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The Synlophe and Other Structural Characteristics of Sarwaria bubalis (Nematoda: ) from Cattle in Guyana

J. Ralph Lichtenfels Parasitic Disease Lab, ARS, United States Department of Agriculture, [email protected]

Eric P. Hoberg United States Department of Agriculture, [email protected]

Patricia A. Pilitt Animal Parasitic Disease Lab, ARS, United States Department of Agriculture, [email protected]

T. M. Craig Texas A&M Universit

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Lichtenfels, J. Ralph; Hoberg, Eric P.; Pilitt, Patricia A.; and Craig, T. M., "The Synlophe and Other Structural Characteristics of Sarwaria bubalis (Nematoda: Trichostrongyloidea) from Cattle in Guyana" (1996). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 636. https://digitalcommons.unl.edu/parasitologyfacpubs/636

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THE SYNLOPHEAND OTHERSTRUCTURAL CHARACTERISTICS OF SARWARIABUBALIS (NEMATODA: TRICHOSTRONGYLOIDEA) FROMCATTLE IN GUYANA

J. R. Lichtenfels, E. P. Hoberg, P. A. Pilitt,and T. M. Craig* USDA,Agricultural Research Service, Livestock and PoultrySciences Institute, Beltsville,Maryland 20705-2350

ABSTRACT:The synlophe(longitudinal, surface cuticular ridges) of Sarwariabubalis is describedfor the firsttime. It is a tapering lateral synlophe of about 40 ridges. The synlophe of S. bubalisis similar to that of Ostertagiaostertagi but markedlydifferent from that of speciesof Spiculopteragiaand Mazamastrongylus.New informationis providedalso on the structureof the esophagus and perivulvalpores. The esophagealvalve is more than twice as long as wide. The bilateralperivulval pores were located 192- 267 Am posteriorto the vulva and dorsal to the laterallines. The new informationwill be useful in a study of the genericlevel systematicsof the Ostertagiinae.Sarwaria bubalis appears to be well establishedin tropicalSouth Americawhere it infects its normal host, the Asian water buffaloBubalus bubalis, as well as domestic cattle Bos taurusand mixed breed cattle B. taurus x Bos indicus.

