Serendip Deborahae N. Gen. and N. Sp. (Eucestoda: Tetraphyllidea: Serendipidae N

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Serendip deborahae n. gen. and n. sp. (Eucestoda: Tetraphyllidea: Serendipidae n. fam.) in Rhinoptera steindachneri Evermann and Jenkins, 1891 (Chondrichthyes: Myliobatiformes: Myliobatidae) from Southeastern Ecuador

Daniel R. Brooks University of Toronto, [email protected]

Ramiro Barriga Escuela Politecnica Naciona (Quito, Ecuador)

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Brooks, Daniel R. and Barriga, Ramiro, "Serendip deborahae n. gen. and n. sp. (Eucestoda: Tetraphyllidea: Serendipidae n. fam.) in Rhinoptera steindachneri Evermann and Jenkins, 1891 (Chondrichthyes: Myliobatiformes: Myliobatidae) from Southeastern Ecuador" (1995). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 221. https://digitalcommons.unl.edu/parasitologyfacpubs/221

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SERENDIPDEBORAHAE N. GEN. AND N. SP. (EUCESTODA:TETRAPHYLLIDEA: SERENDIPIDAE N. FAM.)IN RHINOPTERASTEINDACHNERI EVERMANN AND JENKINS,1891 (CHONDRICHTHYES:MYLIOBATIFORMES: MYLIOBATIDAE) FROM SOUTHEASTERNECUADOR

Daniel R. Brooks and Ramiro Barriga* Department of Zoology, Universityof Toronto, Toronto, Ontario, Canada M5S 1A1 ABsTRAcT: Cestodes collected in spiral valves of Rhinoptera steindachneri from the southern coast of Ecuador represent an undescribed species of Tetraphyllidea. The new species has bothridia possessing septa but lacking apical suckers. It is diagnosably distinct from all other tetraphyllidean genera by possessing a scolex comprising 4 triangular bothridia that are fused together forming a platelike structure, each of which is subdivided by 2 simple and 1 bifurcating septa radiating from its base and ringed by marginal loculi; therefore, a new genus is proposed for it. By exhibiting some degree of bothridial fusion, testes arranged in 2 layers in the proglottis and postovarian testes, the new species appears to be a member of a clade containing Dioecotaenia, Duplicibothrium, and Glyphobothrium. The new species possesses vitelline fields that converge dorsally in each proglottis, except for the ovarian and terminal genitalia areas, a feature that has been reported previously only in Duplicibothrium and Glypho- bothrium. Furthermore, Duplicibothrium and Glyphobothrium, like the new species, are markedly protandric. Therefore, we propose that Duplicibothrium, Glyphobothrium, and the new species comprise the sister group of the Dioecotaeniidae, and propose a new family name for the clade. Tritaphros is rejected as a possible sister group for the clade; suggested alternatives include some species of Caulobothrium, Rhodobothrium, or some members of the Phyllobothrium centrurum group.

