Cestodes in Malaysia 2006

7/30/2019 Cestodes in Malaysia 2006

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Three New Species of Rhinebothrium (Cestoda: Tetraphyllidea) from the Freshwater Whipray,

Himantura chaophraya, in Malaysian BorneoAuthor(s): Claire J. HealySource: The Journal of Parasitology, Vol. 92, No. 2 (Apr., 2006), pp. 364-374Published by: The American Society of ParasitologistsStable URL: http://www.jstor.org/stable/40058491 .

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THREE NEW SPECIES OF RHINEBOTHRIUM(CESTODA: TETRAPHYLLIDEA) FROM THEFRESHWATER WHIPRAY,HIMANTURACHAOPHRAYA, IN MALAYSIAN BORNEOClaire J. HealyDepartment fEcology& Evolutionary iology,UniversityfConnecticut, torrs, onnecticut 6269-3043. e-mail:[email protected]

J. ParasitoL,92(2), 2006, pp. 364-374 American ocietyof Parasitologists 006

abstract: Three new Rhinebothriuminton,1890 species,R. kinabatanganensisn. sp., R. megacanthophallus . sp., and R.abaiensis n. sp., collected from hespiral ntestines f 6 freshwater hipraysHimantura haophraya,Dasyatidae) in theKina-batanganRiver,MalaysianBorneo,are described.This is thefirst ecordof cestodes from heKinabatanganRiver and fromH.chaophraya.The new Rhinebothriumpecies are differentiatedrom he 34 validRhinebothriumpecies in addition o 2 species,Echeneibothrium uiTseng,1933 and E. oligotesticularis ubramaniam, 940 that re herein ransferredoRhinebothrium.achof the new species was examined with ight nd scanningelectronmicroscopy.Two of the new species possess cilia on theirbothridia,which have notpreviously een reported ormembers f thisgenus.HimanturachaophrayaMonkolprasit& Roberts,1990 is apotentially bligatefreshwatertingray hathas been reportedfromriverbasins in Thailand, Cambodia, Laos, Vietnam, n-donesian and MalaysianBorneo,Papua New Guinea, and Aus-tralia MonkolprasitndRoberts,1990; Last and Stevens,1994;Kottelat, 001). Verylittle s known about thebiologyof thisray, nd it is currentlyistedbythe World ConservationUnion(IUCN) as critically ndangered n Thailand and vulnerablethroughouthe rest of its distributionSharkSpecialist Group,2000). As part f a survey fthe elasmobranchs nd theirmeta-zoan parasitesofMalaysian Borneo,6 individualsof H. chao-phrayawere collected,withthehelp of local fishermen,romtheKinabatanganRiver n northeastern alaysianBorneo.Pri-or to thiswork,parasites f this pecieswereentirely nknown.Three new species of Rhinebothrium inton, 1890 werefoundamongnumerous ther estode species in the spiralin-testine f H. chaophraya.AlthoughRhinebothriumncludes 48nominalspecies, thisgenus currentlyomprises34 valid spe-cies, the remainderhaving been transferredo othergenera(e.g., Baer, 1948; Mayes et al., 1981; Ball et al., 2003). Inaddition,2 species originallyplaced in Echeneibothrium anBeneden, 1850,E. huiTseng,1933 and E. oligotesticularisub-ramaniam,1940, exhibitfeaturesmoreconsistentwith the di-agnosisofRhinebothriumsensu Euzet, 1994; Ball et al., 2003)in thatthey ack a myzorhynchusnd postvaginaltestes andpossess faciallymultiloculate othridia ividedby a longitudi-nal septum.Therefore,hesespecies arehereby ransferredntoRhinebothriumTable I), as R. hui (Tseng, 1933) n. comb, andR. oligotesticularis Subramaniam,1940) n. comb. The newRhinebothriumpecies described here thus are differentiatedfrom he 36 valid Rhinebothriumpecies listed nTable I. Rhi-nebothriumpecies,as adults, re onlyknown to parasitize hespiral ntestine f batoid fishes Elasmobranchii:Squalea), andhave been reported rommembersof 9 of the 13 families ofbatoidsrecognizedby Shirai 1996).

MATERIALS AND METHODSIn 2003 and 2004, 1 and 5 Himanturachaophrayaindividuals, e-spectively, erecaughtusing ong ines ntheKinabatanganRiver,nearKampungAbai, Sabah, Malaysia. The spiral intestines f these rayswere opened witha longitudinalncision and examined forparasites;cestodeswere found n all 6 individuals.Cestodes wereremovedfromthespiral ntestine r left n situ; n either ase, theywerefixed n 4%

neutralbuffered ormalin or a minimum f 1 wk and subsequentlystored n 70% ethanol.Cestodes prepared s whole mountswere hydratedn 35% ethanoland distilledwater, tained n Delafield's or Gill's hematoxylin,iffer-entiated ntapwater, estained nacidic 70% ethanolfollowedbybasic70% ethanol,dehydratedn 95% ethanol nd 100% ethanol, leared nmethyl alicylate, nd mounted n Canada balsamon glass slides. Ces-tode egg mounts were preparedas follows. Gravid proglottidswereseparatedfrom hestrobila,which was retained s a voucher. he pro-glottidswereplaced in a 1:3 mixture f lactophenol nd 70% ethanol,in an uncovered ontainer nder n exhausthood,overnight. he pro-glottids ubsequentlywere placed on a glass slide in a dropof lacto-phenol, easedopenwith nsectpinsto releasetheeggs from heuterus,the arger ieces ofproglottidemoved, nd theremainder lacedundera coverslipand sealed with nail polish.Cestodes prepared s histolog-ical sections were dehydratedn a graded ethanol series,cleared inxylene, mbedded nparaplastSherwoodMedical Industries,t.Louis,Missouri), and 7 u>m ections were cut using an OlympusCUT4060retracting otarymicrotome. ections were affixed o glass slides witha 3% sodiumsilicate olution; he lidesthenwere stained n Delafield'shematoxylin,ounterstainedn eosin,differentiatedn Scott'ssolution,dehydratedn a gradedethanolseries,clearedin xylene, nd mountedin Canada balsam. Specimens preparedforscanningelectronmicros-copy (SEM) were hydratedn a gradedethanolseries,placed in 1%osmium tetroxide or 10-24 hr,dehydratedn a gradedethanol eries,driedusing hexamethyldisilizaneTed Pella, Inc.,Redding,California),mounted n aluminum tubsusingdouble-sided arbon ape, ndsputtercoated with 10 nm ofgold/palladium.EM was performed ith LEO/Zeiss DSM982 Gemini field missionscanning lectionmicroscope.Measurementswere takenusing a computervideo imaging systemconsisting f a HitachiHV-C20 video camera mounted n a Zeiss Ax-ioscope and an image analysis program, mage ProExpress. Linedrawingswere made usinga camera lucida.All measurements ere takenfrommature roglottidsacking n ex-pandedvas deferens nd arepresentednmicrometers,nlessotherwisenoted. For each measurement,he range is given in the text;mean,standarddeviation,number of measurementsmade, and numberofworms examined(if more than 1 measurementwas made perworm)are given in Table II. Microthrix erminology ollows Faliex et al.(2000). The followingmuseum bbreviationsppear nthe text: PMB,InstitutenyelidikanMarin Borneo BorneoMarine Research nstitute),UniversitiMalaysia Sabah, Kota Kinabalu, Sabah, Malaysia; LRP,LawrenceR. PennerParasitology ollection,UniversityfConnecticut,Storrs, onnecticut, nitedStates;MZUM(P), MuziumZoologi, Univ-ersitiMalaya,Kuala Lumpur,Malaysia;USNPC, United tatesNationalParasiteCollection, Beltsville,Maryland,United States.