Nematodes of the subfamily Ostertagiinae were collected in of both B. taurusand B. indicusancestry, ranging in age from 1 to more than 6 of S. bubalis from the B. 1974 from 16 of 21 cattle of mixed breeding (Bos taurus L. x yr. Additional specimens type host, bubaliswere obtained from Dr. Jan Bos indicus in of this sub- Dr6zdz (Dr6&dz,1965). L.) Georgetown, Guyana. Specimens were studied as: (1) temporarywhole mounts cleared in family are generally recognized as the most economically im- phenol-alcohol (80 parts melted phenol crystalsand 20 parts absolute portant gastrointestinal parasites of cattle. However, they are ethanol) and examined with regularlight microscopyor interference- not encountered often in tropical areas and the literature con- contrast microscopy at a magnificationof 400-1,600; and (2) cross sections in free-handcuts made with a cataractknife and mounted in cerning the presence of Ostertagiinae in these areas is sparse. It glycerinejelly. was determined that the nematodes differed from Male specimens were identifiedto species on the basis of the mor- ostertagi, the species commonly encountered in cattle. The nem- phology of the copulatorybursa, spicules, and genital cone (Sarwar, atodes were subsequently identified as Sarwaria bubalis (Sarwar, 1956; Dr6&dz,1965) prior to study of the synlophe and esophagus. 1965. Bursalray patternswere determinedand describedusing the system of 1956) Dr6zdz, Durette-Dessetand of the cone and Sarwariabubalis is a of the water Chabaud(1981). Papillae genital primarily parasite buffalo, rays of the copulatorybursa followed the numberingsystem of Chabaud Bubalus bubalis (L.). It was described from that host in Pakistan et al. (1970). The lengths of the esophageal-intestinal(E-I) valves, de- as Gruhneria bubalis Sarwar, 1956. Dr62d2 (1965) reported this terminedto extend from the posteriorend of the cuticularlining of the in B. bubalis in Vietnam and created a new genus, triradiatelumen of the esophagusto the posteriorend of the esophagus were measured(Tables I, Femalenematodes were identified Sarwaria, for it. Sarwaria bubalis was reported from its type (Fig. 7), II). on the basis of the morphologyof the synlophe, ovejectors, and tail host B. bubalis in in Venezuela 1986 (de Moreno, 1986). Hin- length(Lichtenfels and Pilitt, 1991; Table II). For measurementsof the aidy and Prosl (1981) proposed that Skrjabinagia boevi Pande infundibulaand sphinctersof the ovejectors(Table II), the edge of the and Chauhan, 1969, also described from B. bubalis, is a syn- muscularportion of the sphincterwas used as a dividing line between and the coat around the and the of the onym of S. bubalis. Durette-Desset (1983, 1989) and Jansen them, fluffy sphincter portion overlapped the musclesof the wereignored considered both Sarwaria and to be infundibulum by sphincters (1986) Skrjabinagia syn- (Fig. 9). Becausethe separationof the vestibule from the sphincterwas onyms of Spiculopteragia. However, we prefer to follow Dr602d difficultor impossible to determine,the vestibule was counted as part (1965) and Gibbons and Khalil (1982) in recognizing Sarwaria of the sphincter.The measurementfor length of the sphincterincludes for S. bubalis until a phylogenetic analysis of the Ostertagiinae the distance from the distal end of the sphincterto the vulva. Mea- surementsare in micrometersunless indicatedotherwise. is completed. As part of a study of the systematics of the Ostertagiinae in progress in this laboratory, the synlophe, perivulval pores, and RESULTS characteristics of the esophagus of S. bubalis are described for General the first time. Other morphological characteristics adequately characters described by Sarwar (1956) or Dr60d` (1965) for S. bubalis or Nematodes of the species S. bubalis were found in 16 of the by Pande and Chauhan (1969) for S. boevi are described only 21 abomasa examined. A mean of 151 adult worms was found briefly. in each infected abomasum. The synlophe of S. bubalis consists at the anterior end in the MATERIALSAND METHODS region of the esophagus of 24-44 longitudinal ridges (Figs. 1, 2) Abomasafrom 21 cattlekilled at the Georgetown,Guyana, municipal with the smaller number anteriorly. The pattern observed is the abattoirwere collectedin 1974 and washed;2 1:20 aliquotsof contents tapering lateral synlophe or type I (Lichtenfels et al., 1988). The were takenand fixedin 10%formalin. The cattlewere of mixed breeding synlophe is divided into 8 fields by continuous ventral, dorsal, 2 lateral, 2 subventral, and 2 subdorsal ridges (dotted in Figs. 1, 2). The tapering lateral synlophe is so named because ridges 22 28 Received May 1995; revised 28 August 1995; accepted August in the lateral fields are and end ad- 1995. angled posteriorly toward, * TexasA&M University, Department of VeterinaryPathobiology, Col- jacent to, the slightly thinner lateral ridge, which runs just ven- lege Station, Texas 77843-4467. tral to the anterior deirid or cervical papilla. The tapering pattern 146 1 2 TABLEI. Morphometricsof Sarwariabubalis males.*

Measure- S. boevi ment of Pande and Sarwar Chauhan Character Present I Ii study (1956) (1969) Number examined 14 Body length (mm)t 5.75-7.36 (6.51) 6.5-7.0 7.0-9.0 Width at E-I junction 58-91(75) Nerve ringt 233-291 (274) 220-230 Subventralesophageal gland orificest 186-279 (238) 230-240 Excretoryporet 279-342 (311) 260-321 Cervicalpapillaet 303-373 (339) 290-336 ep i Esophaguslengtht 640-753 (684) 475-650 596-765 Esophagealvalve length 96-112 (103) I I I i cp IIi Esophagealvalve width 27.9-58.3 (44.8) I I I Esophagusas percentage of body length 8.78-11.8 7.3-9.3? 8.511 I I Spicule length 147-163 (157) 150-175 156-180 I I I Percentageof body with II I II i taperinglateral syn- lophe 30.8-63.0 (48.7)t 1 I l I Distance of end of lateral I I I IiI IiI synlophe from prebursal IiI 23-70 I I I papillae (56) Distance of end of ventral 1 1 synlophe from prebursal papillae 326-478 (402) Dorsal Ii I ray length 34.9-46.6 (39.9) 40-50 * Measurements(in micrometersunless noted otherwise) are ranges followed by meansin parentheses. t Measurementsfrom anterior end. t n= 13. I I ? Calculatedfrom data of Sarwar(1956). IICalculated from data of Pandeand Chauhan (1969).

