(Nematoda: Habronematidae) from the Burchelps Zebras and Hartmann's Mountain Zebras in Southern Africa

Proc. Helminthol. Soc. Wash. 56(2), 1989, pp. 183-191

Habronema malani sp. n. and Habronema tomasi sp. n. (Nematoda: Habronematidae) from the BurchelPs Zebras and Hartmann's Mountain Zebras in Southern Africa

ROSINA C. KRECEK Department of Parasitology, Faculty of Veterinary Science, University of Pretoria, Private Bag X04, Onderstepoort 0110, South Africa

ABSTRACT: Habronema malani sp. n. is described from the stomachs of 44 Burchell's zebras, Equus burchelli antiquorum, in the Etosha and Kruger national parks and 6 Hartmann's mountain zebras, Equus zebra hartmannae, from the Etosha National Park in southern Africa. Habronema tomasi sp. n. is described from the small intestines of 35 Burchell's zebras in the Kruger National Park. Habronema malani is distinguished from other members of the genus by its deep buccal capsule with walls that are narrower anteriorly than posteriorly and have projections in the anterior end; spicule length ratio (right:left) ranging 1:2.3 to 1:3.7; a short, stout, and striated right spicule; and a long and slender left spicule with a pointed projection. Habronema tomasi is differentiated from the other species by buccal capsule walls that are wider anteriorly than posteriorly; a distance between the anterior wall of the buccal capsule and the inner surface of the lateral lips that is almost equal to the buccal capsule depth; an ovejector with spiral-shaped muscles; and a spicule length ratio (right: left) ranging 1:1.5 to 1:2.95. The right spicule of//, tomasi is short and cross striated except at the distal fourth where the tip is flanged. The left spicule is long and cross striated in the first one-third and partially cross striated in the second one-third. A key to the equine Habronema species is also included. KEY WORDS: taxonomy, Nematoda, Equus burchelli, Equus zebra, key to genera of equine Habronema, zebras, equids, southern Africa.

Members of the nematode family Habrone- Materials and Methods matidae parasitize the stomachs of mammals and Adult worms were recovered from the stomachs and birds. There are 6 species found in equids and small intestines of 35 Burchell's zebras (Equus burchelli these are frequently pathogenic. These include 5 antiquorum H. Smith, 1841) in the Kruger National belonging to the genus Habronema and 1 to the Park (KNP), Republic of South Africa, and 9 Burchell's zebras and 6 Hartmann's mountain zebras (Equus ze- genus Draschia (Yamaguti, 1961). The larval bra hartmannae Matschie, 1898) in the Etosha Na- stages develop in flies (e.g., Musca domestica), tional Park, South West Africa/Namibia. These nema- and if the infective larvae of some of these habro- todes agree with the generic description of Habronema nematids (e.g., Draschia megastoma (Rudolphi, by Lichtenfels (1975), but they could not be assigned 1819), Habronema majus (Creplin, 1849) Ran- to known species. The zebras were processed for parasitological studies som, 1911, Habronema muscae (Carter, 1861) and the nematodes were killed in Lugol's iodine and Diesing, 1861) are deposited in wounds, they fixed in 10% formalin (Malan et al., 198la, b). The cause "summer sores" (Lichtenfels, 1975; Arun- specimens were cleared in lactophenol and examined del, 1978). The adults of Draschia megastoma with a Nikon Optiphot light microscope fitted with disc (syn. Habronema megastoma (Rudolphi, 1819) interference contrast. The anterior end of some of the specimens was cut transversely in the region of the Railliet, 1923) often form abscesses that can range buccal capsule. This cut end was mounted en face, in size from 2.5 to 10.0 cm in diameter and are which enabled the structures of the head region to be found in both the glandular and non-glandular examined. portions of the stomach in both domestic and For scanning electron microscopy (SEM) the for- malinized nematodes were dehydrated in ethanol and wild equids (Lichtenfels, 1975; Scialdo-Krecek, critical point dried in liquid CO2 (Humphreys, 1975). 1984). The dried nematodes were oriented onto a stub bearing During parasitological investigations on Bur- adhesive and coated with gold/palladium. They were chell's zebras and Hartmann's mountain zebras examined by SEM at 5-20 kV. (Scialdoetal., 1982; Scialdo-Krecek, 1983; Scial- Specimens of Habronema from the United States National Museum Helminthological Collection (USNM do-Krecek et al., 1983), 2 new species of Habro- Helm. Coll.), Beltsville, Maryland, U.S.A., which were nema were recovered. These are described be- borrowed and examined, included H. majus (USNM low. Helm. Coll. Nos. 31066, 31091), H. muscae (USNM 183

