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1995

Comparative Morphology of the Scolices and Microtriches Among Five Species of Tetrabothrius (: Tetrabothriidae)

Eric P. Hoberg USDA-ARS, [email protected]

D. E. Sims University of Prince Edward Island

P. H. Odense National Research Council of Canada

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Hoberg, Eric P.; Sims, D. E.; and Odense, P. H., "Comparative Morphology of the Scolices and Microtriches Among Five Species of Tetrabothrius (Eucestoda: Tetrabothriidae)" (1995). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 725. https://digitalcommons.unl.edu/parasitologyfacpubs/725

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. Parasitol., 81(3), 1995, p. 475-481 ? American Society of Parasitologists 1995

COMPARATIVEMORPHOLOGY OF THESCOLICES AND MICROTRICHESAMONG FIVE SPECIES OF TETRABOTHRIUS (EUCESTODA:TETRABOTHRIIDAE)

E. P. Hoberg, D. E. Sims*, and P. H. Odenset UnitedStates Departmentof Agriculture,Agricultural Research Service, Biosystematicsand NationalParasite Collection Unit, BARC-East #1180, 10300Baltimore Avenue, Beltsville,Maryland 20705-2350

ABSTRAcr:The structureof the scolex, neck, and adjacentstrobila of 5 species of Tetrabothriuswas evaluatedusing low to high magnificationscanning electron microscopy.Species-specific patterns and morphotypes(spiniform, papilliform, and filiform)of microtricheswere found on the scolices and strobilartegument of Tetrabothrius(Oriana) affinis, Tetrabothrius (Oriana)filiformis, and Tetrabothrius(Culmenamniculus) laccocephalus; microtriches were absentin Tetrabothrius(Culmenamniculus) cylindraceus and Tetrabothrius(Tetrabothrius) sp. The presence, distribution,and form of microtrichesmay not be correlatedwith the subgenericdivisions of Tetrabothriusor the host taxon. Unique patternsdo not appearto be sharedwith othergroups of cestodes, particularlyother tetraphyllideans.We suggestthat the spiniform,filiform, and papilliformtypes of microtrichesmay be sym- plesiomorphicfor the Eucestoda.

