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6-1992

Cestode Parasites in motoro (Natterer) (: ) from Southwestern Brazil, including Rhinebothroides mclennanae n. sp. (Tetraphyllidea: Phyllobothriidae), and a Revised Host-Parasite Checklist for Helminths Inhabiting Neotropical Freshwater Stingrays

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

Jose F.R. Amato Universidade Federal Rural do Rio de Janeiro

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Brooks, Daniel R. and Amato, Jose F.R., "Cestode Parasites in Potamotrygon motoro (Natterer) (Chondrichthyes: Potamotrygonidae) from Southwestern Brazil, including Rhinebothroides mclennanae n. sp. (Tetraphyllidea: Phyllobothriidae), and a Revised Host-Parasite Checklist for Helminths Inhabiting Neotropical Freshwater Stingrays" (1992). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 247. https://digitalcommons.unl.edu/parasitologyfacpubs/247

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. J. Parasito., 78(3), 1992, p. 393-398 ? American Society of Parasitologists 1992

CESTODEPARASITES IN POTAMOTRYGONMOTORO (NATTERER) (CHONDRICHTHYES:POTAMOTRYGONIDAE) FROM SOUTHWESTERNBRAZIL, INCLUDING RHINEBOTHROIDESMCLENNANAE N. SP. (TETRAPHYLLIDEA:PHYLLOBOTHRIIDAE), AND A REVISED HOST-PARASITECHECKLIST FOR HELMINTHSINHABITING NEOTROPICALFRESHWATER STINGRAYS

Daniel R. Brooks and Jose F. R. Amato* Department of Zoology, Universityof Toronto, Toronto, Ontario, Canada M5S 1A1

ABSTRACT: Specimensof 5 species of cestodes were collected in 6 specimens of the freshwaterstingray species Potamotrygonmotoro (Natterer),collected in the vicinity of Corumba,Mato Grosso do Sul, Brazil.Acantho- bothriumregoi, Potamotrygonocestusorinocoensis, Rhinebothroides venezuelensis, and Rhinebothriumparatry- goni are reportedfrom P. motoroand from southwesternBrazil for the firsttime. Rhinebothroidesmclennanae n. sp. appears to be the sister species of Rhinebothroides glandularis, the only other member of the genus exhibiting darkly staining glandular cells lying free in the parenchyma surrounding the terminal genitalia. The new species resembles Rhinebothroidesglandularis, Rhinebothroides freitasi, and Rhinebothroidesscorzai by having poral ovarian arms that extend anteriorly beyond the posterior margin of the cirrus sac, coiled vaginae, and vitelline follicles not interrupted on the poral side in the vicinity of the genital pore. It differs from all 6 previously described members of the genus by possessing an average of 31 testes per proglottid, compared with an average of 45 for R. glandularis, 55 for R. freitasi and R. venezuelensis, 77 for Rhinebothroides circularisi and Rhinebothroidesmoralarai, and 80 for R. scorzai. An updated phylogenetictree for Rhinebothroidesis presented.