Helm. Coll. Nos. 33300, 43258, 58493), H. zebrae and Burchell's zebras in the KNP and Etosha (USNM Helm. Coll. No. 79007), and type specimens National Park. of//, longistoma (USNM Helm. Coll. No. 61415). TYPE SPECIMENS: Three intact males and females (T-2169) in the Onderstepoort Helmin- Description of Species thological Collection, Veterinary Research In- GENERAL: Spirurida, Habronematoidea, stitute, Onderstepoort, South Africa; 3 intact Habronematidae, Habronematinae, Habrone- males and females (1985. 2185-2190) in the Brit- ma. Long, filiform worms. Deep buccal capsule, ish Museum, London, U.K.; and 4 intact males walls narrower anteriorly than posteriorly with and females (79803) in the United States Na- projections in anterior end. Head with 2 lateral tional Museum Helminthological Collection trilobed pseudolabia with 6 inner labial papillae. (USNM Helm. Coll., USDA), Beltsville, Mary- Four cephalic papillae each with 1 outer labial land, U.S.A. papilla next to it, and 2 amphids with 1 outer HOST AND LOCALITY: Equus burchelli anti- labial papilla next to each. Anterior portion of quorum H. Smith, 1841. Kruger National Park, esophagus muscular and narrower than posterior Republic of South Africa (25°12'-24°24'S, 31°36'- glandular portion. 32°2'E). Etosha National Park, South West Af- rica/Namibia (19°15'S, 14°31'E). Habronema malani sp. n. Equus zebra hartmannaeMalschie, 1898. Eto- (Figs. 1-7, Table 1) sha National Park, South West Africa/Namibia DESCRIPTION: Dimensions given as range (19°15'S, 14°31'E). (mean in ^m ± 1 standard deviation) unless oth- SITE OF INFECTION IN HOST: Stomach. erwise indicated. ETYMOLOGY: This species is named after Dr. MALES (10 specimens): Length 16.3-19.6(18 F. S. Malan, a South African parasitologist. ± 1.0) mm. Width 305-332 (316 ± 22.5). Depth of buccal capsule 52-70 (59 ± 6.9). Width of Habronema tomasi sp. n. buccal capsule 20-42 (29 ± 7.6). Base of buccal (Figs. 8-16, Table 1) capsule to outer lip 72-90 (79 ± 6.6). Esophagus GENERAL: Anteriorly in buccal capsule, and 2.1-4.2(3 ± 0.6) mm long and 120-240(166 ± interlabially, is a pair of medial ridges with a slit- 32) wide. Nerve ring 217-303 (273 ± 27.8) from like opening between them. Each has 3 teeth. base of stoma. Right spicule stout and striated, Posteriorly there is a larger tooth on either side 580-900 (772 ± 98.0). Left spicule slender, 1.9- of the ridges. Two lateral pseudolabia with 4 in- 2.4 (2 ± 0.2) mm with a pointed projection. ner labial papillae. Four cephalic papillae with Spicule length ratio ranging (right:left) 1:2.3 to 1 outer labial papilla next to each, and 2 amphids 1:3.7. Four pairs of pedunculated preanal pa- with 1 outer labial papilla next to each. pillae, 4 on the right slightly anteriorly placed DESCRIPTION: Dimensions given as range relative to the cloaca. Four postanal papillae, 1 (mean in ^m ± 1 standard deviation) unless oth- next to lip of cloaca, 1 single and 1 pair % distance erwise indicated. from anus to posterior extremity. MALES (10 specimens): Length 7.9-10.9(9.1 FEMALES (10 specimens): Length 17.8-24.6 ± 0.9) mm. Width 144-208(174 ± 20.2). Depth (22 ± 2.0) mm. Width 305-492 (354 ± 56.0). of buccal capsule 28-52 (40 ± 7.4). Width of Depth of buccal capsule 52-88 (67 ± 12.4). Width buccal capsule 12-32 (21 ± 6.2). Base of buccal of buccal capsule 20-30 (26 ± 3.0). Base of buc- capsule to outer lip 76-82 (80 ± 2.4). Esophagus cal capsule to outer lip 80-112 (91 ± 10.4). 2.2-2.8 (2.4 ± 0.2) mm long and 72-112 (86 ± Esophagus 2.8-3.9 (3 ± 0.3) mm long and 104- 12.1) wide. Nerve ring 180-240 (204 ± 15.8) 200(156 ± 41.0) wide. Nerve ring 239-332 (294 from base of stoma. Right spicule stout and ± 65.3) from base of stoma. Vagina short 72- striated, 336-480 (410 ± 49.5) and distal fourth 104(78 ± 15.2). Ovejector long 700-1,000 (887 with flanged tip. Left spicule slender, 690-992 ± 102.4). Vulva 8.7-12.6 (11.0 ± 1.2) mm from (851 ± 108.9). Spicule length ratio ranging (right: anterior extremity. Anus 240-340 (286 ± 38.2) left) 1:1.5 to 1:2.95. Four pairs of pedunculated from tip of tail. Egg 40-80 (66 ± 12.3) long and preanal papillae, 4 on the right slightly anteriorly 4-16 (10 ± 4.1) wide. placed relative to the cloaca, and 1 single preanal HOST RECORD INFORMATION: Total burdens papilla next to the cloaca. Two postanal pairs of (3-1,244) of this species were recovered from the papillae, 1 posterior to the cloaca and the other stomachs of both Hartmann's mountain zebras separated so 1 on either side, approximately half