DESCRIPTIONRhinebothriumkinabatanganensis n. sp.(Figs. 1-5, 18-21)Measurementsbased on whole mountsof 6 completeand 1 partialmatureworms nd 1 SEM specimen.Worms uapolytic, .16-6A\ mmlong; maximumwidth402-562 located at level ofscolex; 29-51 pro-glottids erworm.Scolex consisting f scolex proper earing stalkedbothridia nd cephalic peduncle.Bothridia acking ateral onstrictions,Received 7 January 005; revised 19 April2005; accepted20 April2005.

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HEALY- THREE NEWSPECIES OF RHINEBOTHRIUM 365

Table I. Validspecies fRhinebothrium,ncludingwo new combi-nations.RhinebothriumaeriEuzet, 959R. biorchidumuber Schmidt,985R. burgeriaer, 948R. cadenati uzet, 954R. ceylonicumhipley Hornell,906R. chilensisuzet& Carvajal, 973R. chollaensisriggens Duszynski,005R. corymbumampbell, 975R.devaneyirooks Deardoff,988R. ditesticulumppy& Dailey,1977R. euzetiWilliams,958R.flexile inton, 890R.ghardaguensisamadan, 984R.gravidumriggens Duszynski,005R. hawaiiensisornford,974R. himanturiilliams,964R. hui Tseng, 933)n. comb.R. leiblei uzet& Carvajal, 973R. lintoni ampbell, 970R. maccallumiinton, 924R.margaritenseayes& Brooks, 981R. monodi uzet, 954R. oligotesticularisSubramaniam,940)n. comb.R.paratrygoniego& Dias, 1976R.pearsoni utler,987R. rhinobatiailey& Carvajal, 976R. scobinae uzet& Carvajal, 973R. setiensisuzet, 955R. spinicephalumampbell, 970R. taeniuri amadan, 984R. tetralobatumrooks, 977R. tumidulumRudolphi,819)Euzet, 953R. urobatidiumYoung, 955)Appy& Dailey, 977R. verticillatumSubhaprada,955)Ramadan, 984R.walga Shipley Hornell, 906)Euzet, 959R. xiamenensis ang& Yang, 001349-579 ong,maximum idth 90-388 ocated t middle rslightlyanterioromiddle fbothridium,ivided y16-21transverseepta nd1 ongitudinaleptumnto 3-43 oculi. ongitudinaleptumxtendingfrom osterior arginfanteriormostoculus oposterior arginfbothridium.nteriormostoculus ingle, 6-70 ongby49-73wide;2posteriormostoculi, ach42-44 longby32-64 wide;widestoculus20-28 longby123-171wide, ocated t middle f bothridium.talksshort,angingromnconspicuouso42-81 ong y73-127wide; talkattachedobothridiumlightlynterioro middle fbothridium.e-phalic eduncle0-156 ong,with istinctosterior argin.Distal ndproximalFig. 19) bothridialurfacesearing ongfili-trichesnd bladelikepinitriches;n both urfaceslong dgeofbo-thridium,pinitrichesbsent ut ilitrichesresent.othridialims ear-ingnarrowandofconspicuouslyonger ilitriches.othridialtalks(Fig.20) and trobilarurfacesFig.21) bearingongfilitriches.Proglottidsraspedote.osterior-13 proglottidsature;-7 ter-minalproglottidsithgreatlyxpanded as deferens.erminalro-glottids09-667 ongby125-197wide, ometimes ith pent estes,with enital ore ocated 4-58% of engthrom roglottidosteriormargin.estes 7-34 ongby33-60wide,10-15 nnumber,rrangedin 2 columnsxtendingrom nterior arginfproglottido anteriormarginfvagina;postvaginalestes bsent.Remainderf measure-mentsaken romerminalroglottidsithxpandedas deferens:en-ital trium-18 longby23-42 wide, urroundedydarkly tainingcells.Vas deferensosteriorlyxpanded,xtendingromevelofovar-ian sthmuso cirrusac,then arrowingndcoiling o levelofpos-teriormostow of testes,nteringnterior arginf cirrus ac near

genital ore, ulk f vas deferensnterioro cirrusac.Cirrusac thin-walled, yriform,traightrslightlyngled osteriorly,19-126 ongby77-80wide; irrus 0-34wide, earingpinitriches.agina peninganteriorocirrusngenitaltrium,inuous,urroundedydarklytain-ing ells;poralportionxpanded,hick-alled, xtendingromenitalatriumlong nterior arginfcirrusac,acrossmidline fproglottidtoapproximateporal imit f cirrusac; medial ortionbruptlyar-rowed,xtendingosteriorlyndrecurvingowardmidline fproglot-tid; erminalortionbruptlyxpandednto eminal eceptacle. varytetralobedn crosssection, -shapedn dorsoentral iew,148-226longby150-192 wide.Vitelline ollicles blong, 5-20 ongby46-61wide, rrangedn4 columns f ingle ollicles,dorsal nd1ventralcolumnn eachsideofproglottid,ot eachingnterior arginfpro-glottid,xtendingoposterior arginfproglottid,lightlyosterioroovary, nterruptedorsallyndventrallyt genital oreand ovarianisthmus.terusxtendingnteriorlyromocapt egiono nterior ar-ginofproglottid.ravid roglottidsot een.Taxonomic summary

Typehost:HimanturahaophrayaMonkolprasit Roberts, 990,freshwaterhipray.Additionalosts:None.Locality: ampung bai 0545.184'N, 1823.070'E), inabatanganRiver,Malaysian orneo.Additionalocalities:None.Siteof nfection:piralntestine.Holotype:MZUM(P) 155.Paratypes:PMB77.14.02, RP 3738-3739, SNPC 96426.Etymology:hisspecies s named or tstype ocality,heKinaba-tangan iver.