Nothing is known about the parasite fauna of elasmobranchs for ovarian and terminal genitalia areas, may converge ventrally to form inhabiting the coast of Ecuador. During the initial stages of an a circummedullary band. Parasites of myliobatid stingrays. Western Atlantic and eastern Pacific oceans. of the of Ecuadorian elasmo- inventory parasite biodiversity Typegenus: Serendipn. gen. branchs, stingrays were collected from Puerto Bolivar, Puerto Other genera: Duplicibothrium Williams and Campbell, 1978; Gly- Jeli, and Puerto Hualtaco, Provincia de el Oro. Among the phobothrium Williams and Campbell, 1977. parasites collected were specimens of an undescribed and un- Serendip n. gen. usual tetraphyllidean eucestode, which we describe and discuss Diagnosis: Eucestoda; Tetraphyllidea. Scolex comprising 4 triangular herein. bothridia, each subdivided by septa extending radially from base dividing bothridial face but not into distinct loculi, ringed with marginal MATERIALSAND METHODS loculi with thin velum. Bothridial apical suckers lacking. Bothridia fused to form a structure bothridial faces a dorsal rather in bottom trawls single platelike giving Stingrayswere collected by professionalfishermen than lateral sucker embedded in sea killed in a relaxed aspect; pedicels lacking. Vestigial apical using bag seines. Cestodeswere relaxed water, in tissues of scolex Testes in 2 with and stored in apex. Proglottides apolytic, protandric. condition with hot water, fixed immediately AFA, in each of 2 fields in each Some testes in stained with layers proglottid. postovarian 70% ethanol. Whole mounts were Mayer'shematoxylin. as Cirrus sac of were cut 7 stained with maturing proglottides, disappearing ovary develops. spher- Serial cross sections proglottides gm thick, ical; cirrus armed. Genital pore and counterstainedwith eosin. Whole mounts pre-equatorial. Vagina passing anteriorly Mayer's hematoxylin, to cirrus sac. in cross section; lobes Vitel- cross sections were mountedin Canadabalsam. All measurements Ovary X-shaped digitiform. and laria follicular, medullary, in 2 lateral fields extending length of proglottis are in unless otherwise n = numberof examined ,m noted; specimens ventrally; vitelline fields converging dorsally in each proglottis, except or measured,MEPN refersto Museode la EscuelaPolitecnica Nacional, for ovarian and terminal areas. refersto Museumof Natural genitalia Quito, Ecuador;MNHG History,Geneva, Typeand only species: Serendipdeborahae. Switzerland. n. fam. Serendipidae Serendip deborahae n. sp. Diagnosis: Eucestoda;Tetraphyllidea. Scolex comprising4 rounded (Figs. 1-11) each subdivided in various or triangularbothridia, by septa patterns; Description (based on 9 specimens, 8 whole mounts and 1 scolex or Bothridia some of distinct loculi present lacking. exhibiting degree prepared for scanning electron microscopy and strobila cut in serial fusion to each to or both. Bothridial suckerslacking. other, scolex, apical cross sections): Strobila craspedote, apolytic, up to 60 mm long, com- Pedicels presentor absent. Vestigialapical suckerembedded in tissues of 150 Scolex 1.5-2.6 mm wide. or posed approximately proglottides. of scolex apex or apical pit may be present. Proglottidesapolytic sucker embedded in tissue of scolex 106-219 by Testes in 2 or more in each Vestigial apical long anapolytic;markedly protandric. layers 44-56 wide. Pedicels lacking. Bothridia 0.7-1.2 mm long by 0.8-1.6 proglottis.Postovarian testes present.Cirrus sac sphericalto subspher- mm fused at anterior end into 2 at end into anterior wide, pairs, posterior single ical; cirrusarmed. Genital pore preequatorial.Vagina passing platelike, anteriorly directed, structure; subdivided by 2 simple and 1 to cirrussac. Ovary X-shaped in cross section;lobes digitiform.Vitel- muscular not bothridial of bifurcating, radially diverging, septa dividing lariafollicular, medullary, in 2 lateralfields extending length proglottis face into distinct of bothridia with small loculi and thin, in each loculi; margins ventrally;vitelline fields convergingdorsally proglottis,except contractile, velum-like membrane. Neck 6.9-9.6 mm long. Proglottides slightly craspedote. Immature proglottides wider than long. Mature proglottides squared. Terminal attached proglottides (n = 9) 272-856 long Received 27 April 1994; revised 9 August 1994; accepted 9 August by 546-781 wide. Testes in 2 longitudinal fields and 2 layers extending 1994. of 64-116 in 3-8 25-45 36- * length proglottis, total; preporal, postporal, Departamentode las Ciencias Biologicas, Escuela Politecnica Na- 63 aporal;47-125 in diameter. Cirrussac in anterior 1/3 of proglottis, cional, Apartado2759, Quito, Ecuador. 125-312 long by 156-281 wide, containing spined, eversible cirrus. Vas 80 BROOKSAND BARRIGA-NEW CESTODEFROM ECUADORIAN STINGRAY 81