80 pm Figures 1-5. Habronema malani sp. n. 1. Lateral view of head. 2. En face view of head. 3. Lateral view of male tail showing spicules. 4. Ventral view of male tail with papillae. 5. Lateral view of female vulva, vagina, and ovejector. of the distance between the tip of the tail and the from anterior extemity. Anus 136-200 (176.4 ± cloaca. 19.3) from tip of tail. Egg 96-120 (110.4 ± 10.4) FEMALES (10 specimens): Length 13.2-16.4 long and 8-12 (8.4 ± 4.1). (14.9 ± l.l)mm.Width 192-260(229.2 ± 20.9). HOST RECORD INFORMATION: Total burdens Depth of buccal capsule 48-92 (67.2 ± 14.6). (1-1,243) of this species were recovered from the Width of buccal capsule 12-32(20.8 ± 5.9). Base small intestines of 35 Burchell's zebras in the of buccal capsule to outer lip 72-100 (86.0 ± KNP. 8.7). Esophagus 2.3-4.2 (3.0 ± 0.6) mm long and TYPE SPECIMENS: Three intact males and fe- 80-128 (105.6 ± 17.6) wide. Nerve ring 176- males (T-2170) in the Onderstepoort Helmin- 360 (251.6 ± 61.0) from base of stoma. Vagina thological Collection, Veterinary Research In- very short, 20-40 (22.2 ± 6.7). Ovejector long stitute, Onderstepoort, South Africa; 3 intact and straight, 300-400 (346.6 ± 33.5) with spiral- males and females (1985. 2191-2196) in the Brit- shaped muscles. Vulva 5.0-7.0 (6.2 ± 0.7) mm ish Museum, London, U.K.; and 5 intact males