Stingrays of the family Potamotrygonidae, sam. All measurements are in micrometers. Measure- permanently restricted to neotropical freshwater ments are based on 25 observations unless noted by host a rich helminth fauna that "n," indicating a higher number of observations as habitats, strongly stated in each case. reflects their Pacific marine ancestry (Brooks, Thorson, and Mayes, 1981; Brooks and Dear- dorff, 1988; Brooks and McLennan, 1991). On DESCRIPTION 29 May 1988, 6 specimens of Potamotrygon mo- Rhinebothroides mclennanae n. sp. 1-4) toro (Natterer), collected in the vicinity of Co- (Figs. rumba, Mato Grosso do Sul, Brazil, were ex- Description(based on examinationof 70 specimens): Strobila craspedote, apolytic, up to 25 mm com- amined for helminth of 5 long, parasites. Specimens posed of 16-25 proglottids. Scolex with 4 pedicellated, species of cestodes were collected, 4 of which are bilobed, elongate bothridia; apical complex lacking. reported from P. motoro and from the Pantanal Pedicels contractile, 188-312 long. Bothridia 625-875 region of Brazil for the first time and 1 of which long by 281-418 wide; hingelike constriction between lobes; divided into and medial is described herein as a new species. marginal portions by indistinct marginal septum; divided horizontally by 24-29 septa; medial loculi 49-59 in MATERIALS AND METHODS number; marginal loculi 49-59 in number. Immature proglottids squared Stingrays were collected with hand-held spears. Ces- to longer than wide. Mature proglottids 938-1,950 long todes were relaxed in tap water until moribund, then by 294-438 wide. Testes in 2 broad fields in anterior fixed in alcohol-formalin-acetic acid and stored in 70% 2/3 of proglottid, 19-43 in number (n = 293; x = 31); ethanol. Whole mounts were stained with Mayer's he- 25-47 in diameter. Cirrus sac in posterior 20-25% of matoxylin and mounted in Canada balsam. Serial cross proglottid, 218-344 long by 50-70 wide, containing sections of proglottids were cut 5 um thick, stained spined eversible cirrus and internal seminal vesicle, with hematoxylin-eosin, and mounted in Canada bal- poral end surrounded by darkly staining cells lying free in the parenchyma. External seminal vesicle extending length of cirrus sac, with extensive coiling immediately Received 12 July 1991; revised 30 January 1992; anterior to cirrus sac, joining cirrus sac near poral end accepted 31 January 1992. and vas deferens near posterior end of Gen- * proglottid. Instituto de Biologia, Universidade Federal Rural do ital atrium shallow; genital pores alternating irregularly Rio de Janeiro, km 47 antiga Rodovia Rio-Sao Pau- 22-33% (x = 27%) of total proglottid length from pos- lo, 23851 -Seropedica, Rio de Janeiro, Brazil. terior end. Vagina anterior to cirrus sac, coiled; vaginal 393 394 THE JOURNALOF PARASITOLOGY,VOL. 78, NO. 3, JUNE 1992