FIGURES1-4. Scanningelectron micrographs ofSerendip deborahae n. gen., n. sp. 1. En face view of scolex. Scalebar = 500 ,m. 2. Enlargement of bothridial face showing the bifurcatingand 1 of 2 simple septa. Scale bar = 250 gm. 3. Lateralview of scolex. 4. Lateralview of scolex. Magnificationof Figures3 and 4 same as Figure 1. deferensextensively coiled mostly on poral side of cirrussac posterior in diameter. Immatureuterus a glandularsinuous sac extending ven- to testes, with some coils aporal to cirrus sac; joining cirrus sac near trally from ovary to near anteriorend of proglottis.Mature detached posterior end. Genital pores alternatingirregularly, 23-29% of total proglottides(n = 2) longer than wide, 1.47-1.84 mm long by 581-644 proglottislength from anteriorend of terminalproglottid. Genital atri- wide. Genitalpore 20-23% of proglottislength from anteriorend. Cirrus um shallow. Vagina anteriorto cirrus sac and posttesticular,passing sac 375-406 long by 281 wide. Few disintegratingtestes present.Ovary medially,curving posteriorly around aporal side of cirrussac and around 344-456 long by 312-375 wide. Vitelline follicles 18-50 in diameter. dorsalside of vas deferens.Vaginal sphincter prominent, at junction of Gravid detachedproglottides not collected. genital pore. Ovary fan-shapedin frontalview, X-shaped in cross section, with digitiform processes extending laterallyjust beyond osmo- wide. regulatoryducts, 125-281 long by 375-562 Maturingproglottides Taxonomic summary with 4-8 postovariantestes. Vitelline follicles medullary, lateral; follicles extendingdorsolateral and ventrolateralto osmoregulatoryducts, ex- Type host: Rhinopterasteindachneri Evermann and Jenkins, 1891 tending ventrallyfrom anteriorextent of testicularfields to near pos- (Chondrichthyes:Myliobatiformes: Myliobatidae). terior end of ovary, interruptednear genital pore, confluent dorsally Type locality: vic. Puerto Bolivar, Provincia de el Oro, Ecuador. except dorsal to ovary and terminalgenitalia. Vitelline follicles 20-62 Site of infection: Middle 1/3 of spiral valve. 82 THEJOURNAL OF PARASITOLOGY,VOL. 81, NO. 1, FEBRUARY1995

5 6 7

w 0 0 3

FIGURES5-11. Serendipdeborahae n. gen. and n. sp. 5. Schematicrepresentation of a bothridiumshowing 2 simple and 1 bifurcatingsepta forming 5 subdivisions of bothridialface. 6. Matureattached proglottis.7. Dorsal surfaceof mature proglottis,showing distinctive pattern of distributionof vitelline follicles. 8, 9. Cross sections of matureproglottis. 8. Mid-proglottis,showing testes in 2 layers.9. Near posteriorend of proglottis.10. Maturedetached proglottis. 11. Terminalgenitalia. Upper scale bar refersto Figures3-7; lower scale bar refersto Figures8. o = Ovary, v = vitelline follicles, t = testes, u = uterus.

Specimensdeposited: Holotype:MEPN. Paratypes:MEPN; MNHG ciated with the bothridia.Regardless of its convenience,this scheme is no. INVE18254. weakbecause the absenceof hooks is plesiomorphic(Brooks et al., 1991; Symbiotypespecimen: MEPN no. 4569. Brooksand McLennan,1993; Bermanand Brooks, 1994) and thus not Etymology: Schmidt(1974) noted that when he found Dioecotaenia an appropriatecharacter on which to base taxonomicgroupings (Wiley in Rhinopterabonasus and realized it belonged in its own family, he et al., 1991). This may have led Schmidt(1986) to recognizethe Dioe- was temptedto name it Serendip,type genusof the family Serendipidae cotaeniidae,comprising 1 genus with 2 species (which Schmidt placed (serendipity)because he was looking for somethingelse at the time he in its own order)and the Triloculariidae,comprising 4 generawith 5 discovered Dioecotaenia.We discovered this cestode species living in species (Bermanand Brooks, 1994). a species of Rhinopterawhile looking for something else, so we have The "Phyllobothriidae"can be divided into cestodes that have both- named it Serendipto honor the memory of Gerald D. Schmidt. The ridial apical suckers,but lack bothridialsepta dividing the bothridial species is named for Deborah A. McLennan. face into distinct loculi (e.g., Anthobothriumvan Beneden, 1850; Ca- lyptrobothriumMonticelli, 1893; ClistobothriumDailey and Vogelbein, 1990; ClydonobothriumEuzet, 1956; CrossobothriumLinton, 1889; Echeneibothriumvan 1863; Remarks Beneden,1805; Monorygma Diesing, Oryg- matobothriumDiesing, 1863; RhodobothriumLinton, 1889; and the The Tetraphyllidealack much rigorous phylogeneticexamination. Phyllobothriumlactuca species group)and species that have bothridial Traditionalclassifications, e.g., Wardleand McLeod(1952), Euzet (1959), septa dividing the bothridialface into distinct loculi but lack bothridial and Yamaguti (1959), divided the order into 2 families, the Phyllo- apical suckers(e.g., CaulobothriumBaer, 1948; DuplicibothriumWil- bothriidaeand the Onchobothriidae,diagnosed on the basis of the pres- liams and Campbell, 1978; GlyphobothriumWilliams and Campbell, ence (Onchobothriidae)or absence (Phyllobothriidae)of hooks asso- 1977; RhabdotobothriumEuzet, 1953; RhinebothriumLinton, 1889; BROOKSAND BARRIGA-NEW CESTODE FROM ECUADORIAN STINGRAY 83