RemarksRhinebothriuminabatanganensisiffersrom ll other hineboth-Hum pecies orwhich here re data nproglottidorphologynpos-sessing itellineollicles hat re nterruptedt the evelofthe varianisthmus. lthoughhis haracters unknownrom hinebothriumpe-cies, t is known rom ther etraphyllideans,ncluding,or xample,several peciesofAnthocephaluminton, 890 andParaorygmato-bothriumuhnke, 994.All other hinebothriumpecies ossess ol-umns fvitellineollicles hat reuninterruptedtthe evel f he vary

or, n R. ghardaguensisnd R. monodi, o notreach he eveloftheovary. ataon this haracterre acking orR. ceylonicum,.flexile,R. himanturi,nd R.paratrygoni.he ast3 species ossessbothridiathat remediallyonstricted,nlike .kinabatanganensis,hich acksa bothridialonstriction;achof these species lso possessesmorenumerousothridialoculi han .kinabatanganensis~60-80, 54,and~60 loculi n R.flexile, . himanturi,ndR.paratrygoni,espectively,versus 3-43 in R. kinabatanganensis).he much reaterotalengthandscolex width f R. ceylonicumabout .8 cm and4 mm, espec-tively)learly ifferentiatetfrom .kinabatanganensis2.76-6.41mmand402-562, espectively).lthough ost hinebothriumpecies os-sess a single osteriormostoculus, hepairofposteriormostoculi nR. kinabatanganensiss notunique mongRhinebothriumpecies. ntaxawith pair fposteriormostoculi, he ongitudinaleptumxtendsall theway otheposterior arginf thebothridium,atherhan top-ping t the nterior arginf theposteriormostransverseeptum,sin taxawith single osteriormostoculus. hischaracterlso is seenin R.ghardaguensis,.maccallumi,. rhinobati,. setiensis,. tetra-lobatumbasedon examinationf 5 paratypes,WML 20253 and20266),andR. tumidulum.t is unclear orR. ceylonicum,. hui,R.oligotesticularis,. paratrygoni,ndR. taeniuri. ikewise, lthoughmost hinebothriumpecies ossess othridiahat re learlyonstrict-ed at somepoint long heirength, . kinabatanganensis,n additionto R. ceylonicum,. cadenati, . ghardaguensis,. lintoni,. maccal-lumi, .monodi, . rhinobati,.setiensis,ndR.tumidulum,acks hisconstriction.monghe pecies hat xhibit oth f hese nusualraits,R.kinabatanganensiss most imilaroR.ghardaguensis.hese peciesmaybe furtheristinguishedased on thenumberfproglottids22-25 in R.ghardaguensisersus 9-51 in R. kinabatanganensis)nd heshape nd size ofvitelline olliclesroundnd, tmost, 3 wide n R.ghardaguensisersusblongnd46-61wide nR.kinabatanganensis).



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366 THE JOURNALOF PARASITOLOGY,VOL. 92, NO. 2, APRIL2006

Table II. Measurements fmorphological eatures f Rhinebothriumpecies.Character* R. kinabatanganensis . sp. R. megacanthophallus . sp. R. abaiensis

Total lengthmm) 4.59 1.39; 6 6.66 1.92; 14 3.56 0.77; 9Scolex maximumwidth 492.4 69.3; 4 780 185; 11 740 159; 6Number fproglottids 43.7 8.1; 6 31.3 7.1; 14 15.3 2; 9Bothridiumength 476.6 102.8; 5; 4 638 87; 17; 9 633 60; 11; 6Bothridiummaximumwidth 275.4 64.7; 7; 6 221 23; 11; 8 227 33; 8; 7Number ransverseepta 18.4 1.9; 7; 4 28.3 1.1; 21; 14 24.8 0.7; 8; 7Numberbothridialoculi 37.9 3.8; 7; 4 54.6 2.1; 21; 14 47.5 1.4; 8; 7Anteriormostoculus length 53.5 10.7; 8; 5 34 3; 16; 10 31 5; 13; 10Anteriormostoculus width 61.4 9.3; 11; 6 43 6; 21; 13 47 9; 16; 10Posteriormostoculus length 43.5 1.3; 2 30 5; 11; 9 32 6; 9; 7Posteriormostoculus width 44.5 10.6; 10; 6 38 7; 22; 14 45 8; 11; 9Widest oculus length 23.4 2.9; 6; 5 29 4; 23; 13 29 4; 13; 10Widest oculuswidth 145 17; 6; 5 109 16; 14; 9 116 15; 11; 8Stalklength 56 15; 8 166 62; 24; 14 137 24; 14; 9Stalk width 102 19; 8 107 14; 24; 14 109 24; 15; 9Cephalic peduncle engthmm) 67.2 46.6; 6 132 30; 14 74 11; 7Numberofmature roglottids 6.3 3.6; 7 3.9 1.7; 17 1.0 0.6; 9Numberofgravid proglottids NA NA 2.6 0.7; 11Terminaltproglottidength 489.9 107; 9; 5 1,217 279; 9 350 92; 11; 10Terminaltproglottid idth 160.8 22.1; 9; 5 223 40; 8 282 39; 11; 10Terminaltproglottid enitalpore position %) 53.7 4.8; 9; 5 73 4; 9 54.8 3.7; 11; 10Genital atriumength 9.4 3.5; 8; 5 59 13; 8 18 5; 12; 11Genital atriumwidth 24.1 6.5; 8; 5 50 5; 8 38 7; 12; 11Numberof testes 12.8 1.5; 14; 7 13.6 2.1; 30; 16 17.7 1.7; 16; 9Testis ength 23.6 4.6; 14; 7 40 6; 6; 3 27 5; 20; 10Testis width 46 7.2; 14; 7 71 16; 6; 3 78 13; 20; 10Cirrus ac length 81.5 19.4; 12; 7 234 21; 9 113 17; 11Cirrus ac width 41.1 6; 12; 7 100 15; 8 51 13; 11Cirruswidth 28 5; 9; 5 54 6; 8 29 6; 11Ovary length 174.2 39.1; 10; 5 610 174; 9 158 37; 11; 10Ovarywidth 113.7 33.9; 10; 5 127 38; 8 173 20; 12; 11Vitellinefollicle ength 16 3; 10; 5 26 7; 18; 9 14 4; 22; 11Vitellinefollicle width 41 11; 10; 5 34 9; 16; 8 36 8; 22; 11* All measurementsregiven n micrometers nlessotherwise oted.All measurementsrepresenteds mean followedbystandard eviation, umber f measurementsmade, and number f worms examined f differentromnumber fmeasurementsmade.t Terminal roglottids: roglottids ith xpandedvas deferens orR. kinabatanganensis nd R. megacanthophallus,mature roglottidsorR. abaiensis.