sphincter and seminal receptacle present. Ovary bi- terior of genital pore; 125-188 wide at isthmus. Vi- lobed in frontalview, X-shapedin cross section;aporal telline follicles lateral,extending from anteriorextent lobe 468-812 long, extendinganteriorly to level of pos- of testicularfields to near posteriorend of proglottid, teriorextent oftesticular field; poral lobe 218-375 long, not interruptednear genital pore; 9-25 in diameter. extendinganteriorly to level of cells surroundingpos- Terminalgravid attached proglottids 1,625-2,218 long by 362-456 wide, tapered posteriorly with spinose quadrilobedposterior ends; lacking ovaries and with degeneratingtestes. Genital pore 25-31% (x = 27%)of 1 \ proglottidlength from posterior end. Uterus saccate with 44-64 (x = 55) lateraldiverticula. Eggs 15-18 in •C diameter, oncospheres 14-17 in diameter, not em- r bryonatedin utero. Taxonomic summary Typehost: Potamotrygonmotoro (Natterer) (Chon- drichthyes:: Potamotrygonidae). Type locality: Vicinity of Corumba,Mato Grosso do Sul, Brazil. Site of infection: Middle third of spiral valve. Specimensdeposited: Holotype: Instituto Oswaldo Cruz no. 32.814a. Paratypes:Instituto Oswaldo Cruz no. 32.814b-f (75 specimens);Harold W. ManterLab- oratory, Division of Parasitology,University of Ne- braskaState Museum no. 34091 (2 specimens). Etymology: The species is named for Deborah A. McLennan. o Remarks Rhinebothroidesmclennanae is the seventh species named to this genus of cestodes, all of which are re- strictedto potamotrygonidstingrays. The new species appearsto be the sisterspecies of Rhinebothroidesglan- dularis Brooks, Mayes, and Thorson, 1981, the only other member of the genus exhibitingdarkly staining glandularcells lying free in the parenchymasurround- ing the terminalgenitalia. We are not aware that this featureis found in any other tetraphyllideansand con- sider it a synapomorphyfor R. glandularis plus R. mclennanae. The new species further resembles R. glandularis, Rhinebothroidesfreitasi (Rego, 1979) Brooks, Mayes, and Thorson, 1981, and Rhineboth- roides scorzai (Lopez-Neyraand Diaz-Ungria, 1958) Mayes, Brooks, and Thorson, 1981, and differsfrom Rhinebothroidesmoralarai (Brooks and Thorson,1976) Mayes, Brooks, and Thorson, 1981, Rhinebothroides venezuelensisBrooks, Mayes, and Thorson, 1981, and Rhinebothroidescircularisi Mayes, Brooks, and Thor- son, 1981, by having poral ovarian arms that extend anteriorlybeyond the posterior margin of the cirrus sac, coiled vaginae, and vitelline follicles not inter- rupted on the poral side in the vicinity of the genital pore. Rhinebothroidesmclennanae differs from all 6 previously described members of the genus by pos- sessingsubstantially fewer testes per proglottid(an av- erage of 31, with a range of 19-43). Rhinebothroides glandularisaverages 45 testes per proglottid, with a rangeof 41-51, R. freitasi averages55 with a rangeof 48-64, R. venezuelensisaverages 53 with a range of 45-64, R. circularisiand R. moralaraiaverage 77 with a range of 66-88, and R. scorzai averages 80 with a rangeof 60-99. FIGURES1-4. Rhinebothroides mclennanae n. sp. Figure 5 depicts a phylogenetictree for Rhineboth- 1. Scolex. 2. Matureattached proglottid.3. Terminal roidesspecies, based on the charactersused by Brooks, genitalia.4. Gravid attached proglottid.Scale bar in- Mayes,and Thorson(1981) for the same taxa. The new dicating 500 ,umis for Figures 1, 2, 4; scale bar indi- tree differs only in the inclusion of R. mclennanae, cating 100 uimis for Figure 3. which is corroboratedas the sister species of R. glan- BROOKSAND AMATO-HELMINTHSFROM NEOTROPICAL FRESHWATER STINGRAYS 395

R. R. R. R. R. R. R. moralarai venezuelensis circularisi scorzai freitasi glandularis mclennanae

7 (0) \ 7L8 (3)

48 (2) 9(1) 6(1)

4 9(1) .8(1)

4(1) \ 7 (1) 3(1) 5(1)

2(1) 1(1)

FIGURE5. Phylogenetic tree for 7 species of Rhinebothroides.Numbers accompanying slash marks on tree refer to putative synapomorphies as follows: 1-1, external seminal vesicle joining cirrus sac near poral end; 2-1, aporal ovarian lobes elongate; 3-1, vitellaria interrupted near genital pore on pore side; 4-1, poral ovarian lobe extending anteriorly only to posterior end of cirrus sac; 5-1, vagina coiled; 6-1, darkly staining glandular cells lying free in the parenchyma surrounding the terminal genitalia; 7-0, proglottids acraspedote; 7-1, proglottids craspedote; 8-1, averages of 53-55 testes per proglottid; 8-2, an average of 45 testes per proglottid; 8-3, an average of 31 testes per proglottid; 9-1, 49-59 loculi per bothridium; 9-2, 41-45 loculi per bothridium.

