ROSINA C. KRECEK(l), R. K. REINECK 0 > and F. S. MALAN< 2 >
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1 OnderstepoortJ. vet Res., 54,7178 (187) STUDES ON THE PARASTES OF ZEBRAS. V. NEMATODES OF THE BURCHELL'S AND HARTMANN'S MOUNTAN ZEBRAS FROM THE ETOSHA NATONAL PARK, SOUTH WEST AFRCA/NAMBA ROSNA C. KRECEK(l), R. K. RENECK > and F. S. MALAN< 2 > ABSTRACf KRECEK, ROSNA C., RENECKE, R. K. & MALAN, F.S Studies on the parasites of zebras. V. Nematodes of the Burchell's and Hartmann's mountain zebras from the Etosha National Park, South West Africa!Nam.ibia. Onderstepoort Journal of Veterinary Research, 54,7178 (187) Nine Burchell's and 6 Hartmann's mountain zebras were culled during the 3 climatic JlCriods characteristic of the Etosha National Park, South West Africa!Nam.ibia, and were examined for helminths. The Burchell's zebras ranged in ae from 4\1 to 1 years and the mountain zebras from 3\1 to 13 years. Twentyfive species of nematodes, belongmg to the families Atractidae, Strongylidae, Oxyuridae, Onchocercidae and Habronematidae, were recovered. Of the family Cyathostominae, the following species were the most numerous in the Burchell's zebras: Cyathostomum monjgomeryi (7 12(} ), Cylicocyclus triramosus ( ), Cylicostephanus minutus ( ) and Cylindropharynx sp.(? injermedia) ( ). The atractids present were: Crossocephalus viviparus ( ) and Probstmayria vivipara ( ). Three of the above cyathostome species were also most abundant in mountain zebras: Cylicocyclus triramosus ( ), Cylicostephanus minutus ( ) and Cylindropharynx sp. (? intermedia) (35 325). New reports include Cylicostephanus longiconus in the Burchell's zebras and Cyathostomum alveatum, Cyathostomum montgomeryi, Cylicostephanus bidentatus and Draschia megastoma in the mountain zebra. The overwintering of 4th stage cyathostomes in the gut walls and their emergence which differ in the 2 hosts, are discussed. lntroducfion The Etosha National Park is the habitat of both Burchell's (Equus burchelli antiquorum) and Hartmann's mountain zebra (Equus zebra hartmannae), where they share some of the same grazing. With the exce{>tion of Equus burchelli, which is designated to species, the early hostparasite checklists (Monnig, 128: Le Roux, 132) oup all the zebras together, regardless of species. ScialdoKrecek, Reinecke & Biggs (183) reported on the seasonal prevalence of the internal parasites of Hartmann's mountain zebra in central SW A/Namibia while Scialdo, Reinecke & DeVos (182) reported o those of Burchell's zebra in the Kruger National Park. Etosha, moreover, presented a unique study. Firstly, it gave the opportunity to compare parasites from 2 zebra host species sharing the same locality and, secondly, to study the parasites from these 2 hosts during the 3 climatic periods which occur in Etosha. MATERALS AND METHODS Study area Nine burchell's and 6 Hartmann's mountain zebras were culled near Otjovasandu (1 15' S, 14 31' E), in the west of the Etosha National Park and in the central area near Okaukuejo (1 8'S, 15 55' E)(Fig. 1) c.rtr ANGOlA 23 FG. 2 An area typical of Otjovasandu " * FG. South West Africa!Nam.ibia, showing Etosha National Park in the North <t> Department of Parasitology, Faculty of Veterinary Sciene, Private Bag X4, University of Pretoria, Onderstepoort OliO <l> Hoechst Research Farm, P.O. Box 124, Malelane 132 Received 16 September 186Editor FG. 3 An area typical of Okaukuejo 71
