thedescription of C. montaukensis given here, allother reports of the genus have been of C. tumidum,reported as P. tumidum. This species hasbeen reported from 9 species of elasmobranchsin 3 orders (see Williams, 1968). I believe thereports of Clistobothrium species from lamniformsharks are corroborated because the accountswere accompanied by original drawingsor descriptions of considerable detail (Linton,1922; Euzet, 1959; Williams, 1968; Dailey andVogelbein, 1990), all of which seem to be consistentwith the diagnosis of Clistobothrium. Reportsof Clistobothrium species from other elasmobranchspecies may refer to other tapewormspecies. For example, the reports of C. tumidumfrom Mustelus manazo Bleeker, 1854 (reportedas Cynias manazo) and Triakis scyllium Miillerand Henle, 1839, by Hsii (1935) probably referto P. lactuca and Phyllobothrium serratum Yamaguti,1952, respectively. These 2 species aresubstantially similar phenetically in bothridialstructure to C. tumidum. Thus, additional speciesof Clistobothrium, if in existence, are likelyto be found in sharks of the family Lamnidae(the mackerel sharks).ACKNOWLEDGMENTSI thank J. Ralph Lichtenfels and Mary HansonPritchard for lending type specimens. I also thankJack Casey of the National Marine Fisheries Ser-

RUHNKE-NEW SPECIES OF CLISTOBOTHRIUM 43vice for help in procuring hosts. I thank BobConklin of Riverhead, Long Island, New York,for a rare collection of a fixed great white sharkspiral intestine. Ken Barber, Scott Snyder, andJanine Caira also contributed to collection ofspecimens. Dr. Caira also provided critical commentson this manuscript. This study was supportedin part by NSF grant BRS-9007613 toJanine Caira.LITERATURE CITEDCAIRA, J. N. 1990. A revision of the North Americanpapillose Allocreadiidae (Digenea) with independentcladistic analyses of larval and adult forms.Bulletin of the University of Nebraska State Museum11: 1-58.,AND M. M. GAVARRINO. 1990. Grillotia similis(Linton, 1908) comb. n. (Cestoda: Trypanorhyncha)from nurse sharks in the Florida Keys.Journal of the Helminthological Society of Washington57: 15-20.DAILEY, M. D., AND W. VOGELBEIN. 1990. Clistobothriumcarcharodoni gen. et sp. n. (Cestoda: Tetraphyllidea)from the spiral valve of the great whiteshark (Carcharodon carcharias). Journal of theHelminthological Society of Washington 57: 113-119.EUZET, L. 1959. Recherches sur les cestodes tetraphyllidesdes selaciens des cotes France. Thesesde Ph.D. Faculte des Sciences, Universite deMontpellier, Montpellier, 263 p.HENNIG, W. 1966. Phylogenetic systematics. Universityof Illinois Press, Urbana, Illinois, 263 p.HsO, H. F. 1935. Contributions a l'tude des cestodesde Chine. Revue Suisse de Zoologie 42: 477-570.LINTON, E. 1922. A new cestode from the maneaterand mackerel sharks. Proceedings of the UnitedStates National Museum 64: 1-16.THOMPSON, R. C. A., A. R. HAYTON, AND L. P. JUESUE. 1980. An ultrastructural study of the microtrichesof adult Proteocephalus tidswelli (Cestoda:Proteocephalidae). Zeitschrift fir Parasitenkunde64: 95-111.WILLIAMS, H. H. 1968. The taxonomy, ecology, andhost-specificity of some Phyllobothriidae (Cestoda:Tetraphyllidea), a critical revision of PhyllobothriumBeneden, 1849, and comments on someallied genera. Philosophical Transactions of theRoyal Society of London, Series B 253: 231-307.