RhinebothroidesMayes, Brooks,and Thorson, 1981; TritaphrosLonn- like Tritaphros retzii, a member of the Rhinebothrium group berg, 1889; and the Phyllobothriumcentrurum species group).Notably, having 3 bothridial loculi, would be its sister species. Given the Triloculariidae bothridial and the comprisesspecies having septa loculi, bothridial of the members of the + some possessing bothridial apical suckers (TriloculariaOlsson, 1867 morphology Serendipidae and EscherbothriumBerman and Brooks, 1994) and some lackingthem Dioecotaeniidae, this assumption is not warranted, and the search (ZyxibothriumHayden and Campbell, 1981 and PentaloculumAlex- for the sister group of this clade begins anew. Below we list some ander, 1953), and the membersof the Dioecotaeniidaehave bothridial possibilities. loculi but lack apical suckers. Members of the Dioecotaeniidae + Serendipidae possess cir- The absence of bothridialsepta by the firstgroup of phyllobothriids is a plesiomorphictrait that rendersthe taxa a paraphyleticcollection rus sacs in the anterior half, often in the anterior 1/4, of the of undeterminedphylogenetic relationships.Because it contains the proglottis, a trait that is unusual among unarmed tetraphyllid- paraphyleticPhyllobothrium, this group retains the appellationPhyl- eans with loculi and no bothridial apical suckers (although com- lobothriidaepending a full phylogeneticanalysis of the assemblage.The mon among members of the basal "Phyllobothriidae"). Species second the Triloculariidaeand com- group,including Dioecotaeniidae, of from the Rhinebothrium exhibit this prises those taxa that have bothridialsepta and loculi. If the septa and Caulobothrium, group, loculi in all these taxa are homologous, and are nonhomologouswith trait. At least some species of Caulobothrium also have post- the bothridialloculi in many onchobothriids,the group would form a ovarian testes or testes extending posteriorly between the ovarian clade. The form and structureof the bothridiaand the septa and loculi lobes (Brooks et al., 1981). These traits may indicate a phylo- in each of the 3 diverse. of groups are, however, Bothridia the Trilo- genetic relationship between Caulobothrium and the Dioeco- culariidaeare round to elongate with 3-5 loculi arrangedin nonlinear patterns.In the Dioecotaeniidae,the bothridiaare roundedwith close- taeniidae + Serendipidae, although preliminary phylogenetic packedhexagonal loculi arrangedas a centralrow of loculi surrounded analysis indicates that Caulobothrium is paraphyletic, compris- by largemarginal loculi. Glyphobothriumis similarto Dioecotaenia,but ing 2 clades within Rhinebothrium (Brooks, unpubl. data). In the loculi are round to squaredrather than hexagonal.Duplicibothrium addition, members of the Dioecotaeniidae + Serendipidae pos- exhibits bothridiawith transverse and a elongate septa anteriorly cup- sesses bothridial as do members of the shaped posterior end with indistinct radially arrangedsepta. Finally, marginal loculi, Phyl- membersthat we will referto as the "Rhinebothriumgroup" (e.g., Cau- lobothrium centrurum group and Rhinebothroides. Marginal loc- lobothrium,Rhabdotobothrium, Rhinebothrium, Tritaphros, Rhineboth- uli are lacking in all members of the Rhinebothrium group, roides,and the Phyllobothriumcentrurum group), have elongate both- including all species assigned to Caulobothrium. ridia with loculi. Members of the linearly arranged Dioecotaeniidae, Finally, species of Rhodobothrium Linton, 1889 also inhabit Duplicibothrium,Glyphobothrium, and the Rhinebothriumgroup share anotherapparently derived trait, the absenceof bothridialapical suck- myliobatid stingrays, are markedly protandric, have testes lying ers. This may indicate that these taxa are more closely relatedto each in 2 layers in each proglottis, and possess postovarian testes, other than either is to the Triloculariidae;however, 2 members of the suggesting a possible relationship with the Dioecotaeniidae + Triloculariidae,Zyxibothrium and Pentaloculum,also lack bothridial Serendipidae. Like S. deborahae, they possess vestigial suckers suckers.The or absenceof bothridial apical presence apical suckers,by embedded in the scolex of itself, may not be a strongindicator of phylogeneticrelationship, or the apex (the "apical pit" Glyphoboth- Triloculariidaemay be paraphyletic. rium may also be a vestigial apical sucker). Species of this group Serendipdeborahae has