2 STUDES ON THE PARASTES OF ZEBRAS. V 64 3 ::J lii 2 1 Q) 4 3 ::J lii 2 E 1 Q) 15 e1oo.s JFMAMJ J A 5 1 1ND FG. 4 Mean monthly maximum ( /:, ) and minimum ( o ) temperatures at Okaukuejo and total monthly rainfall at Otjovasanilu in the Ecosha National Park for 182 The Etosha National Park (23 km 2 ) encompasses 2 major vegetation types: saline desert with a dwarf shrub savanna fringe, and Mopane savanna (Giess, 171). TyJ?ical areas of Otjovasandu and Okaukuejo are illustrated m Fig. 2 and 3. Sources of water for the zebras are both natural and artificial. Waterboles surround the Etosha Pan following rains, and manmade waterholes, providing water during dry periods, have been constructed along the perimeter o( the pan. Rainfall Otjovasandu The total annual rainfall at Otjovasandu for 182 was 235 mm. No rain fell during 8 of the latter months of the year. The predicted longterm rainfall for this area is 335 mm per annum (Department of Water Affairs, SWA/Namibia, unpublished data, 177). Temperature data, which were not available from Otjovasandu, were recorded from Okaukuejo (Fig. 4). Okaukuejo The total annual rainfall recorded at Okaukuejo in 182 was 333 mm and no rain fell from MayAugust (Fig. 5). The predicted rainfall for this area 1s 5 mm per annum (Department of Water Affairs, SW A/Namibia, unpublished data, 177). Animals studied Walter (173), cited by Berry (18), identifies 3 climatic periods at Etosha: Wet and hot (1 January to 3 April) Dry and cold (1 May to 31 August ) Dry and hot (1 September to 31 December). Two Burchell's and 2 Hartmann's mountain zebras at Otjovdu and 1 Burchell's near Okaukuejo were culled m each of the 3 seasons in 182, that is, March, July and November. FG. S Mean monthly maximum(/:, ) and minimum (O) temperatures and total monthly rainfall at Okaukuejo in the Etosha National Park for 182 Age The Burchell's (B) zebras were divided into 2 age groups: Five adult zebras aged 4,56,5 years and 4 old zebras aged 8,51 years. The mountain (M) zebras were also divided according to age: Three adult zebras aged 3,54,5 years and 3 old zebras aged 1213 years. Helminth collection On 2 occasions, 2 zebras from Otjovasandu were shot and transported from 41 h to the Okaukuejo Veterinary Laboratory. A walkin cooler with movable block allowed 1 zebra to be stored in a cool room, while necropsy on the other zebra was in progress. The method of collection of helminths from the zebra has been described by Malan, Reinecke & Scialdo (181 a, b) and ScialdoKrecek et al. (183). dentification of nematode species Species were identified and recorded separately. The 5th stages and the sexually mature adults (A) were determined to the species level, while the 4th larval stage (L 4 ) was recorded as Habronematidae, Cyathostominae and Triodontrophorus spp. RESULTS The total nematode burdens included the families Strongylidae, Oxyuridae, Onchocercidae, Atractidae and Habronematidae (Tables 25). The mean nematode burdens and prevalence of cyathostomes in the intestinal tract of the Burchell's zebras are shown in Fig. 6, while the site distribution of the cyathostomes is illustrated in Fig. 7. The same information for the mountain zebras is presented in Fig. 8 &. Twentyfive nematode species were recovered and divided as follows: 13 Cyathostominae, 4 Strongylinae, 4 Habronematidae, 1 Onchocercidae, Oxyuridae and 2 Atractidae. The Atractidae had the highest burdens. Sixteen Habronema zebrae, recovered from B6, are not included in Table 4. 72