I I was repeated over the anterior 30-63% of the body, after which V L I the ridges were parallel to each other until they ended near the bursa in the male (Table I) and anterior to the anus in the female (Table II). Although the subdorsals, subventrals, ventral, dorsal, and lateral ridges are usually continuous, occasionally 1 of these I I I ridges ends and is replaced by an adjacent ridge (Fig. 2). S LI L Most specimens had 3 parallel ventral ridges (Fig. 2) and 3 parallel dorsal ridges, but in 3 of the 25 specimens available for study, 1 or 2 of the more lateral of the 3 ventral or dorsal ridges was short or was interrupted. The number of ridges was rather constant through the anterior S3/4ofthe body (Figs. 1-5). No differences were observed in the synlophes of males and females in the anterior 3/4of the body. In 1 female studied in cross sections, there were 40 ridges at the level of middle esophagus, 40 at the E-I junction, 40 at midbody, and 46 just anterior to the vulva. In a male (Figs. 3-5), there were 42 at the E-I, 41 at the end of the first 1/4of the body, 40

4--- FIGURES 1, 2. Diagrammaticdrawings of the synlophe of Sarwaria bubalis from the anterior end to the posterior end of the esophagus (dashed lines, sublateral[S], subdorsal [S], lateral [L], or ventral [V] ridges;dotted line indicates a subventralridge involved in a crossover at the level of the excretorypore with an adjacentdashed line ridge;ep, excretory pore; cp, cervical papilla). (scale bar = 100 Am). 1. Lateral view of a male specimen. 2. Ventralview of a male specimen. 148 THEJOURNAL OF PARASITOLOGY, VOL. 82, NO. 1, FEBRUARY1996

at midbody, and 40 at the beginningof the last quarterof the body. Two characteristicsof the esophagusare describedfor the first time. The E-I valve was found to be more than twice as long as wide (Fig. 7; Tables I, II). The subventralesophageal gland orificeswere anteriorto the excretorypore and slightlyposterior to the nerve ring (Tables I, II). The length of the esophagusas a percentageof total body length was 7.7-9.1% in females and

.k 5i` 8.8-11.8% in males. 61F)i Malecharacters We confirmedthe absence of a gubernaculum,but the dorsal wall of the cloaca is thickenedin the areawhere a gubernaculum would be located. The pairedspicules are mirrorimages of each other and, as in all members of the Ostertagiinae,end in the distal third with 3 branches.The main spicularshaft continues as the longest branchthat ends distally in a mediallycurved tip encased in a fleshy pad. The 2 medially directed alae of the central shaft end in nearly equal branchesof which the ventral is a thin sharptip and the dorsalis a thickened,blunt, spadelike tip (Figs. 16-20). The ventral branch ends in an acute point, with the shaft curved stronglymedially; the thin tip is bordered by a crenulatedmembrane supported by prominenttrabeculae. Although the thin tip of the ventral branchcurves dorsomedi- ally, in ventral view (Fig. 19) it may appearto be straight.The dorsal branch is wide, highly cuticularized,with a prominent transversebar dorsally, a ventrally curved apex, and a mem- branouscrenulated margin distal to the sclerotizedtip (Figs. 18, 20). lateralbursal lobes are ef.1 The rays of the bilaterallysymmetrical •X. g}; in a 2-2-1 patternwith the anterolateralray (no. 4) of each lobe ending bluntly short of the edge of the bursa(Figs. 13-15). The posterolateralrays (no. 6) are the longest rays of the bursa.The externodorsalrays (no. 8) are only half as long as the postero- laterals.The dorsal ray is very short (Table I) and is bifurcated for more than half its length, each branchending in a trifurcate tip. The genital cone lacks a proconus. The ventral part of the genital cone bears paired, slender, curved papillae (no. 0) en- closed, except for the distal tips within a bubble-likemembrane (Figs. 15, 21, 22). The dorsalpart of the genitalcone bearspaired finger-likepapillae (no. 7) enclosed, except for the distal tips, within the accessory bursal membrane (Figs. 15, 21, 23). In lateral view, the dorsal ray can be seen curved ventrallyjust dorsal to the accessory bursal membrane(Figs. 14, 21). A tel- amon, or sclerotizedinternal support for the ventralpart of the genital cone, is just anterior to the paired "O" papillae (Figs. 14, 15). There is also a bowl-shaped,internal, sclerotizedsup- port for the dorsal part of the genital cone just anterior to the accessory bursal membrane and the no. 7 papillae (Fig. 23).