bothridiapossessing septa, but lackingapical lack bothridial septa or marginal loculi, although the bothridial suckers.This would seem to place it with the Dioecotaeniidae,Dupli- faces are covered with "numerous convolutions forming an ir- cibothrium,Glyphobothrium, and Rhinebothriumgroup. Dioecotaenia, regular pattern" (Campbell and Carvajal, 1979; Mayes and Duplicibothrium,and Glyphobothriumexhibit severaltraits that appear to be apomorphicamong the Tetraphyllidea,suggesting a relationship Brooks, 1981). They lack the vitelline configuration diagnostic with Serendip.They exhibit some degree of fusion of the bothridia, for the Serendipidae and show no sign of bothridial fusion. If eitherwith each other(Dioecotaenia, Duplicibothrium, Serendip) or with Rhodobothrium is a member of the Dioecotaeniidae + Seren- the scolex (Glyphobothrium).They also possess testes arrangedin 2 dipidae clade, it would be the sister group of the other 2. layers in the proglottisand some postovariantestes. We believe these Phylogenetic systematic studies with 3 traitsindicate that Dioecotaenia,Duplicibothrium, Serendip, and Gly- begin Hennig's Auxiliary phobothriumform a clade. Serendipexhibits vitelline fields that con- Principle (Hennig, 1966; Brooks and McLennan, 1991, 1993; verge dorsallyin each proglottis,except for dorsal to the terminalgen- Wiley et al., 1991) that similarity equals homology. Such initial italia,a featurethat has been reportedpreviously only in Duplicibothrium assumptions are corroborated by congruence with other char- and (Williamsand Like Glyphobothrium Campbell, 1977, 1978). Gly- acters in a phylogenetic analysis and are falsified by incongru- phobothrium,Serendip also lacks vitelline follicles dorsal to the ovary. The radial pattern and arrangementof the bothridial septa, lack of ence. Testing and supporting the above hypotheses of homology distinct loculi, triangularshape of the bothridia,and fusion of the both- and classification consistent with them will require a larger suite ridiato form a singleplatelike structure with dorsalaspect in S. deborah- of characters than the few discussed above. ae, however, differ from previously known tetraphyllideans.In this regard,S. deborahaeis distinct from Duplicibothriumand Glyphoboth- rium, supportingthe designation of a new genus for it. Furthermore, ACKNOWLEDGMENTS Duplicibothriumand Glyphobothrium,like Serendip,are markedlypro- tandric;Dioecotaenia exhibits separate male and female strobila. Of We gratefully acknowledge the cooperation and assistance of secondarysignificance is the observationthat all membersof these taxa Ing. Alfonso Espinosa Ramo, Rector of the Escuela Politecnica inhabit only myliobatid Therefore,we that stingrays. propose Duplici- as well as officials of the of Defense and the bothrium,Glyphobothrium, and Serendipform a clade that is the sister Nacional, Ministry groupof Dioecotaenia.Because its sistergroup is recognizedat the family Ministry of Agriculture, Republic of Ecuador, both in Quito and level, we propose a new family name for the clade containingDuplici- in various localities in the Province of El Oro. We thank the bothrium,Glyphobothrium, and Serendip. people of Puerto Jeli in particular for their unparalleled hos- pitality during our study. We thank Henry Hong, Department of of Toronto for his DISCUSSION Zoology, University help with the SEM portion of this study. Special thanks also to an anonymous Brooks (1982) suggested that if the scolex of Dioecotaenia reviewer who helped focus attention on the relationship between evolved as a result of progressive addition of loculi, a species Serendip, Duplicibothrium, and Glyphobothrium. This study was 84 THEJOURNAL OF PARASITOLOGY,VOL. 81, NO. 1, FEBRUARY1995 funded by operating grant A7696 from the Natural Sciences and phyllidea).Proceedings of the HelminthologicalSociety of Wash- Engineering Council (NSERC) of Canada to D.R.B. ington 46: 88-97. EuzEr,L. 1959. Recherchessur les cestodestetraphyllidesdes selaciens des cotes France.Theses de Ph.D. Facultedes Sciences,Universite LITERATURECITED de Montpellier,Montpellier, France, 263 p. HENNIG,W. 1966. of Illinois ANDD. R. BROOKS. 1994. Escherbothrium molinae Phylogenetic systematics. University BERMAN, R., gen. 263 et n. (Eucestoda:Tetraphyllidea: Triloculariidae) in Urotrygon Press, Urbana, Illinois, p. sp. M. AND D. R. BROOKS.1981. 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