dularis. Outgroup comparisons relied on several levels of 60-99 testes per proglottid, with averages of 77-80 of outgroups including phyllobothriids having medial (R. scorzaihas 60-99 testes per proglottidreported for and marginal loculi and genitalia located near the ovary it, whereasR. circularisiand R. moralaraihave 66-88 (see also Brooks, Mayes, and Thorson, 1981), and gen- reported). Four species have derived conditions: R. eral tetraphyllidean and general eucestode traits as sug- venezuelensishas an average of 53; R. freitasi has an gested by a phylogenetic analysis of the higher level averageof 55; R. glandularishas an averageof 45; and relationships among major eucestode groups (Brooks R. mclennanaehas an average of 31. Based on char- et al., 1991). Six characters could be polarized un- acter optimization, we consider the conditions exhib- ambiguously in this manner as the apomorphic states ited by R. venezuelensisand R.freitasi to be convergent in binary transformation series: external seminal ves- traits (8-1 in Table I and Fig. 5), the condition exhibited icle joining cirrus sac near poral end (1-1 in Table I by R. glandularisto be derived from that found in R. and Fig. 5); elongate aporal ovarian lobes (2-1 in Table freitasi (8-2 in Table I and Fig. 5), and that found in I and Fig. 5); vitellaria interrupted near genital pore R. mclennanaeto be derived from that found in R. on pore side (3-1 in Table I and Fig. 5); poral ovarian glandularis(8-3 in Table I and Fig. 5). lobe extending anteriorly only to posterior end of cirrus Second, the number of medial loculi per bothridium sac (4-1 in Table I and Fig. 5); vagina coiled (5-1 in (which is the same as the number of marginal loculi Table I and Fig. 5); and darkly staining glandular cells per bothridiumin Rhinebothroides)(character 9 in Ta- lying free in the parenchyma surrounding the terminal ble I and Fig. 5) also varies greatly among these species, genitalia (6-1 in Table I and Fig. 5). Three additional and the structure of the bothridia themselves makes it transformation series provided ambiguous informa- more difficult to assess loculi number consistently. tion, for which outgroup comparisons were augmented However, the number ofbothridial loculi has been used by functional outgroup analysis and phylogenetic op- as an important taxonomic character for other tetra- timization (Brooks and McLennan, 1991; Wiley et al., phyllideangroups, such as Rhinebothriumand its rel- 1991). atives, and Echeneibothriumand its relatives.Current First, functional outgroup analysis and optimization reportslist R. moralaraias having 45-49 medial loculi of testes number per proglottid (character 8 in Table I per bothridium,R. venezuelensisas having 51-53 loc- and Fig. 5) are consistent with the hypothesis that the uli, R. circularisias having 69-79, R. scorzaias having plesiomorphiccondition in Rhinebothroidesis a range 69-79, R.freitasi as havingapproximately 59, R. glan- 396 THEJOURNAL OF PARASITOLOGY, VOL. 78, NO.3, JUNE1992