Figures 6, 7. Habronema malani sp. n. 6. Scanning electron micrograph of en face view of head. A, amphids; P, outer labial papillae; C, cephalic papillae; arrows, inner labial papillae. Scale bar = 40 pm. 7. Light micrograph of female vulva (top arrow) with long ovejector (ends at bottom arrow). Scale bar = 300 jim. and females (79804) in the United States Na- 2 species, H. malani has a shorter vagina. This tional Museum Helminthological Collection, structure crosses the body transversally in both USDA, Beltsville, Maryland, U.S.A. species before reaching a long muscular ovejec- HOST AND LOCALITY: Equus burchelli anti- tor. Further, the spicule ratio of H. malani is quorum H. Smith, 1841. Kruger National Park, smaller than that of//, muscae. Habronema ma- Republic of South Africa (25°12'-24°24'S, 31°36'- lani is a large worm surpassed only by H. majus 32°2'E). in total body length. Habronema malani is fur- SITE OF INFECTION IN HOST: Small intestine. ther distinguished by the buccal capsule shape, ETYMOLOGY: This species is named after my which is narrower anteriorly than posteriorly, and husband, Mr. Tomas E. Krecek. by the anterior projections on the buccal capsule walls. Discussion Although H. tomasi sp. n. does not closely The 6 habronematid species reported from resemble any of the other known species, its clos- equids are: H. longistoma van den Berghe, 1943; est possible congener in terms of ovejector shape H. majus; H. muscae; H. tyosenense Yamaguti, is H. majus. Habronema tomasi differs from 1943; H. zebrae Theiler, 1923; and D. mega- Theiler's (1923) H. majus in the distance be- stoma. With the exception of H. tyosenense, all tween the anterior wall of the buccal capsule and these species have been reported from Hart- inner surface of the lateral lips, which is almost mann's mountain zebras and BurchelFs zebras equal to the buccal capsule depth. Habronema (Theiler, 1923; Round, 1968;Scialdoetal., 1982; tomasi has 1 more postanal papilla near the cloa- Scialdo-Krecek, 1983; Scialdo-Krecek et al., ca than H. majus. The ovejector of//, tomasi is 1983). muscular and spiral-shaped but elongated, while Although H. muscae is reported from a dif- that of//, majus is muscular and rounded. Fur- ferent host than H. malani sp. n., this new species ther, H. tomasi is a small worm and delicate in most closely resembles H. muscae. Between these appearance. This may be because of its short

Copyright © 2011, The Helminthological Society of Washington Table 1. Principa l measurement s of Habronema muscae, H. majus, H. malani, and H. tomasi (all measurement s in /urn unless otherwise indicated) .

H. muscae H. majus H. malani H. tomasi

3 9 $ 0 & 2 3 9

Total length (mm) 9.5-13.0 11.2-19.7 15.2-18.4 22.6-23.2 16.3-19.6 17.8-24.6 7.9-10.9 13.2-16.4

Width 199-279 199-319 360-400 440-500 305-332 305-492 144-208 192-260 ON Buccal capsule G Length 42-70 40-60 48-64 54-64 52-70 52-88 28-52 48-92 Width 12-20 20-30 16-30 36-54 20^12 20-30 12-32 12-32 ma Base buccal capsule to outer lip 60-80 60-80 66-88 84-88 72-90 80-112 76-82 72-100 J O Esophagus •—, Length (mm) 1.9-2.5 1.8-2.8 3.1-4.0 3.3-3.8 2.1^. 2 2.8-3.9 2.2-2.8 2.3-4.2 Gr Width 88-144 96-140 140-160 1 60-200 120-240 104-200 72-112 80-128

Distance nerve ring from base of stoma 191-244 198-297 120-280 240-280 217-303 239-332 180-240 176-360 oo

Copyright © HelminthologicalThe 2011,of SocietyCopyright© Washingto Spicule lengths Right spicule 360-520 - 340-380 580-900 - 336^8 0 - Left spicule (mm) 2.0-2.8 - 750-810 _ 1.9-2.4 — oyu-yy/ — Length of vagina _ 176-400 — 136-140 - 72-104 - 20^ 0 Length of ovejector - 0.8-1.0 — 200-250 - 0.7-1.0 - 300-40 0 Distance vulva from anterior end (mm) - 5.5-8.1 — 9.2-9.6 - 8.7-12.6 - 5.0-7. 0 Distance anus to tip of tail - 280-376 - 220-240 240-340 136-200 Egg Length - 48-60 — 15-18 - 40-8 0 - 96-120 Width - 8-12 - 6-8 - 4-16 8-12

F O [NGTON, ] WASH E VOLUM 188 PROCEEDINGS OF THE HELMINTHOLOGICAL SOCIETY

11 12 80 Figures 8-12. Habronema tomasl sp. n. 8. Lateral view of head. 9. En face view of head. 10. Lateral view of male tail with spicules. 11. Ventral view of male tail showing papillae. 12. Lateral view of female vulva, vagina, and ovejector. body length but widely separated transverse (onchia) that develop from the lining of the buc- striations of the cuticle. cal capsule (Inglis, 1964). Inglis speculated on The medial interlabial ridges of the buccal cap- the feeding functions of these structures. Habro- sule of H. tomasi may be an extension of the nema tomasi inhabits the small intestine of the capsule walls and of the interlabia, and appear zebra, and in the equid this organ is rarely in- to separate the buccal capsule into a lower and habited by helminths. The viscous character of an upper chamber. This buccal capsule differs the small intestinal contents contrasts markedly considerably from all of the other equine species with the dry, coarse ingesta of the stomach of of this genus. However, there is some morpho- equids. In the present study, it appears that the logic similarity with a free-living marine enoplid interlabial ridges could be of assistance during Pontonema yaena Inglis, 1964. This species has feeding in this viscous environment. ventro-lateral and dorsal tooth-like structures The description of the genus Habronema ac-