Microtrich-like structures on the holdfasts of tetraphyllidean cocephalusSplitlich, 1909, Tetrabothrius(Oriana) fiiformis Nybelin, cestodes have been recognized as potentially significant char- 1916, Tetrabothrius(Culmenamniculus) cylindraceus Rudolphi, 1819, and Tetrabothrius latter acters in (Whittaker and Carvajal, 1980; (Tetrabothrius)sp. (the apparentlyundescribed) systematic analyses were recovered while alive from hosts recently collected in the field. Whittaker et al., 1985). Although genera and species of the Specimens were simultaneouslykilled and fixed in hot 10%buffered Onchobothriidae and Phyllobothriidae have received attention neutralformalin and later transferredto 70%ethanol for storage.Spec- in studies using scanning electron microscopy (SEM) (Caira, imens of Tetrabothrius(Oriana) affinis (Lonnberg, 1891) were also ap- collected while but the fixative is unknown. 1992; Caira and Ruhnke, 1990, 1991; Ruhnke, 1993, 1994) parently alive, original The following materialwas studied. Tetrabothrius 8 cestodes members of the have to be examined. affinis: Tetrabothriidae yet froma bluewhale, Balaenoptera musculus (Linnaeus), collected at Hawkes Morphological studies of the scolices among species of Te- Harbor, Labrador(57'13'N; 55'20'W) by R. L. Stevenson on 31 July trabothrius Rudolphi, 1819 have included detailed evaluations 1951 (USNM 81901). Tetrabothriuslaccocephalus: 5 specimens from by Spaitlich (1909), Rees (1956), and Andersen and Lysfjord a greatershearwater, Puffinus gravis (O'Reilly),collected at Gough Is- land, South Atlantic Ocean P. G. on (1982). Considerable information on the configuration of the (40?21'S;9?23'W) by Ryan 11 November 1984 (EPH 2270; and USNM 80012). and Temirova and Tetrabothriusfilizfor- scolex is also presented by Baer (1954) Skria- mis: 10 specimens from a greatershearwater collected at GoughIsland bin (1978). Observations of Tetrabothrius pauliani Joyeux and (collectiondata as above; EPH 2267; and USNM 80010). Tetrabothrius Baer, 1954 and Tetrabothrius sp. from penguins involved SEM, (Tetrabothrius)sp.: 2 specimens from a black-leggedkittiwake, Rissa collectedat Talan northernSea of but high magnifications were not employed (Andersen and tridactyla(Linnaeus) Island, Okhotsk, Russia E.P.H. on 23 1988 there is minimal information on (59'18'N; 149'02'E)by August (EPH 3060; Lysfjord, 1982). Consequently, USNM 81903). Tetrabothriuscylindraceus: 5 specimens from a black- the structure of the of the holdfast and strobila among leggedkittiwake at TalanIsland (collection data as above,USNM 81902). genera and species of the Tetrabothriidae. In preparationfor SEM,specimens were dehydrated through a graded In the present study, using SEM, we evaluated the structure series of ethanol;warmed in 100%ethanol to 35 C; placed for 1 hr at constanttemperature in 1:1 ethanol and II, a fluorocarbonthat of the tegument of the holdfasts and strobila of 5 species of Peldri? may be used as a substitute for critical point drying (Kennedy et al., Tetrabothrius from avian and mammalian hosts. A preliminary 1989). Samples were then placed in 100%Peldri II at 35 C for 1 hr. appraisal is given for the configuration and distributional pat- Followinginfiltration, the sampleswere cooled to 20 C and then placed terns of microtriches as systematic characters in this group. in a low vacuumuntil the Peldr II was completelysublimed. Specimens were mountedon aluminumstubs with double-sided Microtriches are compared among tetrabothriids and some oth- tape, sputtercoat- ed with an estimated 100-250 A of and examined with a er to further elucidate sister re- gold, JEOL tetraphyllideans putative group 35 SEM at 25 kV acceleratingvoltage. lationships for these taxa (Hoberg, 1987, 1989). In the context Meristic and structuralcharacteristics apparent in light microscopy of phylogenetic hypotheses for the Eucestoda (Brooks et al., of these specieshave beenreported extensively in the literature(Splitlich, 1991), microtriches found among tetrabothriids are compared 1909; Baer, 1954; Rees, 1956; Temirova and Skriabin,1978). The fol- focuses on attributesof microtrich-likestructures observed on with those reported among the major orders of cestodes. lowing the tegumentof the bothridia,auricles, apical organ,neck, and strobila. Evaluationof the holdfastamong species of Tetrabothrius,where com- MATERIALSAND METHODS plementary,included those regionsof the scolex suggestedby Cairaand 3 of the 4 of the Tetrabothrius Ruhnke(1990) in studiesof othertetraphyllideans. Terminology for the Species representing subgenera genus structureof follows Caira and Ruhnke and Rich- were examined. Specimens of Tetrabothrius(Culmenamniculus) lac- microtriches (1990) mond and Caira(1991) and aredefined as follows:spiniform = flattened, often blade-likestructures with a base substantiallywider than the apex; Received 14 September 1994; revised 15 December 1994; accepted filiform = typically tubular or cylindricalstructures of consistent di- 15 December 1994. ameter that may vary from relativelyshort to highly elongate;papilli- * Departmentof Anatomyand Physiology,Atlantic Veterinary College, form = ovoid structuresthat are typically wider than long. Measure- University of Prince EdwardIsland, Charlottetown,Prince Edward ments are presentedas length, width, and diameterin micrometersas Island, CanadaCIA 4P3. determinedfrom photomicrographs(with an estimatederror of + 10%); t National ResearchCouncil of Canada, 1411 Oxford Street, Halifax, sample sizes are indicatedas (n=); rangesare presented with meanvalues Nova Scotia, CanadaB3H 3Z2. Deceased. in parentheses. 475 476 THE JOURNALOF PARASITOLOGY,VOL. 81, NO. 3, JUNE 1995

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FIGURES1-5. Tetrabothriusaffinis (scale bars = 500 Am for Fig. 1; 1.0 Am for Figs. 2-5). 1. Apical view of scolex showing view of apical organ and massive sucker-likebothridia, reduced auricles (pointers),and positions of high magnificationviews for Figures 2-5 indicated by arrows.2. Papilliformto filiformmicrotriches on apicalorgan. 3. Spiniformmicrotriches on adherentsurfaces of bothridia.4. Spiniformmicrotriches along marginof bothridium.5. Spiniformmicrotriches covering external surfaces of bothridia.