TABLE I. Data matrix summarizingcharacter argu- portedfor the R. freitasi-R. glandularis-R.mclennan- mentation for 9 transformationseries for 7 species of ae group,the values for R. moralaraifall below them. Rhinebothroides.* The only differencebetween the alternativesis the rec- ognition of an autapomorphictrait for R. moralarai, Characters so the phylogenetictree topology is not affected.We Taxa 1 2 3 4 5 6 7 8 9 have chosen the latter interpretation,which results in the hypothesis that the condition found in R. vene- OG 0 0 0 0 0 0 0 0 0 zuelensis(9-1) is convergentwith that found in the R. MO 1 1 1 1 0 0 0 0 2 frietasi-R. glandularis-R.mclennanae group (9-1) and VE 1 1 1 1 0 0 1 1 1 is plesiomorphicto the condition found in R. mora- CI 1 1 1 1 0 0 0 0 0 larai (9-2 in Table I and Fig. 5). SC 1 1 0 0 1 0 1 0 0 FR 1 1 0 0 1 0 0 1 1 Third, proglottidsof Rhinebothroidesspecies may GL 1 1 0 0 1 1 1 2 1 be craspedoteor acraspedote(character 7 in Table I MC 1 1 0 0 1 1 1 3 1 and Fig. 5). The generalplesiomorphic condition among all eucestodes is acraspedote,but the derived condi- * OG, outgroup; MO, R. moralarai; VE, R. venezuelensis; CI, R. circu- tion, craspedoteproglottids, appears to be a relatively larisi; SC, R. scorzai; FR, R. freitasi; GL, R. glandularis; MC, R. mclen- common and convergenttrait. Treatingthe craspedote nanae. 1-0, no external seminal vesicle joining cirrus sac near poral condition as apomorphicfor Rhinebothroidesleads to end; 1-1, external seminal vesicle joining cirrus sac near poral end; 2-0, the postulatethat craspedote proglottids have appeared aporal ovarian lobes not elongate; 2-1, aporal ovarian lobes elongate; 2 times in and have been 3-0, vitellaria not interrupted near genital pore on pore side; 3-1, vitel- independently(7-1 Fig. 5) laria interrupted near genital pore on pore side; 4-0, poral ovarian lobe secondarilylost once (7-0 in Fig. 5). extending anterior to posterior end of cirrus sac; 4-1, poral ovarian TableI presentsa datamatrix summarizing the above lobe extending anteriorly only to posterior end of cirrus sac; 5-0, vagina characterargumentation in a formatsuitable for com- not coiled; 5-1, vagina coiled; 6-0, no darkly staining glandular cells puter-assistedanalysis. Phylogeneticanalysis of this lying free in the parenchyma surrounding the terminal genitalia; 6-1, matrix using the PAUP 3.0 computer program (all darkly staining glandular cells lying free in the parenchyma surrounding charactersordered, rooted with an all-zero outgroup the terminal genitalia; 7-0, proglottids acraspedote; 7-1, proglottids function,Acctran or Deltranoptimization, Branch and craspedote; 8-0, averages of 77-80 testes per proglottid; 8-1, averages Bound option) produces the tree shown in Figure 5, of 53-55 testes per proglottid; 8-2, an average of 45 testes per proglottid; 8-3, an average of 31 testes per proglottid; 9-0, 69-79 loculi per bothrid- with a consistencyindex of 75%. ium; 9-1, 49-59 loculi per bothridium; 9-2, 41-45 loculi per bothrid- ium. DISCUSSION We collected specimens of 4 other species of cestodes in the P. motoro from near Corumba. dularisas and R. mclennanaeas having 51-59, having These included Potamotrygonocestus orinocoen- 49-59. If we beginconservatively by recognizing2 cat- egoriesof loculi number,69-79 and 45-59, functional sis Brooks, Mayes, and Thorson, 1981, Acan- outgroupanalysis is consistentwith the hypothesisthat thobothrium regoi Brooks, Mayes, and Thorson, the plesiomorphiccondition is 69-79 medial loculi, 1981, and R. venezuelensis Brooks, Mayes, and becauseR. scorzaiand R. circularisiare basal members Thorson, 1981, which were known previously of their subcladeswithin Rhinebothroides. respective from the delta of the Orinoco River in Ven- Characteroptimization supports either the hypothesis only that 45-59 loculi is the plesiomorphiccondition or that ezuela (Brooks, Mayes, and Thorson, 1981) and 69-79 is the plesiomorphiccondition, because each which had never been collected in P. motoro. In hypothesis requires convergent evolution of the de- addition, we collected specimens of Rhineboth- rived state. We have the that 69- adopted hypothesis rium paratrygoni Rego and Dias, 1976, known 79 loculi is the plesiomorphiccondition, because two criteria (characteroptimization and functional out- previously from the delta of the Orinoco River, group analysis) are consistent with it. Using the ple- the Rio Salobra, Mato Grosso, Brazil, and near siomorphiccondition as a referencepoint, 2 groupsof Hohenau, Paraguay, but never previously col- species exhibit derived conditions for numbersof bo- lected in P. motoro. Thus, this report constitutes thridialloculi. the values of R. First, reported freitasi, new host and records for all 4 R. glandularis,and R. mclennanaefall within 49-59 locality species. loculi, and we consider them to have the same state Voucher specimens of them have been deposited (9-1 in Table I and Fig. 5). Second, there appearto be in the collection of the Instituto Oswaldo Cruz 2 ways of interpretingthe observationsthat R. vene- (nos. 32.816a-f [P. orinocoensis, 15 specimens], zuelensis has 51-53 loculi and R. moralaraihas 45- 32.817a-f[A. regoi, 20 specimens], 32.818a-f[R. 49 loculi. On one hand, the total rangeof 45-53 loculi exhibitedby the 2 species is not broader,and does not venezuelensis, 78 specimens], and 32.819a-f [R. differsubstantially from, that exhibitedby the R. frei- paratrygoni, 7 specimens]) and the Harold W. tasi-R. glandularis-R. mclennanae group; therefore, Manter Laboratory, University of Nebraska State these 2 species could be consideredto exhibit a com- Museum (nos. 34094 [P. orinocoensis, 2 speci- mon trait that is with the condition found convergent 34093 2 34092 in the R. freitasi-R. glandularis-R.mclennanae group. mens], [A. regoi, specimens], [R. Alternatively,it could be recognizedthat althoughthe venezuelensis, 3 specimens], and 34095 [R. para- value for R. venezuelensisfalls within the values re- trygoni, 1 specimen]). BROOKSAND AMATO-HELMINTHSFROM NEOTROPICAL FRESHWATER STINGRAYS 397