Figures 13-16. Habronema tomasi sp. n. 13. Scanning electron micrograph (SEM) of en face view of head with teeth on interlabial ridges and teeth either side. A, amphids; P, outer labial papillae; C, cephalic papillae; arrows, inner labial papillae. 14. SEM of vulvar opening (arrow) and widely separated transverse striations. 15. SEM of male tail showing papillae near cloaca and a spicule partially extruded. 16. Light micrograph of spiral- shaped, muscular female ovejector with vulvar opening (arrow). Scale bars = 20 /tin, Figure 13; 40 /im, Figures 14-16. cording to Lichtenfels (1975) should be revised factors. Habronema tomasi is a much smaller to accommodate the total body length as 7-35 nematode than the others of its genus. The mean mm and not 8-35 mm. total length is almost half the length if compared The location in the host for the Habronema with H. malani. Hence, such a nematode could species known in the horse is the stomach (Lich- be easily missed using conventional recovery tenfels, 1975). It is of interest to note than H. techniques. Furthermore, few nematodes appear tomasi sp. n. was recovered only from the small to inhabit the small intestine of the equid as com- intestine in the zebras. Contrastingly, in horses pared with the other organs (Lichtenfels, 1975). it is uncommon to recover any nematodes from It remains though a sizeable organ, and if not this organ. sampled adequately, a small nematode such as The absence of the 2 new species from Thei- H. tomasi may be overlooked. Theiler's study ler's (1923) study may be attributable to several was only semi-quantitative, and presumably

techniques used for nematode recovery were not postanal papillae. All other Habronema species as advanced as those of today. The high preva- have extra papillae post- or preanally as well as lence of H. malani in recent reports, 96% in 25 an asymmetric arrangement. Burchell's zebras (Krecek et al., 1987), suggests that this nematode may have been present but Acknowledgments was not detected in Theiler's small sample size I thank Dr. F. S. Malan, Professor R. K. Re- of 3 zebras. Alternatively, it is possible that con- inecke, and Professor Anna Verster, who con- ditions required for the presence of a suitable tributed to discussion of the new species; Pro- intermediate host for these nematodes were ab- fessor Verster for helpful comments regarding sent in the habitat of Theiler's zebras, and there- the manuscript; Dr. J. R. Lichtenfels for his help- fore, the life cycle of this nematode was not com- ful comments regarding the 2 new species; United pleted. States National Museum Helminthological Col- A key to distinguish all equine species of the lection for the loan of study specimens; Mr. T. genus Habronema follows. E. Krecek for helpful discussion and assistance with the drawings and in layout of the plates; la. Very long cylindrical buccal capsule 2 Mrs. Norita Chaney, Plant Stress Laboratory, Ib. Short buccal capsule 3 2a. Cuticular collar present at anterior end of sto- Electron Microscope Facility, Agricultural Re- ma H. longistoma1 search Service, Beltsville, Maryland, U.S.A., for 2b. Cuticular collar absent; left spicule 4 times the scanning electron micrographs; and the ref- length of right; vagina long and narrow, erees whose criticism substantially contributed crosses body transversally before reaching to the manuscript. This is a portion of a disser- long muscular ovejector H. zebrae 3a. Left spicule 2-3 times length of right; vagina tation submitted for the D.Sc. degree in Zoology, very short before reaching rounded part of University of Pretoria, South Africa, and was muscular ovejector 4 supported by the following in South Africa: Uni- 3b. Left spicule 2-5 times length of right; vagina versity of Pretoria, Council for Scientific and In- crosses body transversally before reaching long muscular ovejector 5 dustrial Research, Hoechst, and the Fritz Visser 4a. Vagina short (136-140 yum) with large rounded Agricultural Bursary. ovejector (200-250 Mm); cuticle without widely separated transverse striations; teeth Literature Cited present on ventral and dorsal walls of buccal Arundel, J. H. 1978. Parasitic diseases of the horse. capsule H. majus The Postgraduate Foundation in Veterinary Sci- 4b. Vagina very short (20-40 /xm); ovejector 300- ence. Veterinary Review 18:83 pp. 400 ^m long with spiral-shaped muscles; cu- Humphreys, W. J. 1975. Principles and techniques ticle with widely separated transverse stria- of scanning electron microscopy. Pages 707-714 tions; pair of medial ridges interlabially with in O. Johari and I. Corvin, eds. Scanning Electron slit-like opening and 3 small teeth on each Microscopy. IIT Research Institute, Chicago. ridge, also, larger tooth either side of the Inglis, W. G. 1964. The marine Enoplida (Nema- ridges H. tomasi toda): a comparative study of the head. Bulletin 5a. Vagina short (72-104 jum); left spicule 21/2-3'/2 of the British Museum (Natural History) Zoology times length of right H. malani 2:265-376. 5b. Vagina long and narrow (176-400 /um); left Krecek, R. C., F. S. Malan, R. K. Reinecke, and V. de spicule 5 times length of right H. muscae Vos. 1987. Nematode parasites from Burchell's zebras in South Africa. Journal of Wildlife Dis- H. tyosenense is not included in the preceding eases 23:404-411. key because type specimens were not available. Lichtenfels, J. R. 1975. Helminths of domestic equids. Illustrated keys to genera and species with em- Based on Yamaguti (1961), H. tyosenense resem- phasis on North American forms. Proceedings of bles H. majus and H. tomasi with a 1:2 (right: the Helminthological Society of Washington (Spe- left) spicule ratio. Habronema tyosenense differs cial issue)42:92 pp. from all other species in the arrangement and Malan, F. S., R. K. Reinecke, and R. C. Scialdo. number of genital papillae. The number of pa- 198 la. Recovery of helminths postmortem from equines. I. Parasites in arteries, subperitoneum, pillae are fewest and are the most symmetrically liver and lungs. Onderstepoort Journal of Veter- arranged, with 4 pairs of preanal and 2 pairs of inary Research 48:141-143. , , and . 1981b. Recovery of helminths postmortem from equines. II. Helminths and larvae of Gasterophilus in the gastro-intestinal ' Type specimens are all females; males were not tract and oestrids from the sinuses. Onderstepoort included in original description, and are still unknown. Journal of Veterinary Research 48:145-147.