RESULTS terspecific differences, particularly in the tegument of the hold- fast, were evident. Specimens of T. affinis (Figs. 1-5), T. lac- Among the 5 species examined, the configuration, dimen- cocephalus (Figs. 6-9), and T.filiformis (Figs. 10-22) were found sions, and distributional patterns of microtriches on the scolex, to have species-specific patterns of distribution for papilliform, neck, and strobila did not vary intraspecifically. Substantial in- filiform, and spiniform microtriches that were restricted to par-

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FIGURES6-9. Tetrabothriuslaccocephalus (scale bars = 100 Am for Fig. 6; 1.0 Amfor all other figures).6. Scolex showing generalstructure and positions of high magnificationviews for Figures7-9 indicatedby arrows.7. Spiniformmicrotriches of uniformstructure on adherentsurfaces, apicalorgan, and auricles;depicted is the adherentsurface; arrow on auricleindicates region extending onto apicalorgan where identical microtriches occur. 8. Spiniformmicrotriches on the marginsof the bothridia.9. Spiniformmicrotriches on the neck. HOBERGET AL.-TETRABOTHRIUS MICROTRICHES 477 ticular regions of the scolex and strobila (Table I). All specific and bacteriaon the surfacebut otherwisenot apparentlyaltered regions of the scolex and strobila were covered by only a single due to fixation or processing(Figs. 25, 26, 29, 30). morphotype of microthrix. In contrast, microtricheswere not observed on the of the or strobila of T. tegument scolex, neck, DISCUSSION (Tetrabothrius)sp. (Figs. 23-26) and T. cylindraceus(Figs. 27- 30). Detailed studies of the structureof the scolex among species Among species of Tetrabothrius,the scolex of T. affinis is of Tetrabothriushave included those by Spiitlich(1909), Baer comparativelymassive (Fig. 1), with largesucker-like bothridia (1954), Rees (1956), and Andersenand Lysfjord(1982). Meristic but with reduced auricles and apical organ. The central to pe- and gross morphologicalaspects of the holdfasts among those ripheral regions of the apical organ (Fig. 2) are covered with species examined in the current study have been documented minuscule papilliformto filiform structures(n = 10) 0.14-0.20 previously(Baer, 1954; Temirova and Skriabin,1978) and agreed (0.17) in diameter. The adherentsurfaces of the bothridia have with observations from the currentstudy. However, structural a dense uniformlydistributed covering of spiniformmicrotrich- characteristicsevident at high magnificationwith SEMhave not es, of consistent structureand dimensions (n = 10), 0.46-0.54 been considered. (0.51) long (Fig. 3). The tegument on the margins and outer In agreementwith other tetraphyllideans,including trypano- surfaces of the bothridia (Figs. 4, 5, respectively) is densely rhynchs,that have been examined with SEM,intraspecific vari- covered with relatively long spiniform microtriches(n = 10), ation was not apparent,but interspecificvariation was notable 1.20-1.63 (1.46) in lengthand 0.22-0.28 (0.24) in width. Similar (Caira, 1990, 1992; Cairaand Ruhnke, 1990, 1991; Richmond spiniform microtricheswere found on the neck and strobila. and Caira, 1991; Ruhnke, 1993, 1994). These authors have Specimens of T. laccocephalushave a relativelyrobust scolex suggested that the scope of intraspecificvariation, if present, (Fig. 6), characterizedby flat bothridia with muscularmargins may be fully documentedin small samples of specimens. How- and well developed auriclesand apical organ.The apical organ, ever, the results of the currentstudy, particularlywith respect distal marginsof the auricles,and adherentsurfaces of the both- to observations of T. cylindraceusand T. (Tetrabothrius)sp., ridia are densely covered with spiniformmicrotriches (n = 10), indicate that this conclusion should be regardedwith caution. 