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6-1973

Cathetocephalus thatcheri gen. et sp. n. (Tetraphyllidea: Cathetocephalidae) fam. n. from the Bull Shark

Murray D. Dailey Marine Mammal Center, [email protected]

Robin M. Overstreet Gulf Coast Research Laboratory, [email protected]

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Dailey, Murray D. and Overstreet, Robin M., "Cathetocephalus thatcheri gen. et sp. n. (Tetraphyllidea: Cathetocephalidae) fam. n. from the Bull Shark" (1973). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 474. https://digitalcommons.unl.edu/parasitologyfacpubs/474

This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. THE JOURNAL OF PARASITOLOGY Vol. 59, No.3, June 1973, p. 469-473

CATHETOCEPHALUS THATCHER' GEN. ET SP. N. (TETRAPHYLLIDEA: CATHETOCEPHALIDAE FAM. N.) FROM THE BULL SHARK: A SPECIES DEMONSTRATING MULTISTROBILIZATION

Murray D. Dailey* and Robin M. Overstreett

ABSTRACT: Cathetocephalus thatcheri gen. et sp. n. is described from the spiral valve of the bull shark, Carcharhinus leucas (Valenciennes), taken in the Gulf of Mexico and the Atlantic coast of Florida. A new family is erected for the new genus. The species most closely resembles Pillersium owenium Southwell, 1927, in that both possess a scolex which is perpendicular to the long axis of the strobila. It differs, however, in having a single neck and holdfast organ rather than a bifurcate neck with 2 bothridia. Also, the surfaces of the scolex differ from those of P. owenium by possessing fleshy pa­ pilliform structures on the leading and trailing edges rather than leaflike folds. Specimens with sev­ eral strobilae are figured and discussed.

A heavy infection of cestodes was found in with a central longitudinal fold extending entire the spiral valve of two specimens of the bull length. Neck entire, not branched into 2 bothridia. shark, (Valenciennes) , Strobila dorsoventrally flattened, slightly craspe­ Carcharhinus leucas dote, apolytic, with distinct segmentation. Longi­ that had been collected in Galveston Bay, tudinal muscles well developed, forming boundary Texas. The sharks had been flown to Sea between cortex and medulla. Testes numerous, World, San Diego, California, and died several medullary. Cirrus sac present. Genital pores days later. Additional specimens were also lateral, alternating irregularly. Ovary large, bi­ lobed, posterior. Vj'telline follicles cortical, en­ recovered from the same species of host at Mi­ circling medulla. Excretory stems in medulla. ami, Florida. The presence in those worms Parasites of elasmobranch fishes. Type and only of a unique multistrobilate condition in some genus: specimens prompted this study. The species Cathetocephalus gen. n. does not have the typical tetraphyllidean scolex, but is considered here as representing Diagnosis: With characters of the family. Strobilae occasionally multiple. Type and only a new genus in a new family in the order species: Tetraphyllidea. Worms were fixed in AFA, Bouin's fluid, or Cathetocephalus thatcheri sp. n. 10% formalin. Whole mounts were stained (Figs. 1-9) with cellestine blue B or Semichon's carmine. Description (based on 15 specimens): Total Sections of other specimens were cut at 6, 8, length 101 (70 to 105). Strobila consisting of and 10 p. and stained with hematoxylin-eosin 269 (228 to 325) segments; multistrobilate forms or Mallory's trichrome stain. All material was rare, occasionally with up to 14 strobilae per dehydrated in ethanol, cleared in xylene, and individual. Proglottids approximately 4 times longer than bmad when mature in gravid worms, mounted in Piccolyte. Drawings were made 3.8 (2.9 to 4.1) long by 1.03 (0.86 to 1.21) wide; with the aid of a drawing tube and stereo­ 5.5 by 1.0 when gravid; wider than long until scopic microscope. Average measurements region of 200th segment. Scolex consisting of are given, with ranges in parentheses. They single continuous holdfast organ, perpendicular to long axis of strobila, size variable depending on are in millimeters unless otherwise indicated. maturity of worm; 6.1 (4.0 to 10.0) long with right side 2.28 (1.50 to 3.40) and left side 2.64 Cathetocephalitlae fam. n. (1.44 to 4.72), 0.72 (0.54 to 0.96) wide at neck Diagnosis: Moderately sized. Scolex a single attachment, narrowing to 0.27 (0.16 to 0.43) at transverse organ; anterior surface highly rugose, tip in mature unistrobilate forms; up to 23.0 long with fleshy papilliform projections on leading and in multistrobilate forms. Longitudinal fold on trailing edges; posterior surface of organ smooth posterior surface of organ constitutes origin of strobilae in both single and multistrobilate forms. Received for publication 11 July 1972. Neck 0.98 (0.55 to 1.50) wide with strobilization * Department of Biology, California State Uni­ beginning 1.44 to 2.70 posteriorly in mature uni­ versity, Long Beach, California 90804. strobilate forms, usually originating near center of t Gulf Coast Research Laboratory, Ocean Springs, scolex. Mississippi 39564. Testes spherical to subspherical, 60 I-' (53 to 67)