A ciliumwas observed on theproximalbothridial urface fR. kin-abatanganensis.Rhinebothriummegacanthophallus n. sp.(Figs.6-11,22-27)Measurements ased on whole mounts f 14 completeand 5 partialmatureworms, slides ofproglottidrosssections,1 slide of bothridialcrossand longitudinalections, nd 3 SEM specimens.Worms uapol-ytic,3.6-10.33 mmlong; maximumwidth568-1,204 located at levelof scolex; 20-45 proglottids er worm. Scolex consistingof scolexproperbearingremnantpical organ,4 stalkedbothridia,nd cephalicpeduncle.Bothridia 27-863 long,maximumwidth172-257 located nanterior alf of bothridium,aterally onstricted,3-145 wide at con-striction,ividedby 26-30 transverse epta and 1 longitudinal eptuminto50-58 loculi (13-14 loculi on either ide of longitudinal eptumanterioro constriction,1-14 loculi on either ide of longitudinalep-tumposterior o constriction).Bothridialconstrictionacking loculi,bearing2 additional, educedtransverseepta; locular nterruption2-36 long. Longitudinal eptumextending romposteriormargin f an-teriormostoculus to anteriormarginof posteriormostoculus. Anter-iormost oculus single,28-38 long by 34-53 wide; posteriormostoc-ulus single,25-43 long by 26-48 wide; widest oculus 24-42 long by85-136 wide, locatedanterior o bothridial onstriction.talks 92-371longby85-134 wide,attached o bothridiumnterior o bothridial on-striction. ephalic peduncle99-192 long,with distinct osteriormar-gin.

Apex of scolex proper nd strobila Fig. 27) bearingonly long fili-triches. istal bothridial urfacesFig. 23) bearing ladelike pinitrichesand long filitrichesn longitudinalnd transverseeptaand centers floculi,peripheryf loculi bearingonly ong filitriches;n central, on-stricted egion, ilitrichesre longer han nother arts fdistal urfaceand longer han distalspinitriches. othridial im see Fig. 24) bearinga narrow band of conspicuously ong filitriches. roximal bothridialsurfaces Figs. 24 and 25) bearingbladelikespinitrichesnd longfili-triches, pinitrichesacking n narrowband along edge of bothridiumthatwidens on proximal urfaces f anterior- nd posteriormostoculi.Stalks (Fig. 26) and cephalic peduncle bearingbladelike spinitrichesand long filitriches.Proglottids raspedote,with longitudinalmuscles forming iscretebundles visible in cross section. Posterior1-7 proglottidsmature; er-minalproglottid f some individualswithgreatly xpandedvas defer-ens, 760-1,651 long by 183-290 wide withgenital pore located 66-76% of length rom roglottid osteriormargin, ometimeswith penttestes; matureproglottidswithout xpanded vas deferens408-1,327long by 154-298 wide withgenitalpore ocated 55-73% of ength romproglottid osteriormargin.Genital atrium 3-54 long by36-83 wide,surrounded y darkly staining ells. Testes 10-18 in number, 7-54long by 42-87 wide, arranged n 2 columnsextending rom nteriormargin f proglottido level of vagina or cirrus ac; postvaginal estesabsent. Vas deferensposteriorly xpanded at level of cirrus ac, thennarrowing nd coiling to level of posteriormost-5 rows of testes,entering nteriormarginof cirrus sac near genital pore, bulk of vas



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Figures 1-5. Rhinebothriuminabatanganensisn. sp. (1) Scolex. (2) Single open bothridium.3) Matureproglottid.4) Matureproglottidwith xpandedvas deferens.5) Whole worm.

deferens nterior o cirrus ac. Cirrus sac thick- alled, oval, straight,lying vertically r angled posteriorly,24-218 long by 60-140 wide(204-267 long by 80-120 wide in terminal roglottidsn whichvasdeferens s expanded); cirrus 2-66 wide,bearing onspicuously argespinitriches 4-26 long by 12-24 wide. Vagina opening anterior o

cirrus n genitalatrium, inuous,surrounded y darkly taining ells;poral portionexpanded, thick-walled, xtendingfromgenitalatriumalonganteriormargin fcirrus ac, sometimeswith nterior ink, crossmidline of proglottido approximate poral limitof cirrus ac; medialportion bruptly arrowed, xtending osteriorlynd recurvingoward



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Figures 6-11. Rhinebothriwn egacanthophallus . sp. (6) Scolex. (7) Matureproglottid,entral iew. (8) Matureproglottid ith xpandedvas deferens, orsal view. (9) Whole worm. 10) Proglottidross section at level of testes. 11) Proglottidross section t level of ovary.midlineof proglottid; erminal ortion bruptly xpanded into seminalreceptacle. Ovary tetralobedn cross section, n dorsoventral iew H-shaped ventrally nd inverted--shaped dorsally Figs. 7, 8, 11), i.e.,withposterior egionsof dorsal lobes fused,169-597 long by 92-218wide (345-887 long by 88-180 wide in terminal roglottidsn whichthevas deferens s expanded).Vitellinefollicles 10-47 long by 13-48wide, arranged n 4 columns of singlefollicles,1 dorsal and 1 ventralcolumn on each side ofproglottid, otreaching nteriormargin fpro-glottid, xtending oposteriormargin fproglottid,lightly osterior o

ovary,uninterrupted.terus xtendsposteriorlyrom ocaptregionbe-tween ventralovarian lobes beyond posteriormarginof ovary,thenanteriorlyntoanterior a f proglottid, otreaching nteriormargin fproglottidr vitelline ollicles.Gravidproglottids ot seen.Taxonomic summary

Typehost: Himanturachaophraya Monkolprasit& Roberts, 1990,freshwater hipray.



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Figures 12-17. Rhinebothriumbaiensis n. sp. (12) Scolex. (13) Matureproglottid, entralview. (14) Whole worm. 15) Proglottidrosssection t level of testes. 16) Proglottidross section at level of ovary. 17) Egg.Additionalhosts: None.Locality:KampungAbai (0545.184'N, 11823.070'E), KinabatanganRiver,MalaysianBorneo.Additional ocalities:None.Siteofinfection: piral intestine.Holotype:MZUM(P) 156.Paratypes: PMB 77.14.03, LRP 3740-3747,USNPC 96423-96425.Etymology: his species is named for the large spinitriches n itscirrus.