TABLE II. Host-parasitelist for helminths inhabiting TABLEII. Continued. neotropicalfreshwater stingrays, revised accordingto the and nomenclatureof Rosa (1985).*

Host species Host species Parasite species Parasite species

Potamotrygon magdalenae (Valenciennes, 1865) Trygon sp. (this could have been a species of Plesiotrygon, Paratrygon, Potamotrygonocestus magdalenensis Brooks and Thorson, 1976 or Potamotrygon) Acanthobothrium quinonesi Mayes, Brooks, and Thorson, 1978 Eutetrarhynchus araya (Woodland, 1934) Rego and Dias, 1976 Rhinebothroides moralarai (Brooks and Thorson, 1976) Mayes, Brooks, and Thorson, 1981 * Parasite records are from Woodland (1934), Lopez-Neyra and Diaz- Paravitellotrema overstreeti Brooks, Mayes, and Thorson, 1979 Ungria (1958), Brooks and Thorson (1976), Rego and Diaz (1976), Mayes, Brooks, and Thorson Potamotrygon yepezi Castex and Castello, 1970 (1978, 1981a, 1981b), Brooks, Mayes, and Thorson (1979, 1981), Rego (1979), Brooks, Thorson, and Mayes Potamotrygonocestus amazonensis Brooks, Mayes, and Thorson, 1981 (1981), and Deardorff et al. (1981). Acanthobothrium quinonesi Mayes, Brooks, and Thorson, 1978 Rhinebothroides venezuelensis Brooks, Mayes, and Thorson, 1981 Potamotrygon orbignyi (Castelnau, 1855) Eutetrarhynchus araya (Woodland, 1934) Rego and Dias, 1976 Brooks, Mayes, and Thorson (1981) suggested Potamotrygonocestus amazonensis Mayes, Brooks, and Thorson, 1981 that identification of host species for helminths Potamotrygonocestus orinocoensis Brooks, Mayes, and Thorson, 1981 Acanthobothrium regoi Brooks, Mayes, and Thorson, 1981 inhabiting neotropical freshwater stingrays was Rhinebothrium paratrygoni Rego and Dias, 1976 tentative in some cases, due to the confused no- Rhinebothroides venezuelensis Brooks, Mayes, and Thorson, 1981 menclature of the potamotrygonids. Because of Rhinebothroides glandularis Brooks, Mayes, and Thorson, 1981 Rhinebothroides scorzai (Lopez-Neyra and Diaz-Ungria, 1958) Mayes, this, they reported that they had deposited rep- Brooks, and Thorson, 1981 resentative specimens of their hosts in the U.S. Echinocephalus daileyi Deardorff, Brooks, and Thorson, 1981 National Museum of Natural History. Subse- Potamotrygon constellata (Vaillant, 1880) quently, Rosa (1985) revised the family, includ- Potamotrygonocestus amazonensis Mayes, Brooks, and Thorson, 1981 ing examination of the specimens deposited Acanthobothrium amazonensis Mayes, Brooks, and Thorson, 1978 by Rhinebothroides circularisi Mayes, Brooks, and Thorson, 1981 Brooks, Mayes, and Thorson, and clarified many Paraheteronchocotyle tsalickisi Mayes, Brooks, and Thorson, 1981 of the nomenclatural problems. According to Potamotrygonocotyle amazonensis Mayes, Brooks, and Thorson, 1981 Rosa's all Echinocephalus daileyi Deardorff, Brooks, and Thorson, 1981 study, previous records for Potamo- histrix and reticulatus in Potamotrygon motoro (Natterer, 1841) trygon Potamotrygon the delta of the Eutetrarhynchus araya (Woodland, 1934) Rego and Dias, 1976 Orinoco River in Venezuela Potamotrygonocestus orinocoensis Brooks, Mayes, and Thorson, 1981 should be assigned to Potamotrygon orbignyi, and Acanthobothrium regoi Brooks, Mayes, and Thorson, 1981 all records for Potamotrygon circularis collected Acanthobothrium terezae Rego and Dias, 1976 Rhinebothrium paratrygoni Rego and Dias, 1976 near Leticia, Colombia, should be assigned to Rhinebothroides scorzai (Lopez-Neyra and Diaz-Ungria, 1958) Mayes, Potamotrygon constellata. Table II is a new host- Brooks, and Thorson, 1981 parasite checklist for helminths Rhinebothroides venezuelensis Brooks, Mayes, and Thorson, 1981 inhabiting po- Leiperia gracile (Diesing, 1835) tamotrygonids reflecting Rosa's findings. Brevimulticaecum sp.