0.88-1.40 (1.06) long (Fig. 7). Densely and uniformlydistributed Spiniform microtricheswere the most commonly occurring long spiniformmicrotriches extend to the lateralmuscular mar- type (Table I). This morphotypeappeared relatively similar in gin of each bothridium (n = 5) 1.16-1.24 (1.20) (Fig. 8). The structureamong taxa, although interspecificdifferences in size tegument of the neck region (Fig. 9) is similar in structureto and density were apparent. In specimens of T. laccocephalus, that observed on the scolex being covered with spiniform mi- spiniform structuresoccurred on the apical organ(apically and crotriches (n = 5) 0.57-0.75 (0.70) long. Microtricheson the on the auricles), adherent surfaces, and lateral margins of the strobila are short and papilliform toward the middle of each bothridia, the neck, and the posteriormargins of the segments. segment (not depicted in figure),becoming spiniformand elon- Among specimens of T. filiformis, similar microtriches were gate along the posterior margin,giving the posteriorborders of distributedon the adherentand proximal regions of the both- each segment a fringedappearance. ridia, distal marginsof the auricles,neck, and fringedposterior The scolex of T. filiformis has flattened, muscularbothridia borders of the segments. Narrow spiniform microtrichesin T. and well developed auriclesand apical organ(Figs. 10, 11). The affiniswere limited to the auriclesand proximal surfacesof the apex of the apical organhas densely packedpapilliform to short bothridia.Blade-like spiniform microtriches were relativelyrare, filiformmicrotriches (n = 10) 0.17-0.23 (0.20) in diameter(Fig. being present only on the adherentsurfaces of the bothridiain 12 at center; Fig. 13 on lateral field) that become reduced in T. affinisand T.filiformis. Papilliform structures were observed number laterallyand somewhat elongate and filiform, measur- apicallyin T. affinisand T.filiformis and as prominentcushion- ing (n = 5) 0.65-0.78 (0.71) in length(Fig. 14 on lateralmargins). like microtriches on the surfaces of the segments in T. lacco- Laterally,between the bothridia (Fig. 15), the filiform micro- cephalusand T. filiformis. Filiform microtricheswere confined triches are evenly but not densely distributed. The adherent to the apical region of T. filiformis and T. affinis. surfaces of the bothridia (Fig. 16) have short, blade-like, spi- The absence of microtricheson specimens of T. (Tetraboth- niform microtriches(n = 10), 0.70-1.05 (0.86) in length, pos- rius) sp. and T. cylindraceusis anomalous. Specimens of these sibly arrangedin linear rows. The externalsurfaces of the both- were recoveredwhile alive and were fixed and stored in a com- ridia (Fig. 17) have a dense covering of slender spiniform mi- parablemanner to the other species of Tetrabothriusfrom avian crotriches(n = 5), 0.78-0.99 (0.87) in length.The distal margins hosts. The tegumentofthese specimenswas intactand otherwise of the auricles (Fig. 18) have a dense covering of spiniform did not appearto have been alteredby fixationor storage.Spec- microtriches measuring (n = 5) (1.07-1.19) (1.14) long. The imens of both species were gravid, and acquisitionby the host, craspedotestrobila (Fig. 19) has a highly defineddistribution of a 25-day-old chick of Rissa tridactyla,would have been rela- microtrichesof 2 distinct morphotypes(Fig. 20). Those on the tively recent. Thus, it is possible that development of the teg- mid-surfaceregion are pad-like and papilliform, measuring(n umental microtricheswas incomplete or was undergoingrapid - 10) 0.21-0.33 (0.27) in diameter(Fig. 21); elongatespiniform turnover in these young cestodes. In this regard, Caira and microtrichesmeasuring (n = 15) 1.15-1.94 (1.37) extend pos- Ruhnke (1991) noted substantial changes in the pattern and teriad along the posterior margin of each segment (Fig. 22). distribution of microtriches during ontogeny of the scolex in Microtricheswere not observed on the scolex and strobilaof Calliobothriumverticillatum (Rudolphi, 1819). T. (Tetrabothrius)sp. (Figs. 23-26) and T. cylindraceus(Figs. In contrast, specimens of T. fihformis and T. laccocephalus 27-30). The tegument appearedintact with particles of debris were also collected from recentlyinfected hosts (Hoberg, 1987) 478 THE JOURNALOF PARASITOLOGY,VOL. 81, NO. 3, JUNE 1995