RemarksRhinebothrium egacanthophallusan be distinguishedrom ll oth-er Rhinebothriumpecies for whichthere re data on proglottidmor-phology npossessinga tetralobed varythat ppearsH-shaped n ven-tral view and inverted-A-shapedn dorsal view because theposterior,dorsal ovarian obes are fused. Data on thischaracter re notavailableforR. ceylonicum r R. paratrygoni,whichmaybe distinguishedromR. megacanthophallus y theirgreater ength 5.8 cm and 23 mm,re-



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370 THE JOURNALOF PARASITOLOGY,VOL. 92, NO. 2, APRIL 2006

Figures 18-21. Scanning electronmicrographs f Rhinebothriumkinabatanganensis . sp. (18) Scolex; transverseepta (1 indicatedbyan arrowhead) nd longitudinaleptum arrow) visible n theopen bo-thridium.19) Proximalbothridialurface. 20) Stalksurface. 21) Pro-glottid urface. cale bars: 18, 100 u,m;19-21, 2 |xm.

spectively, ersus3.6-10.33 mm n R. megacanthophallus) nd, in thecase of R. ceylonicum, reater colex width 4 mmversus568-1,204inR. megacanthophallus),ndR. paratrygoni, ewer estes 5-6 versus10-18 inR. megacanthophallus). he extremelyargesize ofthe cirrusspinitriches f R. megacanthophallus lso may prove to be uniqueamongRhinebothriumpecies,but thisfeature as notbeen quantifiedformost species. Rhinebothriummegacanthophalluss relativelyun-usual in thatthe constricted ortionof its bothridium onspicuouslylacks loculi. However, hisfeature s also seen inR. baeri,R. biorchid-um,R. chilensis,R. ditesticulum,. leibeli,R.pearsoni,and R. scobinaeand is unclear nR. hawaiiensis,R. hui,R. paratrygoni, . taeniuri, ndR. verticillatum.f these,R. megacanthophalluss most similar o R.hui,R. pearsoni,R. taeniuri, nd R. verticillatum,utmaybe distin-guishedfromR. hui based on the number f columns of testes 3-4versus2), fromR. pearsoni based on the number f bothridial oculi(32 versus50-58), fromR. taeniuribased on the number ftestes 4-8 versus 10-18), and fromR. verticillatum ased on the numberofproglottidsnd total ength76-1 15 and 33 mmversus20-45 and 3.6-10.33 mm n R. megacanthophallus).

A narrowband of spinitriches ncircling he anteriormargin f ma-tureproglottids as seen with ightmicroscopy, ut not confirmed ithSEM.Rhinebothrium baiensis n. sp.(Figs. 12-17, 28-35)

Measurements ased on whole mountsof 9 completeand 3 partialmatureworms,2 slides of proglottidross sections,2 slides of eggs,and 2 SEM specimens.Worms polytic, .8-4.78 mm ong;maximumwidth 99-935 locatedat level of scolex; 13-19 proglottids erworm.Scolex consistingof scolex proper bearingremnant pical organ,4stalkedbothridia nd cephalicpeduncle.Bothridia 97-714 long,max-imum width170-263 located nanterior alfofbothridium,ividedby24-26 transverseeptaand 1 longitudinaleptumnto 6-50 loculi 11-12 loculi on either ide of longitudinal eptum nterior o constriction,11-12 loculi on either ide of longitudinaleptumposterioro constric-tion).Bothridia aterally onstricted;onstriction9-168 wide, ackingloculi,bearing2 additional, educed transverse epta; locular nterrup-tion 15-52 long.Longitudinal eptum xtending rom osteriormarginofanteriormostoculus to anteriormargin fposteriormostoculus.An-teriormost oculus single, 18-39 long by 30-62 wide; posteriormostloculus single,19-41 longby 34-58 wide; widest oculus 18-33 longby 83-136 wide. Stalks 103-191 long by 78-139 wide, attachedtobothridia t or slightly nterior o bothridial onstriction. ephalic pe-duncle 55-87 long,withdistinct osteriormargin.Distal bothridial urfacesFigs. 29-3 1 bearingbladelike pinitrichesand long filitriches n longitudinalnd transverseeptaand centers floculi; anterior ndposteriorwalls of oculibearing nly ongfilitriches;in central, onstricted egion,filitrichesongerthan n otherpartsofdistal surfaceand longerthan distal spinitriches. othridialrim seeFig. 29) bearing narrow and of conspicuously ongfilitriches.rox-imal bothridialurfacesFig. 32) bearing ladelike pinitrichesnd ongfilitriches,pinitrichesacking n narrow andalong edge of bothridiumthatwidens on proximal urfaces f anterior- nd posteriormostoculi.Stalks Fig. 33) and cephalic peduncle Fig. 34) bearingbladelike pin-itriches nd longfilitriches.trobila Fig. 35) bearing nly ongfilitrich-es.Proglottidscraspedote;9-13 immature roglottids,-2 mature ro-glottids, -4 gravid proglottids.Matureproglottids 20-507 long by224-335 wide withgenitalpore located 49-60% of length rompro-glottid posteriormargin.Genital atrium10-32 long by 29-57 wide,surroundedy darkly taining ells. Testes 18-40 long by59-105 wide,15-21 innumber,rrangedn 2 columns xtending rom nteriormarginofproglottido level ofvaginaor anteriormargin fovary; postvaginaltestes bsent.Vas deferens otexpanded, xtending rom osteriormar-gin of cirrus ac or anterior obes of ovary to level of posterior -3rows of testes, nteringnteriormargin f cirrus ac neargenitalpore,bulk of vas deferens nterior o cirrus ac. Cirrus ac thin- alled,pyr-iform, traight, ngledposteriorly,9-138 long by 35-80 wide; cirrus21-40 wide, bearing pinitrichesess than 6 long. Vagina opening n-terior o cirrus n genital trium,inuous, urroundedydarkly tainingcells; poral portion xpanded, hick-walled,xtending rom enital tri-um along anteriormargin f cirrus ac across midlineof proglottidoapproximate poral limit of cirrus ac; medial portion hort, bruptlynarrowed, xtending osteriorlynd recurving owardmidlineof pro-glottid;terminalportionabruptly xpanded into seminal receptacle.Ovary tetralobedn cross section,H-shaped ventrallynd inverted-A-shapeddorsally Figs. 13, 16) in dorsoventral iew, .e., withposteriordorsal lobes fused,103-219 long by 145-211 wide. Vitellinefollicles7-20 long by 20-53 wide, arranged n 4 columns of singlefollicles,1dorsal and 1 ventral olumn on each side of proglottid, otreachinganteriormargin f proglottid,xtending oposteriormargin fproglot-tid, lightly osterior oovary,uninterrupted.terus xtends osteriorlyfrom ocapt regionbetweenventral varian obes beyondposteriormar-ginof ovary, nteriorlyntoanteriorV4of proglottid, otreaching n-teriormarginof proglottid. ravidproglottids 72-939 long by 226-347 wide, may containeggs with hexacanths.Eggs single,with1-2polarfilaments,mbryonatedn utero.Taxonomic summary

Typehost: Himanturachaophraya Monkolprasit& Roberts, 1990,freshwater hipray.



