THE JOURNAL OF PARASITOLOGYVol. 60, No. 1, February 1974, p. 29-34RECORDS OF CESTODES FROM CHILEAN SHARKSJuan CarvajalLaboratorio de Zoologia, Instituto de Ciencias Biol6gicas, Universidad Cat6lica de Chile,Casilla 1 14-D, Santiago, ChileABSTRACT: Thirteen species of cestodes, including a new species of Prochristianella, are recorded from6 of 11 species of Chilean sharks. Most of the cestodes were found in the same or closely related hostsas those previously reported from other localities. Several new host records are presented.Knowledge of cestodes from Chilean sharksis limited to only two references, Yafiez (1950)and Carvajal (1971), both concerning trypanorhynchans.In this report 13 species from Chileansharks are recorded. Among these, Prochristianellamusteli is new, whereas the remainingspecies have been reported in the literaturefrom the same or closely related hosts. Thesharks examined were collected from 1967-72,either by trawl nets of commercial fishingboats, operating from Papudo to Talcahuano,Chile, or from fishermen at San Antonio,Coquimbo, Antofagasta, and Archipielago delos Chonos.MATERIALS AND METHODSWhenever possible, the specimens were examinedalive in seawater and relaxed in 10% magnesiumchloride solution; they were then fixedand stained by methods already described (Carvajaland Goldstein, 1969, 1971). Drawings weremade with the aid of a Leitz drawing tube. Thetetraphyllideans from Mustelus mento were examinedby Dr. Louis Euzet at the University ofMontpellier, who corroborated my identifications.Measurements of the new species are in microns,unless otherwise indicated.RESULTSThe following host-parasite list includestetraphyllideans and trypanorhynchan cestodesobtained in the survey of species from Chileanelasmobranchs and does not include wormsfrom other sources.1. Hexanchus griseus (Bonnaterre, 1780):Phyllobothrium sinuosicepsPhyllobothrium dohrniiGrillotia heptanchii2. Prionace glauca (Linnaeus, 1758):Crossobothrium angustumPlatybothrium auriculatumHepatoxylon trichiuriReceived for publication 17 November 1972.3. Alopias vulpinus (Bonnaterre, 1788)Crossobothrium angustum4. Triakis maculata Kner and Steindachner, 1867Lacistorhynchus tenuis5. lMustelus mento Cope, 1877Orygmatobothrium musteliPhyllobothrium lactucaCrossobothrium triacisCalliobothrium verticillatumProchristianella musteli sp. n.6. Centrocyllium granulosus Gunther, 1880Gilquinia squali7. Squalus fernandinus Molina, 1782 negative8. Aculeola nigra De Buen, 1959 negative9. Galeorhinus zyopterus Jordan andGilbert, 188210. Halaelurus chilensis (Guichenot,1847)11. Squatina armata (Philippi, 1887)negativenegativenegativeOrder Tetraphyllidea Van Beneden, 1849Family Phyllobothriidae Braun, 1900Genus Phyllobothrium Van Beneden, 1849Phyllobothrium lactuca Van Beneden, 1850Three of 35 Mustelus mento examined werefound to harbor this parasite in the spiralvalve; one shark was from Talcahuano andthe others were from Coquimbo. This is thefirst report of this cestode from the southeasternPacific, and M. mento is a new host.It seems that P. lactuca is cosmopolitan inspecies of Mustelus. For detailed records, seeWilliams (1968); for description, see Euzet(1959) and Williams (1968).Phyllobothrium dohrnii (Oerley, 1885)Host: Hexanchus griseus: Algarrobo, San Antonio,Archipielago de los Chonos. Six fishesexamined: 4'positive, 2 negative.This cestode may be cosmopolitan, as itsusual host, Hexanchus griseus, occurs on bothsides of the Atlantic, the Mediterranean, the29