Female characters The vulva is located at 80-87% of body length from the an- terior end. The vulva is a transverse opening without lobes,

FIGouREs3-5. Cross sections of a male Sarwariabubalis (arrows at lateralridges) (scale bar = 20 Lm).3. Throughposterior esophagus showing42 ridges.4. At one-fourthof bodylength from anterior end showing41 ridges.5. At midbodyshowing 40 ridges. LICHTENFELSETAL.-MORPHOLOGY OF S. BUBALIS 149

TABLEII. Morphometricsof Sarwariabubalis females.*

Measurementof S. boevi Character Presentstudy Sarwar(1956) Pandeand Chauhan (1969) Numberexamined 11 Bodylength (mm)t 7.17-9.40(8.44) 8.0-9.0 9.0-11.0 Widthat E-Ijunction 72-98 (83) Nerveringt 224-314(266) 250-280 Subventralesophageal gland orificest 189-291(240) 300-340 280-310 Excretoryporet 254-356(314) 316-342 Cervicalpapillaet 273-410(345) 340-380 Esophaguslengtht 648-746(692) 650-700 642-765 Esophagealvalve length 93-124(110) Esophagealvalve width 41.9-58.3(49.6) Esophagusas percentageof bodylength 7.71-9.06(8.25) 7.8-8.1 7.0-7.1? Vulvaposition (percentage) 80.3-87.0(85.1) 83.4-84.1? Anteriorinfundibulum length 131-196(164) Anteriorsphincter length 100-119(110) Vaginalength 30-60 (45) 34-48 Posteriorsphincter length 86-131(108) Posteriorinfundibulum length 121-168(147) Combinedovejector length 477-594(524) 57511 500? Egglength x width 72-87 (78) x 36-46 (30)$ 85-95 x 45-50 78-91 x 37-48 Numberof eggsin anterioruterus 6-15 (10) Numberof eggsin posterioruterus 6-16 (9) Taillength 84-114(101) 122-149 Percentageof bodywith a taperinglateral syn- lophe 30-61 (41) Distanceof end of lateralsynlophe from tail tip 108-384(232) * Measurements(in micrometersunless noted otherwise)are rangesfollowed by means in parentheses. t Measurementfrom anteriorend. tn = 7. ? Calculatedfrom data of Pande and Chauhan(1969). IICalculated from drawingin Sarwar(1956). flaps, knobs, or other ornamentations.The vagina is short with (Lichtenfelset al., 1995). The new informationmakes it possible a thick cuticular lining (Fig. 9). The vestibule is short, deeper to compare S. bubalis with other Ostertagiinaewith a tapering than long. Because the boundariesof the vestibule are difficult lateralsynlophe (Lichtenfelsand Pilitt, 1991; Lichtenfelset al., to distinguishfrom the adjacentsphincters, it was not measured 1993; Lichtenfelsand Hoberg, 1993). This new informationis separately.The sphinctersare thick-walledand lined with thick also required for a phylogenetic analysis of the Ostertagiinae, cuticle. Each sphincter consists of an oval, wider than long, an essential study for determiningthe genericlevel systematics bulblike valve next to the infundibulum and a longer barrel- of this subfamily. shaped extension that connects with the short vestibule (Fig. 9). The synlophe of S. bubalisis very similar in the region of the The infundibula were less than half as thick and 50% longer esophagus to the tapering lateral synlophe described earlier than the sphincters. The anterior sphincterand infundibulum (Lichtenfelset al., 1988) for Ostertagiaostertagi and Telador- were slightly longerthan their posteriorcounterparts (Table II). sagia circumcincta(Stadelmann, 1894), and for Ostertagiabi- Eggswere usuallypresent in both anteriorand posterioruteri. sonis Chapin, 1925 by Lichtenfelsand Pilitt (1991). The afore- Uterine eggs were oval-shaped and usually in the 32-64-cell mentioned speciesall have continuoussubventral and subdorsal stage of development (Fig. 11). ridges that, with the lateral ridges and the dorsal and ventral Perivulvalpores (Lichtenfelset al., 1995) (Fig. 10) were pres- ridges,divide the synlopheinto 8 fields of mostly shorterridges. ent bilaterallyin the females. The pores were located 192-267 The synlophe of S. bubalisdiffers significantly,however, from gm posteriorto the vulva, slightlydorsal to the lateralridge, at the tapering lateral synlophe of Mazamastrongylusspp. de- or near the level of the posterior infundibulum. scribed by Lichtenfelset al. (1993), which lacks the continuous The tail was found to be short, conical, and usually with a subdorsaland subventralridges. In Mazamastrongylusspp., the roundeddigitiform tip (Fig. 12). The posteriorend of the females synlophe is divided into only 4 fields by the 2 lateral and the had a marked ventral curvature(Fig. 12). dorsal and ventral ridges (Lichtenfelset al., 1993). A pattern similar to that of Mazamastrongylusspp. has been observed in several of P. DISCUSSION species Spiculopteragia(E. Hoberg,unpubl. obs.). Most Ostertagiinaewith a tapering lateral synlophe have the New information on S. bubalispresented herein includes the patternseen in S. bubalis,0. ostertagi,0. bisonis, description of the synlophe, esophagus, and perivulval pores circumcincta,and others. The pattern described for Mazama- 150 THEJOURNAL OF PARASITOLOGY, VOL. 82, NO. 1, FEBRUARY1996