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Figures 22-35. Rhinebothrium egacanthophallus . sp. (scanningelectronmicrographs2-27). (22) Scolex. (23) Distal bothridial urface.(24) Proximal bothridial urfaceof posteriormostoculus. (25) Proximal bothridial urface way frombothridial dge. (26) Stalk surface. 27)Proglottid urface. 28-35. R. abaiensis n. sp. (28) Scolex. (29) Distal bothridial urfaceof entire oculus. (30) Distal bothridial urface oflongitudinaleptum. 31) Distal bothridial urfaceat edge of loculus wall, note cilium. (32) Proximal bothridial urface way frombothridialedge. (33) Stalk surface. 34) Cephalic peduncle surface. 35) Proglottidurface. Scale bars: 22, 28, 200 |xm;24, 3 |xm;25-27, 31-35, 2 |xm;29, 20 M-m;0, 5 u,m.



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372 THE JOURNALOF PARASITOLOGY,VOL. 92, NO. 2, APRIL 2006

Additionalhosts:None.Locality:KampungAbai (0545.184'N, 11823.070'E), KinabatanganRiver,MalaysianBorneo.Additional ocalities:None.Site of infection: piral intestine.Holotype:MZUM(P) 154.Paratypes: IPMB 77.14.01, LRP 3734-3737, USNPC 96423-96425.Etymology: his species is namedforthe town of KampungAbai.Remarks

Rhinebothriumbaiensis and R. megacanthophallusre theonlyspe-cies of Rhinebothrium nownto possess a tetralobed vary that s H-shaped in ventralview and invertedA-shaped in dorsal view becausethe posterior, orsal ovarian lobes are fused. However,data on thischaracter re notavailable forR. ceylonicum r R. paratrygoni,whichmaybe distinguishedromR. abaiensis by their reater ength 5.8 cmand 23 mmversus2.8-4.78 mm n R. abaiensis) and,in the case of R.ceylonicum, reater colex width 4 mm versus499-935 in R. abaien-sis)y nd R. paratrygoni, ewer estes 5-6 versus 15-21 in R. abaien-sis). Rhinebothriumbaiensis is most similar o R.megacanthophallus.However,whereasR. megacanthophalluss euapolytic, ossesses cirrusmicrotricheshat re at least 14-26 long,50-58 bothridialoculi, anda cephalic pedunclethat s 99-192 in length,R. abaiensis is apolytic,possesses cirrusmicrotrichesess than 6 long,46-50 bothridialoculi,and a cephalicpedunclethat s 55-87 in length.This species is consideredhere to be apolytic,but a fewspecimensexhibitedmultipleproglottidshat ppearedto have released some oftheir ggs through ventral ehiscence at the evel of thegenitalpore.This aspectof thebiologyofthis peciesremains o be verified.solatedcilia were seen in regionsof the bothridial oculi lacking spinitriches(Fig. 31); a row of widely spaced cilia was seen near theedge of thebothridium n the proximalsurface of the posteriormostoculus. Anarrowband of spinitrichesncircling he anteriormarginof matureandgravidproglottids as seenwith ightmicroscopy utnot onfirmedwithSEM.DISCUSSION

A list of the36 valid species ofRhinebothriumTable I) wascompiledthroughn examination fthe iterature,ased on thediagnosticcharactersgiven by Euzet (1994) and Ball et al.(2003) forthisgenus. Accordingto theseauthors,Rhineboth-riumspecies are characterized,n part,by theirpossession ofbothridia hat are divided into facial loculi by 1 longitudinalseptum nd more than 1 transverseeptum ndbytheir ack ofpostvaginal estes.All species ofRhinebothrium,xceptR. cad-enati and R. monodi, xhibit hese characteristics.hese last 2species lack a longitudinal othridial eptumand, in thisre-spect,are moreconsistentwiththediagnosisof Scalithrium,genuserectedby Ball et al. (2003) to accommodatetetraphyl-lidean species exhibiting ll of theRhinebothriumharacteris-ticsexceptthe ongitudinal othridialeptum.Ball et al. (2003),however, id nottransfer . cadenati and R. monodi to Scalith-rium.These species remain n Rhinebothriumwaitingreex-aminationand taxonomicreassessment,because theirscolexmorphologies re unusual in otherways,makingtheirgenericplacement mbiguous.Two additionalspecies includedhere in Rhinebothriume-quire comment.Tseng (1933) describedEcheneibothrium ui,fromDasyatis akajei in Qingdao of Shandong Province innortheast hina, as 15 mm in total ength, ossessing stalkedbothridia hat re divided into 2 halves by a transverse inge,i.e., laterally onstricted, rows ofabout24 loculi perbothrid-ium,12 testes ocated nthe anterior alfof theproglottidnonepostvaginal),and 40-50 proglottids er worm. Subramaniam(1940) described E. oligotesticularis, romRhinobatus [sic]