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FIGURES 23-26. Tetrabothrius(Tetrabothrius) sp. (scalebars = 50 Amfor Figs. 23 and 24; 1.0 Amfor Figs. 25 and 26). 23. Scolexin dorsoventral view showing positions for Figures25 and 26 indicatedby arrows.24. Scolex in apical view showingwell developed apical organ.25. Marginof bothridiumshowing tegumentlacking microtriches.26. Adherentsurface of bothridiumshowing tegumentlacking microtriches. and microtriches were fully developed. Consequently, the ab- for T. (Oriana) spp. Microtriches occurring on the scolex also sence of microtriches on specimens of T. cylindraceus and T. were not apparently correlated with host group. Tetrabothrius (Tetrabothrius) sp. cannot be readily explained and may suggest affinis is a characteristic cestode of cetaceans, whereas T. fili- that intraspecific variation could influence observations in some formis and T. laccocephalus occur among Procellariiformes and circumstances. Additional freshly collected material from an- T. (Tetrabothrius) sp. and T. cylindraceus occur in Charadri- other source will be necessary to determine whether or not the iformes. A broader representation of Tetrabothrius spp. is re- observations are an artifact of fixation and preparation. quired to evaluate fully the hypotheses that patterns and forms The systematic value of patterns of distribution and config- of microtriches may be influenced by intraspecific variation, uration of the microtriches among species of Tetrabothrius is and that specific types and distribution of microtriches may currently unrevealing. The speciose genus Tetrabothrius has been provide resolution of systematics at the subgeneric level. partitioned into 4 subgenera (Murav'eva, 1975; Temirova and A tetraphyllidean ancestry for the tetrabothriids (Baer, 1954; Skriabin, 1978), but a phylogenetic basis for recognition of these Euzet, 1959) or inclusion of the family within the Tetraphyllidea groups has yet to be established (Hoberg, 1989, 1994). The has been postulated (Hoberg, 1987, 1989; Brooks et al., 1991). structure and distribution of microtriches among T. (Oriana) Some derived onchobothriids have been considered the prob- affinis, T. (Oriana) filiformis, and T. (Culmenamniculus) lac- able sister-group based on postlarval ontogeny and some struc- cocephalus are highly variable and no patterns were recognized tural characteristics of the strobilar stages (Hoberg, 1987). Caira among these species that could contribute to differentiation at (1990) and Caira and Ruhnke (1990, 1991) suggested that mi- the subgeneric level. However, additional study is necessary to crothrix structure was a significant systematic character among establish whether blade-like spiniform microtriches on the ad- the Onchobothriidae. Based on unique patterns of distribution herent surfaces of the bothridia and filiform structures confined (on the holdfast), they postulated monophyly for some inclusive to the apex of the apical region may represent characters unique groups of genera. Among 17 genera of the onchobothriids, great