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FIGuREs13-18. Camera lucida drawingsof male characteristicsof Sarwaria bubalis. 13. Posteriorend, ventral view of copulatorybursa, genital cone, and spicules. 14. Lateralview of bursaand genitalcone. 15. Genitalcone and dorsal-ray,ventral view. 16. Left spicule,ventral view. 17. Distal half of left spicule, lateralview. 18. Distal half of right spicule, dorsal view.

strongylus and reported for Spiculopteragia has been seen only binagia a synonym of Spiculopteragia. However, we disagree in members of these 2 genera and in all members of these genera with Durette-Desset (1983, 1989) and Jansen (1986) who con- that have been examined by us. sidered Sarwaria a synonym of Spiculopteragia. We decided to A discussion of the generic level systematics of the Osterta- follow Dr6zdi (1965) and Gibbons and Khalil (1982) in rec- giinae is needed but is beyond the scope of this paper. It was ognizing Sarwaria as a separate genus for this species, We based necessary, however, to decide which genus should be used for this decision on the marked differences between the synlophe the species redescribed here. As we explained earlier, S. bubalis and spicules of S. bubalis and those of Mazamastrongylus spp. has been placed in various genera, including Gruhneria, Sar- and Spiculopteragia spp. Characteristics such as the extremely waria,Skrjabinagia, and Spiculopteragia.We agreewith Dr6zdi short dorsal ray and short, thick bursal ray no. 4 distinguish (1965) and others in considering Gruhneria a synonym of Os- Sarwaria from Teledorsagia and Ostertagia. We believe a phy- tertagia and with Durette-Desset (1983) in considering Skrja- logenetic analysis is required to determine a suitable generic

4-- FIGUREs6-12. Photomicrographsof generaland female characteristicsof Sarwariabubalis. All scale bars 50 ,m. 6. Anteriorend, lateralview, of female showing short buccal capsule and dorsal esophagealtooth. 7. Esophagealvalve, lateralview, of male. 8. Lateralridges of synlophe in region of anteriordeirid (=cervical papilla). Lateralridge ventral (right)to deirid. 9. Vulva and ovejectors,lateral view. Arrowsindicate distal ends of infundibula.10. Perivulvalpore on left side of female.Note spacingof ridgesof synlophewith lateralridges closer than dorsal,and ventral ridges. Arrow at lateralridge points to more dorsal perivulvalpore. 11. Eggsin uterus. 12. Ventrallycurved tail, and posteriorbody of female. Arrow at anus. 152 THEJOURNAL OF PARASITOLOGY, VOL. 82, NO. 1, FEBRUARY1996