granulatus, s 20 mm n length, ossessing4 stalkedbothridia,each with a transverse inge, .e., laterally onstricted,nd di-vided by transverse nd longitudinal epta into2 rows of 18-26 loculi,4-7 testes none postvaginal), nd 66 proglottids erworm. A myzorhynchus as neither escribednordepicted nthe description f eitherspecies. Rhinebothrium iffers romEcheneibothriumn that ts species lack a myzorhynchus,.e.,apical organ, n the scolex. Based on this riterion,oth peciesare herein transferredo Rhinebothrium,ecomingR. hui n.comb, and R. oligotesticularis . comb.Examination f the 3 new Rhinebothriumpecies withSEMrevealed thepresenceof cilia on the bothridia f 2 of thespe-cies and complicatedmicrothrix istribution atterns,whichmay lead to changes in theway bothridialmicrothrixatternsare treatedn phylogenetic nalyses.Cilia, observed n R. kin-abatanganensisand R. abaiensis, have not beenreportednthefew other Rhinebothriumpecies for which microthrix atahave been published,R. corymbum, . pearsoni, R. spinice-phalum,and R. urobatidiumButler,1987; Caira et al., 2001).However,thepresenceof cilia on the scolices of a few othertetraphyllideansas been reported, orexample, in Phoreiob-othrium inton,1889 species (Caira et al., 1996). Unlike anyotherRhinebothriumpecies forwhichmicrothrixatterns avebeen characterized, . kinabatanganensis, . megacanthophal-lus, andR. abaiensis appearto exhibit microthrixistributionpattern n theedges of the bothridia hatdiffers rom here-mainder f theproximalbothridialurface. n addition, he ast2 species exhibitmicrothrix istributionatternsn theperiph-eryof thebothridial ocular surfaces hat iffer rom hose eenon the remainder f the distal bothridial urface.The onlyothertetraphyllideanaxa in whichtheproximalbothridialdges areknownto lack spinitriches hat are present lsewhereon theproximal surfaces are 4 Anthocephalumspecies (Ruhnke,1994a). The onlyother etraphyllideanpeciesknown o exhibitvariation n spinithrix resenceor shapebetweendifferentartsof the distal surfaces are Cardiobothriumeveridgei,Crosso-bothrium ohrnii,Crossobothriumaciniatum,Paraorygmato-bothrium rionacis, and P. barberi (Ruhnke,1994b; Ruhnke,1996; McKenzie and Caira, 1998). All 3 of the new speciesdescribed here possess a narrowband of conspicuously ongfilitricheslong the rims of theirbothridia.These microthrixdistributionatterns uggestthatrather hantreatinghe distaland proximal urfaces ach as singleunitswhendefininghar-acters forphylogenetic nalyses (e.g., Caira et al., 1999 and2001), thesesurfacesmoreappropriately ould be divided ntocomponentpartsforcomparisonof microthrixatterns mongsome taxa.Additionally,hemicrothrixatternn thebothridialrim hould be assessed separately rom hose on the other oth-ridial surfaces.Like several other Rhinebothriumpecies, R. megacantho-phallus and R. abaiensis exhibit a conspicuous,central nter-ruption f theirbothridial oculi at the level of the bothridialconstriction.he otherRhinebothriumpeciesknown o exhibitthistypeof interruption,. baeri,R. biorchidum, . chilensis,R. ditesticulum, . leibeli, R. pearsoni, and R. scobinae, allseem to entirelyack both oculi and septa n thisregion;none-theless, here s some variation nthe curvature nd distinctnessofthe boundaries f thisregion nthese pecies.Rhinebothriummegacanthophallus nd R. abaiensis lack loculi, but bear re-duced transverseeptain thisregion.These septawereclearly



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visible only in longitudinal ection. n addition, he filitricheson the distalbothridial urface of thisregion n R. megacan-thophallus nd R. abaiensis aremarkedlyongerthanthose onthe restof the distal surface.Additional data fromthe othertaxa with nterruptedoculi are requiredbeforethehomologyof these ocular nterruptionsan be assessed.The cestodes of elasmobranchs n Malaysian Borneo werevirtually nknown efore he nitiation f thesurveyof whichthis tudy s a part.Preliminaryata from xaminations fces-todes from 3 marine nd 1 euryhaline atoid species also re-sulting rom hisongoing surveyofMalaysian Borneo suggestthat he 3 Rhinebothriumpecies described hereare unique toH. chaophraya. In addition,preliminary ata fromexamina-tions of cestodes from 4 specimensof H. chaophraya fromQueensland,Australia,ndicate hatRhinebothriumpecies alsoparasitize his host n Australia,butthat hespecies describedheremaybe distinct rom hose n Australia.All 6 of the individuals of H. chaophraya examined fromMalaysia examinedwereparasitized yRhinebothriumpecies.All 3 oftheRhinebothriumpecies describedhereco-occurredin 1 of thehost individuals;R. kinabatanganensis arasitized2, R. megacanthophallus arasitized3, and R. abaiensis para-sitizedall 6 of thehost individualsexamined.Rhinebothriumkinabatanganensiswas conspicuously ess abundant thantheother2 Rhinebothriumpecies in the 2 host individuals t in-habited.IfHimantura haophraya s an obligate nhabitant f fresh-water, hen heRhinebothriumpecies describedhere are likelyfreshwateretraphyllideans.his is a rarequalityamongtetra-phyllideans ut is notunique. For example,members f 5 te-traphyllidean enera, including 1 Rhinebothriumpecies, R.paratrygoni, re knownfromrays in the freshwatertingrayfamily otamotrygonidae.hese raysareknown to be obligateinhabitants ffreshwaterystemsn SouthAmerica e.g., Regoand Dias, 1976; Brooks and Amato, 1992; Marques, 2000).There s no indication hatH. chaophraya s closely relatedtothepotamotrygonids,s they recurrentlylassified n separatefamilies.Potential imilarities etweenR. paratrygoni nd theRhinebothriumpecies describedherearedifficulto assess be-cause of therather imiteddescriptive ata currentlyvailableforthat pecies (Rego and Dias, 1976). Given thediversity fpotamotrygonids,nd the strict ostspecificityxhibited yte-traphyllideans,t is not surprisinghat greatnumber f Rhi-nebothriumpeciesremain o be describedfrom otamotrygon-ids (F. Reyda,pers.comm.). The onlyotherbatoids thathavebeen reliablydocumented o occur in freshwaterre 3 poten-tiallyobligatefreshwaterpecies, Dasyatis garouensis,D. lao-sensis,and Urogymnuskpam, nd severalfacultativelyresh-water pecies,such as Pastinachussephen,H. krempfi,nd H.signifer Compagno and Roberts, 1982; Froese and Pauly,2004). A hypothesis f the evolutionary vents thatbroughtmarineRhinebothriumpecies intofreshwaterswaits the dis-covery,description, nd phylogenetic nalysis of the Rhine-bothrium aunas of theseraysand their elatives.