Potamotrygonfalkneri Castex and Maciel, 1963 ACKNOWLEDGMENTS Eutetrarhynchus araya (Woodland, 1934) Rego and Dias, 1976 We acknowledge financial assistance from the Rhinebothrium and 1976 paratrygoni Rego Dias, Conselho Nacional de Desenvolvmento Cienti- Potamotrygon histrix (Muller and Henle, 1844) (these records may not fico e of Brasil in the form of a all refer to P. histrix) Tecnologico grant to to Eutetrarhynchus araya (Woodland, 1934) Rego and Dias, 1976 J.F.R.A. bring D.R.B. and Deborah A. Potamotrygonocestus travassosi Rego, 1979 species inquirenda McLennan to Brazil to conduct a workshop and Rhinebothrium paratrygoni Rego and Dias, 1976 to perform joint fieldwork. Funds for part of this Rhinebothroides freitasi Rego, 1979 Megapriapus ungriai Lopez-Neyra and Diaz-Ungria, 1958 study were provided by operating grant A7696 from the Paratrygon aiereba (Muller and Henle, 1841) Natural Sciences and Engineering Re- Rhinebothroides scorzai (Lopez-Neyra and Diaz-Ungria, 1958) Mayes, search Council of Canada to D.R.B. We es- Brooks, and Thorson, 1981 pecially thank the director and staff of the EM- Paratrygon sp. (as Elipesurus sp.) BRAPA laboratory in Corumba, Mato Grosso Acanthobothrium terezae Rego and Dias, 1976 do Sul, who kindly provided laboratory space Rhinebothrium paratrygoni Rego and Dias, 1976 and technical assistance. We also thank Joao Ba- Rhinebothroides scorzai (Lopez-Neyra and Diaz-Ungria, 1958) Mayes, Brooks, and Thorson, 1981 tista Catto and Marcello Knoff, who acted as field and laboratory assistants. 398 THE JOURNALOF PARASITOLOGY,VOL. 78, NO. 3, JUNE 1992