FIGURES10-22. Tetrabothriusfiliformis (scale bars = 50 Amfor Figs. 10, 11, and 19; 1.0 Amfor other figures).10. Scolex showing general structurein dorsoventralview, with well developed auricles (open arrow)and apical organ (centerindicated by oointer), and positions of high magnificationviews for Figures12-14, 16, and 18 indicatedby arrows.11. Scolexin lateralview showingpositions tbr Figures15 and 17 indicated by arrows.12. Papilliformto short filiformmicrotriches at centerof apical organ.13. Short filiformmicrotriches in the field lateralto the central region of the apical organ. 14. Elongatefiliform microtricheson lateral marginsof the apical organ. 15. Filiform microtrichessituated between the bothridia. 16. Spiniformmicrotriches on the adherentsurfaces of the bothridia.17. Slenderspiniform microtriches on the externalsurfaces of the bothridia. 18. Spiniformmicrotriches on the distal marginsof the auricles. 19. Highly craspedotestrobila showing position of Figure 20 indicated by arrow. 20. Posteriormargin of segment showing overall distributionsof papilliformand spiniform microtrichesand positions of Figures 21 and 22 indicated by arrows. 21. Detail of cushion-likepapilliform microtriches in the medial region of the segment. 22. Detail of spiniformmicrotriches along posteriormargin of segment. 480 THE JOURNALOF PARASITOLOGY,VOL. 81, NO. 3, JUNE 1995

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FIGURES27-30. Tetrabothrius(Culmenamniculus) cylindraceus (scale bars = 50 gm for Figs. 27 and 28; 1.0 4m for Figs. 29 and 30). 27. Scolex in dorsoventralview showingpositions for Figures29 and 30 indicatedby arrows.28. Scolex in apical view showingwell developedapical organ. 29. Adherentsurface of bothridiumshowing tegument lacking microtriches. 30. Neck showing tegumentlacking microtriches. intraspecific uniformity was accompanied by substantial inter- of the scolex (or segment) and 2 or more forms never occurred specific differences in structure and distribution of the micro- in the same region. Filiform to papilliform structures were found triches (Caira, 1990, 1992). Similarly, these general patterns apically on scolices of T. affinis and T. fifhformis and appeared were found among the species of Tetrabothrius examined by us. similar to those described for Calliobothrium spp. (Caira and Spiniform, filiform, and papilliform types of microtriches are Ruhnke, 1990, 1991) and Phyllobothrium spp. (Whittaker et al., represented among the tetrabothriids, onchobothriids, and phyl- 1985). Blade-like spiniform microtriches occurring on the ad- lobothriids (Caira and Ruhnke, 1990; Ruhnke, 1994). Among herent surface of the bothridia in T. affinis and T. fJiliformismay those onchobothriids that have been examined, all regions of be similar to those known for Calliobothrium pritchardae Caira the scolex were covered with at least 1 form of microthrix (Caira, and Ruhnke, 1990 (Caira and Ruhnke, 1990). The widespread 1990). In contrast, among the tetrabothriids considered here, occurrence of these basic morphotypes may constitute the ple- typically a specific morphotype was restricted to a limited region siomorphic condition for these groups of cestodes, although distributional patterns on the tegument may have systematic TABLE I. Distribution and form of microtrichesamong some species value (Caira, 1990). Absence of microtriches has not been ob- of Tetrabothrius. served among the onchobothriids but was reported for the apical region of some lecaniacephalids (Nock and Caira, 1988; Caira, T. T. 1990). (Culmen- (Culmen- Microtriches have been widely reported among all major or- T. T. amni- amni- ders of Eucestoda. These are present on the scolices and strobila T. (Tetra- (Oriana) culus) culus) of representatives of most groups that have been examined with (Oriana) fli- lacco- cylindra- bothrius) SEM. Papilliform, spiniform, and filiform structures have been Region sp. formis cephalus ceus affinis variously reported among the Pseudophyllidea (Andersen, 1975; Scolex, bothridia Granath et al., 1983; Yazaki et al., 1990), Cyclophyllidea (Berger Apical Absent P*, Ft P, F St Absent and Mettrick, 1971; Ubelaker et al., 1973), and the Proteoce- Adherent Absent S S S Absent phalidea (Thompson et al., 1980). The palmate form, apparently Proximal Absent S S S Absent unique to the trypanorhynchs (Whittaker et al., 1985; Richmond Auricles Absent S S S Absent and Caira, 1991; Shields, 1985), and the "corn cob" type found Strobila in Orygmatobothrium musteli (Van Beneden, 1850) (Whittaker Neck Absent S - S Absent and Carvajal, 1980), and 2 species of Paraorygmatobothrium Segment Absent S P, S P, S - Ruhnke, 1994 may constitute apomorphic characters (Caira, Richmond and * = 1990; Caira, 1991; Ruhnke, 1994). Additionally, P papilliform. serrated microtriches were as the t F = filiform. apparently unique recognized t S = spiniform. basis for establishing the latter genus (Ruhnke, 1994). HOBERGET AL.-TETRABOTHRIUS MICROTRICHES 481