ACKNOWLEDGMENTSI thankZainal Abidin Ja'afar, tin,Aznih Etin,Maznih Etin,andSalik fromKampungAbai fortheirhospitality nd assistance,alongwithJanineCaira, KirstenJensen, nd Gavin Naylor, n collecting herays and theirparasitesfor this work. Permission to collect elasmo-

branchs nd theirmetazoanparasiteswas granted o JanineCaira andcolleagues by theEconomic PlanningUnit EPU), Kuala Lumpur,Ma-laysia (permitUPE:40/200/19SJ.924) nd theChiefMinister'sDepart-ment,Kota Kinabalu,Malaysia (permit KM100-24/13/l/223[59]).an-ineCairaprovided ritical omments n a previousversion f thiswork.Hui Xu and Man Wugraciously ranslated heoriginalChinesedescrip-tionof R. hui in Tseng (1933) intoEnglish. Fundingfor thisprojectcame from n NSF BS&I grant DEB 0103640 to JanineCaira, PI;KirstenJensen,PeterLast, Gavin Naylor, nd JohnStevens,Co-PIs)and an NSF PEET grant DEB 0118882 to JanineCaira and TimothyRuhnke).

LITERATURE CITEDBaer, J. G. 1948. Contributions l'&ude des cestodesde selaciens. -IV. Bulletin de la SocietyNeuchateloisedes Sciences Naturelles71: 63-122.Ball, D., L. Neifar, and L. Euzet. 2003. Descriptionof Scalithriumn. gen. (Cestoda, Tetraphyllidea), ithScalithriumminimumVanBeneden, 1850) n. comb., a parasiteof Dasyatis pastinaca (Elas-mobranchii, asyatidae), as type species. Parasite 10: 31-37. [InFrench.]Brooks, D. R., and J. F. R. Amato. 1992. Cestode parasites n Pota-motrygonmotor (Natterer) Chondrichthyes:otamotrygonidae)from outhwestern razil, includingRhinebothroidesmclennanaen. sp. (Tetraphyllidea:hyllobothriidae),nda revisedhost-parasitechecklist orhelminthsnhabiting eotropical reshwatertingrays.Journal f Parasitology 8: 393-398.Butler, S. A. 1987. Taxonomyof some tetraphyllideanestodesfromelasmobranch ishes.AustralianJournal fZoology 35: 343-371.Caira, J.N., C. J.Healy, and J. Swanson. 1996. A new species ofPhoreiobothriumCestoidea: Tetraphyllidea) rom heGreat ham-merhead hark phyrnamokarran nd its mplications or heevo-lution f theonchobothriidcolex.Journal fParasitology 2: 458-462., K. Jensen, nd C. J. Healy. 1999. On thephylogenetic ela-tionshipsamong tetraphyllidean,ecanicephalideanand diphylli-dean tapeworm enera. Systematic arasitology 2: 77-151., , and . 2001. Interrelationshipsmong tetra-phyllidean nd lecanicephalidean estodes. n Interrelationshipsfthe Platyhelminthes,. T. J. Littlewoodand R. A. Bray (eds.).Taylorand Francis,London, U.K., p. 135-158.Compagno,L. J. V, and T. R. Roberts. 1982. Freshwater tingrays(Dasyatidae) of SoutheastAsia and New Guinea,withdescriptionof a new species ofHimantura nd reports f an unidentifiedpe-cies. Environmental iologyof Fishes7: 321-339.Euzet, L. 1994. OrderTetraphyllidea ams, 1863. In Keys to the ces-todeparasites fvertebrates,. F.Khalil,A. Jones, nd R. A. Bray(eds.). CAB International,Wallingford, .K., p. 149-194.FALffix,., G. Tyler, and L. Euzet. 2000. A new species of Ditrach-ybothridiumCestoda: Diphyllidea) from Galeus sp. (Selachii,Scyiorhynidae) rom he southPacificOcean, with a revisionofthediagnosisof theorder, amily,nd genusand notes on descrip-tiveterminologyfmicrotriches.ournal fParasitology 6: 1078-1084.Froese, R., and D. Pauly. 2004. FishBase. WorldWideWebelectronicpublication,www.fishbase.org,ersion 6/2004).Kottelat, M. 2001. Fishes of Laos. WHT Publications Pte.) Ltd.,SriLanka, 198 p.Last, P. R., and J. D. Stevens. 1994. Sharks and rays of Australia.CSIRO, Canberra,Australia, 13 p.Marques, F. P. L. 2000. Evolution of neotropical reshwatertingraysand theirparasites:Taking ntoaccountspace and time.Doctoraldissertation. niversityfToronto, oronto,Canada, 325 p.Ma yes, M. A., D. R. Brooks, and T. B. Thorson. 1981. Two newtetraphyllideanestodes fromPotamotrygon ircularis Garman(Chondrichthyes: otamotrygonidae)n the Itacuai River,Brazil.Proceedingsof the Helminthological ociety of Washington 8:38-42.McKenzie, V. J., nd J.N. Caira. 1998. Threenewgenera nd speciesof tapeworms rom he ongnosesawshark, ristiophorus irratus,with omments n theirmodesofattachmento the piral ntestine.Journal f Parasitology 4: 409-421.



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Monkolprasit, S., and T. R. Roberts. 1990. Himanturachaophraya,a newgiantfreshwatertingrayrom hailand.JapaneseJournal fIchthyology7: 203-208.Rego, A. A., and A. P. L. Dias. 1976. Estudos de cest6ides de peixesdo Brasil. 3.aNota: Cest6ides de raias fluviaisParatrygonidae. e-vista Brasileirade Biologia 36: 941-956.Ruhnke,T. R. 1994a. Resurrection f AnthocephalwnLinton, 1890(Cestoda: Tetraphyllidea)nd taxonomic nformationn fivepro-posed members. ystematic arasitology 9: 159-176.. 1994b. Paraorygmatobothriwnarberi n. g., n. sp. (Cestoda:Tetraphyllidea),with amended descriptions f two species trans-ferred o thegenus. Systematic arasitologv 8: 65-79.. 1996. Systematic esolution f Crossobothriwn inton, 1889,

and taxonomic nformationn four pecies allocatedto thatgenus.Journal f Parasitology 2: 793-800.Shark Specialist Group. 2000. Himantura haophraya. n IUCN 2004.2004 IUCN Red List of ThreatenedSpecies, www.redlist.org.Downloaded on 1 December2004.Shirai,S. 1996. PhylogeneticnterrelationshipsfneoselachiansChon-drichthyes: uselachii). In Interrelationshipsf fishes,M. L. J.Stiassny, . R. Parenti, nd G. D. Johnsoneds.). AcademicPress,San Diego, California, . 9-34.Subramaniam,M. K. 1940. On a newspeciesofEcheneibothriumromRhinobatusgranulatusCuv. Records of the Indian Museum 42:457-464.Tseng, S. 1933. A studyof the cestode parasitesof fishes.Journal fScience,NationalUniversityfShantung : 327-350. [InChinese.]

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