469 470 THE JOURNAL OF PARASITOLOGY, VOL. 59, NO.3, JUNE 1973

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FIGURES 1-3. Cathetocephalus thatcheri. 1. Transverse scolex, ventral view. 2. Mature proglottid. 3. Diagrammatic illustration of multistrobilate fOIID, dorsal view (approximately X 7). C, cirrus; M, Mehlis' gland; 0, ovary; U, uterus; T, testis; V, vitelline follicle; VA, vagina; VD, vas deferens.

long by 48 !J- wide, not extending to anterior or Site: Spiral valve. posterior margins. Cirrus sac not reaching middle Localities: Galveston Bay, Texas, and off Miami, of segment, 570 !J- (528 to 586) long by 288 !J­ Florida. (250 to 336) wide. Cirrus spinose. Internal seminal Holotype: USNM Helm. Coli. No. 72302; Para­ vesicle lacking. Vas deferens large, extending to type No. 72303. anterior tip of uterus, forming a functional external seminal vesicle. Vagina anterior to cirrus, empty­ Remarks ing into a common genital atrium. Genital aper­ ture lateral, irregularly alternating, slightly pos­ The name Cathetocephalus is derived from terior to midsegment. Ovary 1.06 (0.99 to 1.13) the Greek, "kathetos" and "kephalos" meaning long by 0.42 wide (0.34 to 0.50). Vitelline follicles perpendicular-headed, and serves as a noun to small, not extending entire length of proglottid. be treated as masculine in gender. The species Mehlis' gland 0.19 long by 0.15 wide. Eggs 35 !J­ is named for Dr. Vernon E. Thatcher, Departa­ long by 29!J- wide (22 to 43 by 27 to 32). Type host: Carcharhinus let/cas (Valenciennes), mento de Biologia, Universidad del Valle, Cali, bull shark. Colombia, who first recorded the species. DAILEY AND OVERSTREET-NEW MULTISTROBILATE TAPEWORM FROM BUll SHARK 471

FIGURES 4-9. Cathetocephalus thatcheri. 4. Multistrobilate form, ventral view (X 7). 5. "Swirl­ ing" pattern of strobila formation site in scolex of multistrobilate form (X 77). 6. Isolation of strobila formation site in scolex of multistrobilate form (X 214). 7. Isolation site of strobila showing cellular differentiation in scolex of muJ.tistrobilate form (X 125). 8. Anterior region of strobila showing well­ defined cortical and meduUary regions (X 255). 9. "Budding" process seen in mature segment of unistrobilate form (X 22).