Round, M. C. 1968. Check list of the helminth ies on the parasites of zebras. III. Nematodes of parasites of African mammals of the orders Car- the mountain zebra from the farm "Kelpie" and nivora, Tubulidentata, Proboscidea, Hyracoidea, the Namib-Naukluft Park, South West Africa/Na- Artiodactyla and Perissodactyla. Technical Com- mibia. Onderstepoort Journal of Veterinary Re- munication, Commonwealth Bureau of Helmin- search 50:283-290. thology 38. 252 pp. Theiler, G. 1923. The strongylids and other nema- Scialdo, R. C., R. K. Reinecke, and V. de Vos. 1982. todes pa.rasitic in the intestinal tract of South Af- Seasonal incidence of helminths in the BurchelFs rican equines. Reports of the Director of Veteri- zebra. Onderstepoort Journal of Veterinary Re- nary Education and Research, Union of South search 49:127-130. Africa 9-10:601-773. Scialdo-Krecek, R. C. 1983. Studies on the parasites van den Berghe, L. 1943. Enquete Parasitologique. of zebras. I. Nematodes of the Burchell's zebra in II. Helminthes Parasites. Exploration du Pare Na- the Kruger National Park. Onderstepoort Journal tional Albert et du Pare National de la Kagera. I. of Veterinary Research 50:111-114. Mission L. van den Berghe (1936) 2:1-30. . 1984. The nematode parasites of Equus zebra Yamaguti, S. 1943. Studies on the helminth fauna of hartmannae and Equus burchelli antiquorum from Japan. Part 43. Mammalian nematodes, IV. Jap- different areas of southern Africa. D.Sc. Disser- anese Journal of Zoology 10:427-457. tation, University of Pretoria, Pretoria, South Af- . 1961. Systema Helminthum. Vol. 3. The rica. 261 pp. Nematodes of Vertebrates. Interscience Publish- , R. K. Reinecke, and H. C. Biggs. 1983. Stud- ers, Inc., New York. 679 pp.