30 THE JOURNAL OF PARASITOLOGY, VOL. 60, NO. 1,FEBRUARY 1974Pacific coast of North America, Chile, Japan,Australia, southern Indian Ocean, and SouthAfrica (Bigelow and Schroeder, 1948). Thecenter of the abundance of this shark seemsto be in the Mediterranean and North Sea,where most of the records of this parasitehave been made (see Williams, 1968).Phyllobothrium sinuosiceps Williams, 1959Host: Hexanchus griseus: Archipielago de losChonos. One H. griseus examined.Depth: 146 meters.This is the first report of P. sinuosiceps froma locality other than the North Sea. It maybe widespread and its absence in other latitudesreflects the sparse information on recordsof H. griseus, the type host (see Williams,1968).Genus Crossobothrium Linton, 1901Crossobothrium triacis (Yamaguti, 1952)This species was found in two Mustelusmento from Antofagasta and Mejillones. Ithas been previously reported in the Pacificby Yamaguti (1952) from another memberof the Family Carcharhinidae, Triakis scyllium,and from the Mediterranean (Euzet, 1959)in Mustelus canis and M. mustelus.Crossobothrium angustum (Linton, 1889)Hosts: Alopias vulpinus: Coquimbo. Prionaceglauca: Antofagasta.This parasite has been reported from thePacific coast of Japan in the same two hostsas Phyllobothrium prionacis Yamaguti, 1934,and Phyllobothrium filiforme Yamaguti, 1952.Both names are junior synonyms of C. angustum,according to Euzet (1959). Euzet (1952,1959) reported this cestode in the Mediterraneanand the eastern Atlantic in Prionaceglauca (Syn.: Galeus glaucus or Carcharhinusglaucus), and in Alopias vulpinus. The presentreport extends the known distribution of C.angustum to the southeastern Pacific Ocean.Genus Orygmatobothrium Diesing, 1863Orygmatobothrium musteli (Van Beneden, 1850)This cestode was present in 35 of 36 Mustelusmento from Talcahuano to Mejillones.It has been previously reported from theeastern North Atlantic, Mediterranean, Pacificcoasts of Japan and New Zealand, always insharks of the genus Mustelus.Family Onchobothriidae Braun, 1900Genus Calliobothrium Van Beneden, 1850Calliobothrium verticillatum (C. A. Rud, 1819)Twenty-one of 36 Mustelus mento fromTalcahuano to Antofagasta harbored this parasite.According to Euzet (1952), C. verticillatumis cosmopolitan. Its hosts are mainlysharks of the genus Mustelus.Genus Platybothrium Linton, 1890Platybothrium auriculatum Yamaguti, 1952Host: Prionace glauca: Antofagasta. One P.glauca examined.This cestode has been reported from thePacific coast of Japan (Yamaguti, 1952), theeastern North Atlantic and the Mediterranean(Euzet, 1952, 1959). The only host reportedis Prionace glauca, a cosmopolitan shark(Bigelow and Schroeder, 1948).Order Trypanorhyncha Diesing, 1863Family Hepatoxylidae Dollfus, 1940Genus Hepatoxylon Bosc, 1811Hepatoxylon trichiuri (Holten, 1802). PlerocercusHost: Prionace glauca: Antofagasta. One fishexamined.Habitat: Body cavity, on serous membrane ofstomach and liver.This parasite was reported under the nameDibothriorhynchus grosum in the body cavityand on the liver of the same host (Yafiez,1950). The hosts and the geographical distributionof the postlarval Hepatoxylon trichiurihave been discussed by Dollfus (1942).Family Eutetrarhynchidae Guiart, 1927,emended Dollfus, 1942Genus Prochristianella Dollfus, 1946Prochristianella musteli sp n.(Figs. 1-5)Description (based on 20 specimens)Small, acraspedote, euapolytic worm. Length,6 mm; maximal width, 400. Bothridia, 2, quadrangular,300 wide, 200 to 250 long. Pars bothridialis,200 to 250; pars vaginalis, 600 to 800;pars bulbosa, 700 to 850; evaginated proboscis,350 to 650 long. In parasites observed alive inseawater, a bright red spot was clearly visible nearthe posterior region of the pars vaginalis. In 6%formalin the spot rapidly disappeared. Retractormuscle of bulbus inserted at posterior part ofbulbus.
CARVAJAL-RECORDS OF CESTODES AND A NEW SPECIES FROM CHILEAN SHARKS 31EEro -0N-EH -f- ---IiH-0-0-213 40 20 40 pI 1 I I IFIGURES 1-5. Prochristianella musteli sp. n., from Mustelus mento off Chile. 1. Scolex and partof the strobila. 2. Mature proglottid. 3. Basal portion of the proboscide showing the inner face. 4.Basal portion of the proboscide showing the outer face. 5. Metabasal armature of the proboscide.