LITERATURECITED LOPEZ-NEYRA,C. R., AND C. DIAZ-UNGRIA. 1958. Venezuela. V. Cestodes de vertebra- BROOKS,D. R., ANDT. L. DEARDORFF.1988. Rhine- Cestodes de Nova Ciencia 23: bothrium devaneyi n. sp. (Eucestoda: Tetraphyl- dos Venezolanos (segunda nota). 1-41. lidea) and Echinocephalus overstreetiDeardorffand M. A., D. R. BROOKS,AND T. B. THORSON. Ko, 1983 (Nematoda: Gnathostomatidae) in a MAYES, 1978. Two new ofAcanthobothrium thorny back ray, Urogymnus asperrimus, from species (Ces- from Colombian fresh- Enewetak Atoll, with phylogenetic analysis of both toidea: Tetraphyllidea) water of 64: 838- species groups. Journal of Parasitology 74: 459- stingrays. Journal Parasitology 465. 841. AND . 1981 a. Two new tetra- , E. P. HOBERG,AND P. J. WEEKES.1991. Pre- , cestodes from the freshwater liminary phylogenetic systematic analysis of the phyllidean with Eucestoda Southwell, 1930 (Platyhelminthes: Cer- Potamotrygon circularis (Garman), proposal of a new of the comeria). Proceedings of the Biological Society of genus. Proceedings Helmintholog- ical of 48: 38-42. Washington D.C. 104: 661-668. Society Washington AND . 1981b. , M. A. MAYES,AND T. B. THORSON. 1979. , Potamotrygono- n. Mono- Paravitellotrema overstreeti sp. n. (Digenea: Hemi- cotyle tsalickisi gen. et sp. (Monogenea: and amazonensis uridae) from the Colombian freshwater stingray cotylidae) Paraheteronchocotyle et n. from Potamotrygon magdalenae Dumeril. Proceedings gen. sp. (Monogenea: Hexabothriidae) circularis Garman of the Helminthological Society of Washington 46: Potamotrygon (Chondrichthy- Brazil. 52-54. es: Potamotrygonidae) in northwestern of the of , AND . 1981. Systematic review Proceedings Biological Society Washing- ton D.C. 94: 1205-1210. of cestodes infecting freshwater stingrays (Chon- REGO,A. A. 1979. Contribucao ao conhecimento dos drichthyes: Potamotrygonidae) including four new helmintos de raias fluviais Revis- species from Venezuela. Proceedings of the Hel- Paratrygonidae. ta Brasileira de 39: 879-890. minthological Society of Washington 48: 43-64. Biologia A. P. L. DIAS. 1976. Estudos de cestoides , AND D. A. MCLENNAN. 1991. Phylogeny, ,AND de do Brasil. 3a nota: Cestoides de raias ecology and behavior: A research program in com- peixes fluviais Revista Brasileira de Bio- parative biology. University of Chicago Press, Paratrygonidae. 36: 941-956. Chicago, 434 p. logia R. S. 1985. A revision of the South , AND T. B. THORSON. 1976. Two tetraphyl- ROSA, systematic lidean cestodes from the freshwater stingray Po- American freshwater stingrays (Chondrichthyes: Dissertation. tamotrygon magdalenae Dumeril in Colombia. Potamotrygonidae). Unpublished The of William and in Wil- Journal of Parasitology 62: 943-947. College Mary Virginia. 542 , ANDM. A. MAYES. 1981. Freshwater liamsburg, Virginia, p. E. D. SIEGEL-CAUSEY, D. R. BROOKS, AND stingrays (Potamotrygonidae) and their helminth WILEY, O., V. A. FUNK. 1991. The compleat cladist: A prim- parasites: Testing hypotheses of evolution and co- of Kan- evolution. In Advances in cladistics: Proceedings er of phylogenetic procedures. University sas 158 of the First Meeting of the Willi Hennig Society, Press, Lawrence, Kansas, p. W. N. F. 1934. Six new cestodes from V. A. Funk and D. R. Brooks (eds.). New York WOODLAND, Amazon fish. of the So- Botanical Garden, New York, p. 147-175. Proceedings Zoological of London 1: 33-44. DEARDORFF,T. L., D. R. BROOKS,AND T. B. THORSON. ciety 1981. Two species ofEchinocephalus (Nematoda: Gnathostomidae) from neotropical stingrays. Journal of Parasitology 67: 433-439.