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19-23. of male characteristicsof Sarwariabubalis. All scale bars 50 Mm.19. ventral FIGuR•s Photomicrographs Spiculesshowing spinelike branchof each spicule, ventral view. 20. Spicules showingtriangular thickened tips of dorsalbranch of each spiculein ventralview. 21. Genital cone, left lateralview showing tips of I of paired "O" papillae(left arrow),tip of 1 of pairedno. 7 papillae(middle arrow),and the left branch of the dorsal ray with 3 digitate tips (rightarrow). 22. Genital cone, ventral view, showing tiny paired "O" papillaewithin membrane(arrow). 23. Genital cone, ventralview, showing pairedno. 7 papillaewithin accessorybursal membrane (arrows). LICHTENFELSETAL.-MORPHOLOGY OF S. BUBALIS 153 level for the Ostertagiinae.Until this is completed, however, that S. bubalishas apparentlynot been reportedin B. however, the differencesobserved between the synlopheS. bub- indicus in Asia where both B. bubalis and B. indicus are com- alis and those of Mazamastrongylusand Spiculopteragiarequire mon. In the course of this study, we examined the published retainingSarwaria. descriptionofSkrjabinagia bubalis Jiang, Guam, Yan and Zhou, The esophagealvalve of S. bubalisis more than twice as long 1988 and concluded from the descriptionthat it is also a syn- as wide. This character,among others, can be used to separate onym of S. bubalis (Sarwar, 1956). Sarwaria bubalishas been this species from both O. ostertagiand T. circumcincta.Among reportedfrom B. bubalisin the easternhemisphere in Pakistan the Ostertagiinae reported from cattle in the western hemi- (Sarwar,1956), in India (Pande and Chauhan, 1969), in China sphere, the esophagealvalve of S. bubalis is similar to that of (Jiang et al., 1988), in Australia (Bryan et al., 1976), and in O. bisonis among species, with a taperinglateral synlophe and Egypt (Michael et al., 1979). In the western hemisphere, S. also similar to several species with parallelor type II synlophes, bubalis has also been reportedfrom B. bubalisin Brazil (Costa including Marshallagia marshalli (Ransom, 1907) and O. lep- et al., 1980; Starke et al., 1983; Lima and Guimaraes, 1988), tospicularisAsadov, 1953. Other Ostertagiinaeparasitic in cer- in Venezuela(de Moreno, 1986), and now in Guyana.It is clear vids also have a long esophagealvalve (Lichtenfelsand Hoberg, that S. bubalishas been importedinto both South Americaand 1993). Ostertagiabisonis differssignificantly from S. bubalisin Australiawith its normal host, B. bubalis.Furthermore, S. bub- the former species' long dorsal ray and 2-2-1 lateralbursal ray alis has become established in both South America and Aus- patternin the male and the much longerovejector in the female tralia,infecting domestic cattle. Most infectionsreported to date (Lichtenfelsand Pilitt, 1991). have been relativelylight (<250) and it is not possible to predict The location of the perivulval pores at the level of the pos- the pathogenicityof this nematode in B. taurus,especially if the terior infundibulum and slightly dorsal to the lateral line is nematode will develop in more temperate regions. So far, S. similar to their location (Lichtenfelset al., 1995) in other Os- bubalis has been distributedin tropical to subtropicalregions tertagiinae.The function of the perivulval pores is unknown, where its normal host is distributed. but their location has been a useful species-level systematic character(Handoo and Golden, 1992) in plant parasitesof the ACKNOWLEDGMENTS family Tylenchidae.Among the Ostertagiinae,perivulval pores Jan W. Institute of Polish have been describedin ostertagiby Lichtenfelset al. (1995) Dr6idi, Steffinski Parasitology, O. of of herein for S. bubalisand have been observed (J. R. Lichtenfels, Academy Sciences, Warsaw,Poland, supplied specimens Sarwaria bubalis for ArthurAbrams technical unpubl. obs.) in Mazamastrongylusodocoilei. In all 3 species study. provided assistance. of Ostertagiinae,the perivulval pores were located in similar locations. Furthermore,the perivulval pores were also located in closely similar positions to that described for the 3 osterta- LITERATURECITED in other of gines species ,including (Lich- BRYAN,R. P., M. J. BAINBu•RIDGE,ANDJ. D. KERR. 1976. A study of tenfels et al., 1995) 3 species of Haemonchus and helminthparasites in the gastrointestinaltract of the swampbuffalo, oncophora.In Trichostrongyluscolubriformis, however, the per- Bubalusbubalis Lydekker, in the NorthernTerritory. Australian ivulval were located anterior to the vulva in a Journalof Zoology 24: 417-421. pores slightly A. F. A. AND M. C. dorsolateral to that of the other tricho- CHABAUD, G., PUYLAERT, O. BAIN, J. PETTER, position equivalent DURErTTE-DEssET.1970. Remarques sur l'homologie entre les pap- strongylids.Conclusions about the systematicvalue of perivul- illes cloacalesdes rhabdtideset les c6tesdorsales des . val pores within the Trichostrongylidaemust await their de- ComptesRendus de l'Academie des Sciences Paris 271:1771-1774. scriptionin more species. This newly describedcharacter (Lich- COSTA,A. J., L. J. PACOLA,I. G. ARANTES,J. DOHARA, AND C. L. JUSTO. tenfels et should be included in all future 1980. Desenvolvimento das helmintoses gastrintestinaisem bu- al., 1995) descriptions falos (Bubalusbubalis L.) nascidosem Sertaozintio(SP). Boletin of nematodes of the class Secernentea. de IndustriaAnimal 37: 195-205. The vulval region of all S. bubalisfemales availablefor study DE MORENO,L. G. 1986. Helmintos parasitos de bufalos Bubalus were without ornamentationsuch as lobes, flaps,or knobs.How- bubalisde los centros de recria del estado Apure, Venezuela. Revista de la Facultadde CienciasVeterinarias 33: 21-26. ever, Pande and Chauhan (1969) described a "small rounded DR62D2,J. 1965. Studieson helminthsand helminthiases in Cervidae. vulvar flap in 4.5% of Skrjabinagiaboevi, which is believed to I. Revision of the subfamily OstertagiinaeSarwar, 1956 and an be a synonym of S. bubalis. Michel et al. (1972a, 1972b) de- attempt to explain the phylogenesis of its representatives.Acta scribed considerablevariation in the development of O. oster- ParasitologicaPolonica XIII: 445-481. M. tagi and populations of a species with smooth vulvas cannot be DURETTE-DEssrET,C. 1983. Keys to generaof the superfamilyOs- In CIH to the nematode of vertebrates. considered to be indicative of the absence of vulval ornamen- tertagiinae. keys parasites No. 10, R. C. Anderson, and A. G. Chaubaud(eds.). Common- tation for the entire species. wealth AgriculturalBureaux, Farnham Royal, U.K., 86 pp. The posterior ovejector of S. bubalis was found to be slightly . 1989. Nomenclaturepropos6e pour les especes d6critesdan shorter than the anterior. This asymmetry is common in the la sous-famille des OstertagiinaeLopez-Neyra, 1947. Annales de and ParasitologieHumaine et Comparee64: 356-373. Ostertagiinae (Lichtenfels Pilitt, 1991). ANDA. G. CHABAUD.1981. Nouvel essai de classificationdes The distribution of S. to coincide , geographic bubalis appears nematodesTrichostrongyloidea. Annales de ParasitologieHumaine with that of its type host B. bubalis, but the present report and et Comparee56: 297-312. that of Bryan et al. (1976) demonstrate that this nematode can GIBBONS,L. M., ANDL. F. KHALIL.1982. A key for the identification of also infect B. taurus. In Australia, Bryan et al. (1976) found B. generaof the nematodefamily TrichostrongylidaeKeiper, 1912. 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