32 THE JOURNAL OF PARASITOLOGY, VOL. 60, NO. 1, FEBRUARY 1974Proboscis armature heteroacanthous, with hooksof different kinds (Figs. 3-5). Basal region ofproboscis (Figs. 3, 4) contains, at beginning ofbase, approximately 4 rows of hooks with broadbases and extremely recurved points; measurements:greatest dimension, 6; length of base ofimplantation, 4.5; from tip to end of posteriorheel, 3. Beyond these hooks a region 30 in lengthwith slender hooks, about 7 in length. Remainingbasal region contains 5 transverse rows of hooks,5.5 in length, without well-developed heels andwith recurved points. Hooks of both external(Fig. 4) and internal (Fig. 3) faces of basalarmature show similar arrangement, size, andshape. Diameter of proboscis in this region, 33.Metabasal armature (Fig. 5) characterized byobliquely transverse rows of homeomorphous hooksarranged in half turns, those of one face alternatingwith those of the other. Each half turncomprises 9 to 13 hooks having the same shapeand size. Hooks, 7 in length; base of implantation,6. Diameter of proboscis in this region, 27.Number of segments, 10. Anterior proglottidsbroader than long, 120 by 60. Terminal segments,longer than wide, 700 to 1,100 by 200 to 400.Genital atrium irregularly alternate, opens at thelateral margin, slightly posterior to middle ofproglottid. Testes, spherical, in medulary field in2 longitudinal rows from anterior margin of proglottidto level just anterior to ovary; number, 31;diameter, about 60. Ovary medium-sized in posteriorpart of proglottid. No eggs observed.Host: Mustelus mento Cope, 1877. Four sharksexamined, positive.Locality: San Antonio and Antofagasta.Holotype: Museo Nacional de Historia Natural,Chile, No. 20,008.Paratypes: USNM Helm. Coll. No. 72793.RemarksProchristianella musteli sp. n. differs fromP. papillifer (Poyarkoff, 1909), P. aetobatidisRobinson, 1959, and P. penaei Kruse, 1959,mainly in different arrangements and morphologyof hooks; its metabasal armature ishomeomorphous whereas it is heteromorphousin the three other species.Prochristianella tenuispinis (Linton, 1890)has a proboscis diameter of 16 to 18 in thebasal region and 10 to 13 in the metabasalregion or half those of P. musteli in the sameregions. The metabasal hooks of P. mustelihave a well-developed anterior and posteriorheel whereas these hooks in P. tenuispinis arespiniform and without heels.P. musteli is the only species of Prochristianellafrom a shark instead of a ray. This isthe first report of the genus in the easternPacific.Family Lacistorhynchidae Guiart, 1927,emended Dollfus, 1935Genus Lacistorhynchus Pintner, 1913Lacistorhynchus tenuis (Van Beneden, 1858)Host: Triakis maculata: Antofagasta. Oneshark examined.This parasite has been previously reportedin the northeastern Pacific by Young (1954)and Riser (1956) in the spiral valve of Triakissemifasciata, and also occurs in Mustelus canisin the western Atlantic.This is the first report of L. tenuis fromthe southeastern Pacific, and Triakis maculatais a new host.Family GrillotidaeGenus Grillotia Guiart, 1927Grillotia heptanchii (Vaullegeard, 1899)This parasite was reported by Carvajal(1971) in Hexanchus griseus and has beenrecently found in material from San Antonio,Chile, in 2 specimens of H. griseus examined.Family Gilquinidae Dollfus, 1942Genus Gilquinia Guiart, 1927Gilquinia squali (Fabricius, 1794)Host: Centrocyllium granulosus: Coquimbo.One shark examined.A single immature worm was recorded.This species has been found mainly in sharksof the Family Squalidae, and has been reportedin the northeastern Pacific in Squalussuckleyi. I agree with Dollfus (1942) thatthis species could be found in other regions,not showing geographical discontinuity.DISCUSSIONAll 11 cestodes are reported for the firsttime in the