Variation in microthrix structure and distribution has been des c6tes de France. Theses Universit6 de Montpellier.Caussee, Graille applied to the systematics of tetraphyllideans, where it is ap- et Castelneau,Montpellier, France, 263 p. W. J. C. AND G. W. that some be restricted to GRANATH, O. JR., LEWIS, ESCH. 1983. An ultra- parent morphotypes may particular structuralexamination of the scolex and tegument of Bothrioce- taxonomic groups (Ruhnke, 1994). However, the broad distri- phalus acheilognathi(: Pseudophyllidea). Transactions of bution of a variety of morphotypes among disparate orders the American MicroscopicalSociety 102: 240-250. including the Pseudophyllidea, Cyclophyllidea, and Tetraphyl- HOBERO,E. P. 1987. Recognition of larvae of the Tetrabothriidae for the of in marine lidea, in conjunction with recent phylogenetic hypotheses for (Eucestoda):Implications origin tapeworms homeotherms.Canadian Journal of Zoology 65: 997-1000. the Eucestoda (Brooks et al., 1991), suggests that the basic spi- . 1989. Phylogeneticrelationships among generaof the Tetra- niform, filiform, and papilliform microtriches are symplesio- bothriidae(Eucestoda). Journal of Parasitology75: 617-626. morphic among cestodes. . 1994. Keys to the generaand subgeneraof the family Tetra- bothriidae.In CIP keys to the cestode parasitesof vertebrates,L. ACKNOWLEDGMENTS F. Khalil,A. Jones, and R. Bray(eds.). Commonwealth Agricultural Bureaux,International Institute of Parasitology,St. Albans, U.K., 295-304. We thank David O'Neil and Margaret Home for their skillful p. J. R. W. ANDJ. P. GRAY. 1989. Use of Peldri of the SEM and for the of KENNEDY, R., WnLIAMs, operation preparation publication II (a fluorocarbon solid at room temperature) as an alternative to micrographs. Specimens of T. affinis were kindly provided by critical point dryingfor biological tissues. Journalof ElectronMi- Leo Margolis of the Pacific Biological Station, Nanaimo, British croscopyTechnique 11: 117-125. Columbia. Material from greater shearwaters was provided by MURAV'EVA, S. I. 1975. Morfologo-anatomicheskieosnovy sistematiki tetrabotriid. 2: 49. Peter Ryan of the Percy FitzPatrick Institute for African Or- ProblemyParazitologii NOCK,A. M., ANDJ. N. CAIRA.1988. Disculicepsgalapagoensis n. sp. nithology, University of Cape Town. Field studies at Talan (Lecaniacephalidea:Disculicepitidae) from the shark,Carcharhinus Island, USSR (by E.P.H.) were conducted under the Interacade- longimanuswith comments on D. pileatus.Journal of Parasitology my Exchange Program of the National Academy of Sciences; 74: 153-158. G. 1956. The scolex of Tetrabothrius a cestode logistical support in Russia was provided by Alexander Ia. Kon- REES, affinis(L6nnberg) from Balaenopteramusculus L., the blue whale. Parasitology46: dratiev and the Institute of Biological Problems of the North, 425-442. Russia of Magadan, (Russian Academy Sciences). RICHMOND, C., ANDJ. N. CAIRA. 1991. Morphological investigations into Floriceps minacanthus (Trypanorhynca:Lacistorhynchidae) LITERATURECITED with analysis of the systematic utility of scolex microtriches.Sys- tematic Parasitology19: 25-32. ANDERSEN,K. 1975. Comparisonof the surfacetopography of three RUHNKE,T. R. 1993. 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