DISCUSSION described in this report. Southwell (1927) This parasite was first reported from erected the genus Pillersium in the nondescript Carcharhinus limbatus (Valenciennes) in the Heterophyllidea group to accommodate a worm coastal waters of Mississippi and Louisiana by with "several heads but no strobilae from the Thatcher (1961). At that time, he provisionally spiral valve of Urogymnus asperimus. Pear considered it Pillersium owenium Southwell, Banks, Ceylon." Pillersium owenium has a 1927, because of the T-shaped scolex. branched neck with each stalk bearing a Thatcher's original material was reexamined bothridium. No segments were described. and found to be identical to the specimens Yamaguti (1959) considered Pillersium as in- 472 THE JOURNAL OF PARASITOLOGY, VOL. 59, NO.3, JUNE 1973 certae sedis. Cathetocephalus thatcheri appears plified by specimens of Diphyllobothrium most closely related to P. owenium because lanceolatum (Krabbe, 1865) illustrated by of the presence of a scolex without suckers or Delyamure (1955) . As for larval cestodes, hooks and perpendicular to the long axis of Mueller (1966) discussed branching in spar­ the strobila. It, however, differs from that gana and Eckert et al. (1969) discussed multi­ species by having a single neck which is not plication of Mesocestoides corti Hoeppli, 1925. bifurcate and a single organ rather than two To our knowledge, the present report repre­ separate bothridia. The surfaces of the hold­ sents the first of more than two mature strobilae fast also differ, since in C. thatcheri they ex­ arising from a single scolex. The condition hibit fleshy papilliform structures rather than was noted in less than 1% of the observed pop­ leaflike folds on the leading and trailing edges. ulations in four separate collections from Texas Watson (1966), in an unpublished dissertation and the east and west coasts of Florida and, from the University of Nebraska, found uni­ even though unusual, is not considered to be strobilate forms of this or a closely related an abnormality. The low frequency from species from the same host in Nicaragua. widely separated areas suggests a consistency which could be controlled genetically or par­ Multistrobilate forms tially by host influence. Less than 1% of the worms recovered from The multistrobilate condition could repre­ C. leuC1.ls taken off Miami, Florida, and in sent a type of asexual multiplication where a Galveston Bay, Texas, exhibited multistrobi­ portion of scolex buds off distally, taking with lization with up to 14 strobilae originating from it a single strobila or several strobilae. Dr. a single scolex (Fig. 4). Multistrobilate forms Simmons (pel's. comm.) indicated this possi­ of the same species have also been collected by bility in his observations. In the present study, Dr. John Simmons, Department of Zoology, the authors did not see evidence of this con­ University of California at Berkeley, from C. dition, but certainly do not dismiss it as a leucus taken off Sarasota, Florida, with as possibility. Eckert et al. (1969) , in dis­ many as 24 strobilae (pel's. comm.). cussing asexual multiplication in M. corti, men­ Sectioned material reveals that the scolex tioned that in their experiments "individual possesses a complex series of tubules which tetrathyridia appeared to vary widely in their delineate the site of strobila formation by a 'readiness' to respond in the usual manner ..." "swirling" pattern (Fig. 5). The isolated site to the stimulus of strobilization that the in­ of origin is where cellular differentiation takes testinal environment provided. Experimenta­ place, forming the muscular wall of the neck tion is necessary to better understand the region (Figs. 6, 7) . Where the strobila multistrobilate phenomenon. emerges from the scolex, there are well-defined cortical and medullary regions with longi­ ACKNOWLEDGMENTS tudinal collecting tubules (Fig. 8). When two The authors would like to express their strobilae emerge from the same source, one thanks to Dr. John Simmons, University of appears to degenerate (Fig. 3). A "budding" California at Berkeley, for the loan of speci­ process similar to that described by Eckert mens and field notes and to Mr. Dave Powell, et al. (1969) is also seen in some mature seg­ Curator of Fishes, Sea World, San Diego, Cali­ ments, but it seems to degenerate after a short fornia, for making hosts available for examina­ period of growth (Fig. 9) . tion. Dr. Samuel H. Gruber, of the University Asexual multiplication of cestodes in verte­ of Miami, provided some additional material. brates has been reported. Triplotaenia mirab­ We are also grateful to Dr. Gerald Schmidt, ilis Boas, 1902, typically has an unsegmented University of Northern Colorado, for reviewing strobila arising from each side of the scolex. the manuscript and to Lorraine Peterson for Heyneman (1961) found multiple branching her exceptional technical help. existing throughout adult specimens of Hy­ menolepis nana Siebold, 1853, from a specific LITERATURE CITED stock of DBA/1 strain mice only. Abnormal DELYAMURE, S. L. 1955. Helminthofauna of splitting of the strobila below the neck is Marine Mammals (Ecology and Phylogeny). rather common in diphyllobothriids as exem- Izdatel'stvo Akademii Nauk SSSR, Moskva. DAILEY AND OVERSTREET-NEW MULTISTROBILATE TAPEWORM FROM BULL SHARK 473

English translation by Israel Prog. for Sci. SOUTHWELL, T. 1927. On a collection of ces­ Trans. (1968).520 p. todes from marine fishes of Ceylon and India. ECKERT, J., T. VON BRAND, AND MARIETTA VOGE. Ann. Trop. Med. Parasit. 21: 351-373. 1969. Asexual multiplication of Mesocestoides THATCHER, V. E. 1961. Studies on the Cestoda corti (Cestoda) in the intestine of dogs and of elasmobranch fishes of the northern Gulf skunks. J. Parasit. 55: 241-249. of Mexico. Part I. Proc. Louisiana Acad. Sci. HEYNEMAN, D. 1961. A natural population of 23: 65-74. anomalous branched tapeworms, Hymenolepis WATSON, D. E. 1966. Some helminth parasites nana (Cestoda: Hymenolepididae) in a colony of DBA!1 mice. Nature 191 :297-298. of fishes in fresh waters of Nicaragua. Un­ MUELLER, J. F. 1966. Host-parasite relation­ published Ph.D. dissertation, University of ships as illustrated by the cestode Spirometra Nebraska, 96 p. mansonoides. In J. E. McCauley (ed.), Host­ YAMAGUTI, S. 1959. Systema Helminthum. Vol. Parasite Relationships. Oregon State Univer­ II. The Cestodes of Vertebrates. Interscience sity Press, Corvallis, p. 15-58. Publishers, Inc., New York, 860 p.