southeastern Pacific and, generally,in South American waters (Fig. 6).The cestode faunas inhabiting Hexanchusgriseus, Prionace glauca, and Alopias vulpinusare the same that inhabit these sharks in otherparts of the world. For zoogeographical analysisof these hosts, see Bigelow and Schroeder(1948) and Kato et al. (1967). The sparserecords of their parasites reflect the scantparasitological work that has been carried outin areas other than the North Atlantic, Mediterranean,and western Pacific.The tetraphyllidean cestodes of this groupof sharks-Phyllobothrium sinuosiceps, Phyllobothriumdohrnii, Crossobothrium angustum,
CARVAJAL-RECORDS OF CESTODES AND A NEW SPECIES FROM CHILEAN SHARKS 33(1959) considered these parasites as beingrestricted to the genus Mustelus.Gilquinia squali, found in Centrocylliumgranulosum, has been reported from sharks ofthe family Squalidae around the world. Lacistorhynchustenuis was found in the northeasternPacific in Triakis semifasciata (Carcharhinidae),a host closely related to T.maculata.Four Squatina armata, four Squalus fernandinus,10 Aculeola nigra, one Galeorhinuszyopterus, and eight Halaelurus chilensis werealso examined, but all were negative for cestodeparasites.FIGURE 6. Places from which the sharks wereobtained.and Platybothrium auriculatum-are consideredin the present report as Euzet's "especesubiquistes" (Euzet, 1959) with regard to thegeographical distribution.Concerning host specificity, Crossobothriumangustum was the only tetraphyllidean speciesfound in two sharks belonging to differentfamilies. According to Euzet (1959) Phyllobothriumprionacis Yamaguti, 1934, and Phyllobothriumfiliforme Yamaguti, 1952, fromPrionace glauca (Carcharhinidae), and Alopiasvulpinus (Alopiidae), respectively, are synonymsof Crossobothrium angustum.The remaining tetraphyllidean species ofthis group of hosts show close host specificity;this observation is supported by Williams(1968) concerning Phyllobothrium dohrniiand P. sinuosiceps. The majority of recordsfor Platybothrium auriculatum are from Prionaceglauca.The tetraphyllideans from Mustelus mentoare widespread species which have been reportedfrom the literature throughout theworld. Concerning host specificity, EuzetACKNOWLEDGMENTSThis work was supported by Grants 21/70and 13/72 from the Fondo de Investigaci6n,Universidad Cat6lica de Chile, and was partlydone at the Laboratorio de Biologia MarinaS.A.G. in San Antonio and the Laboratorio deOceanologia, Universidad de Chile, Antofagasta,for which I am most grateful.I am deeply indebted to Dr. Louis Euzet ofthe University of Montpellier, who reviewedand critically commented the manuscript; andto Empresa Pesquera Harling of San Antoniowhich provided me with sailing facilities.LITERATURE CITEDBIGELOW, H. B., AND W. C. SCHROEDER. 1948.Fishes of the Western North Atlantic (chapt.3), Sharks, No. 1, part 1. A. Parr, ed. Mem.Sears Found. Mar. Res., New Haven, p. 59-576.CARVAJAL, G. J. 1971. Grillotia dollfusi sp. n.(Cestoda: Trypanorhyncha) from the skateRaja chilensis, from Chile, and a note on G.heptanchi. J. Parasit. 57: 1269-1271., AND R. J. GOLDSTEIN. 1969. Acanthobothriumpsammobati sp. n. (Cestoda: Tetraphyllidea:Onchobothriidae) from the skatePsammobatiscobina (Chondrichthyes: Rajidae)from Chile. Zool. Anz. 182: 432-435., AND . 1971. Acanthobothriumannapinkiensis sp. n. (Cestoda: Tetraphyllidea:Onchobothriidae) from the skate Raja chilensis(Chondrichthyes: Rajidae) from Chile.Zool. Anz. 186: 158-162.DOLLFUS, R. P. H. 1942. Rtudes critiques surles Tetrarhynches du Museum de Paris. Arch.Museum Natl. Hist. Nat. (Paris) 19: 1-466.1946. Notes diverses sur des Tetrarhynches.Mem. Museum Natl. Hist. Nat. (Paris)22: 179-220.EUZET, L. 1952. Cestodes tetraphyllides de lacote atlantique du Maroc et de Mauritanie.
34 THE JOURNAL OF PARASITOLOGY, VOL. 60, NO. 1, FEBRUARY 1974Compt. Rend. Seanc. Soc. Natl. Maroc. 5:91-96.1959. Recherches sur les CestodesTetraphyllides des Selaciens des C6tes deFrance. Thesis Fac. Sci. Univ. Montpellier,263 p.KATO, S., S. SPRINGER, AND M. H. WAGNER. 1967.Field Guide to Eastern Pacific and HawaiianSharks. U. S. Fish and Wildlife Serv. Circular271, 47 p.RISER, N. W. 1956. Early larval stages of twocestodes from elasmobranch fishes. Proc.Helm. Soc. Wash. 23: 120-124.ROBINSON, E. S. 1959. Some new cestodes fromNew Zealand marine fishes. Tr. Roy. Soc.New Zealand 86: 381-392.WILLIAMS, H. H. 1968. The taxonomy, ecologyand host-specificity of some Phyllobothriidae(Cestoda: Tetraphyllidea), a critical revisionof Phyllobothrium Beneden, 1849 and commentson some allied genera. Phil. Tr. Roy.Soc. London Ser. B 253: 231-307.YAMAGUTI, S. 1952. Studies on the helminthfauna of Japan. Part 49. Cestodes of fishes,II. Acta Medica Okayama 8: 1-76.YANSEZ, A. P. 1950. Observaci6n de un Dibothriorhynchus,parasito del azulejo. Rev. Biol.Mar. 2 (2/3): 165-166.YOUNG, R. T. 1954. Cestodes of sharks and raysin southern California. Proc. Helm. Soc.Wash. 21: 106-112.Suggestions to Prospective AuthorsIn addition to general instructions inside thefront cover of the Journal, the following hintshave been printed from time to time:On bibliographic style: 45: 621, 46: 308.On the Research Note: 47: 396.Hints on writing: 48: 176, 51: 553, 52: 232,406, 54: 535, 55: 354, 688, 58: 722, 59: 276.Preparation of drawings and plates: 52: 1024,53: 660, 54: 50, 358, 56: 264, 58: 554.Authors are now charged at the rate of $35.00per page for all pages over 6. Excessive correctionsin proof will be charged to the author.All copy must be double spaced, includingbibliographies, legends to plates, etc., and themaster copy must be a ribbon copy on bond paper.Legends must be typed on a separate sheet andnot tacked on to the illustrations. All illustrationsmust be numbered on the back for identification.Composite halftone plates should be mounted withat least an inch margin to protect edges of theprints, and for editorial marking.Plates must be designed for either single column(16 picas), or double column (33 picas) width, asreproduced. Odd sizes are not permitted. Platesmust be rectangular. Steps in margins are notpermitted. Individual prints must be accuratelysquared and butted, no white showing. Theengraver will cut a fine hairline of separationbetween the figures. It is advantageous, whereconvenient, to have the plate as printed a littleshorter than page length, so that the legend canbe fitted below.The author should make it clear whether magnificationsof plates, as given, are for the plateas it will appear in the Journal, or must be recalculatedfor the intended reduction. Where plateshave been designed for special treatment, in conferencewith the editor, such as bleeding to edgeof page, this must be clearly marked by the authoron margin or back of plate. Otherwise sucharrangements are likely to be forgotten by thetime the manuscript goes to the printer.Excessive bibliographies are to be avoided,particularly references to procedures which haveby now become standard (such as EM techniques).Twenty five entries should be a maximum. Recentlysome research notes have been submittedwith as many as five authors! This would beexcessive for a full blown article, and on a researchnote approaches the ridiculous.When in doubt, authors should study recentnumbers of the Journal for handling of similarmaterial. We cannot permit wide departures fromestablished Journal style since this greatly complicatesthe work of the editor and printer. Wheremost measurements are less than 1 mm, valuesshould be given "in microns unless otherwisestated."The editor's office cannot answer trivial inquiriesunless a self addressed stamped envelopeor postcard is included.THE EDITOR