3 TABLE 1 Descriptions used in the identification of nematodes in BurcheU' s and mountain zebras AUTHORS ROZNA C. SCALOOKRECEK, R. K. RENECKE & F. S. MALAN 8 i N \ :B' = " s.. ell.!... N ::E N" v:; cl!! 'D r..>4..>4 N" J! J! a; v:;., "' j... N... "' ;"' a; ::E ::E :r: = '8 ell.! ell.! 8: !:l.a.. > ; 2.a., " :: = >. 8. CQ.$,! u...1 c>l Cl) ;.. l 1i. Cyathostominae Cyathostomum a/veatum Cyathostomum montgomeryi Cyathostomum tetracanthum Cy/icocyclus adersi* Cylicocyclus auriculatus Cylicozclus triramosus Cylico ontophorus reineckei + Cylicodontophorus schuermanni + Cylicostephanus bidentatus + + Cylicostephanus calicatus Cylicostephanus longiconus + Cylicostephanus minutus Cylindropharynx spp Strongylinae Craterostomum acuticaudatum Triodontophorus serratus Habronematidae Draschia megastoma + Habronema majus + Habronema zebrae + Atractidae Crossocephalus viviparus + + Probstmayria vivipara + + Oxyuridae Oxyuris equi + Onchocercidae Setaria equina + Described by Boulenger (12a) n addition, 2 new Triodontophorus spp. were identified and in this manuscript will be referred to as Triodontophorus n. sp. (A) and Triodontophorus n. sp. (B) Likewise, 2 new Habronema spp. which were recovered will be referred to as Habronema n. sp. (A) and Habronema n. sp. (B) 25, 1 (i) ' ' 1:: 1:: Q) "' ' "' :::J :::J. 15, ' "'... 5.o "' E Q) N Q) 'O 1:: Q) c: 25 Q) "' "'.!:: FG. 6 Mean nematode burdens (D) and prevalence ( ) of BurcheU's zebras infested with 13 species of cyathostomes, Etosha, Cyathostomum alveatum, 2. Cyathostomum montgomeryi, 3. Cyathostomum tetracanthum, 4. Cylicocyclus adersi, 5. Cylicocyclus auriculatus, 6. Cy/icocyclus triramosus, 7. Cylicodontophorus reineckei, 8. Cylicodontophorus schuermanni,. Cylicostephanus bidentatus, 1. Cylicostephanus calicatus, 11. Cylicostephanus longiconus, 12. Cylicostephanus minutus, 13. Cylindropharynx sp. (? intermedia) DSCUSSON This is the frrst report of infestation of mountain zebras by Cyathostomum alveatum, Cyathostomum montgomeryi, Cylicostephanus bidentatus and Draschia megastoma. Triodontophorus n. sp. (A) was recovered from the Burchell's zebras, but not from mountain zebras at Etosha. This is the frrst report of Cylicostephanus longiconus infesting Burchell's zebras. This species had 73 previously been recovered only from mountain zebras (ScialdoKrecek, 183 b; ScialdoKrecek et al. 183). Cyathostomes most abundant in Etosha's Burchell's zebras were: Cyathostomum montgomeryi ( ), Cylicocyclus triramosus ( ), Cylicostephanus minutus ( ) and Cylindropharynx sp. (? intermedia) ( ). Atractids with the highest burdens were: Crossocephalus viviparus
4 J """' TABLE 2 Faecal nematode egg counts and total nematode burdens of Strongylidae, Oxyuridae and Onchocercidae recovered from Burchell's zebras (B), Otjovasandu and Okaukuejo, Etosha, March 182November 182 ;J (*B B61&akaukuejo area) tt1 Zebra No. Age (yr)/sex Date ldlled/season** Eggs per gram of faeces Cyathostominae L 4 Cyathostominae Cyathostomum alveatum Cyathostomum montgomeryi Cyathostomomum tetracamhum Cylicocyc/us adersi Cylicocyc/us auricu/atus Cy/icocyc/us triramosus Cylicodunrophorus reineckei Cylicodomophorus schuermanni Cylicostephanus bidematus Cylicostephanus calicatus Cylicostephanus longiconus Cylicostephanus minurus Cylindropharyru sp. (? illlermedia) Strongylinae Craterostomum acuticaudatum Triodomophorus n. sp. (A) Triodomophorus n. sp. (B) Triodomophorus serratus Oxyuridae Oxyuris equi L 4 Oxyuris equi Adult Onchocercidae Setaria equina *B1 B1 6/M lim 4/3182/Su N.D.() 3/3/82/Su N.D s Bl B. B 6/M 4 5/M 3/3/82/Su 13nt82/W 13nt82/W N.D *B6 B1 Bs 6W 8W 8 14nt82/W 23/11/82/S 23/11182/S 4 2! *B 11M /S N.D. Total Zebras positive Range S M < ** Su =Summer, W =Winter, S =Spring 1 N.D. =notdetermined
5 V! TABLE 3 Faecal nematode egg counts and total nematode burdens of Strongylidae, Oxyuridae and Onchocercidae recovered from mountain zebras (M), Otjovasandu, Etosha, March 182November 182 Zebra No. Age (yr)/sex Date killed/season* Eggs per gram of faeces Cyathostominae L 4 Cyathostominae Cyathostomum alveatum Cyathostomum montgomeryi Cyathostomomum tetracanthum Cylicocyclus adersi Cy/icocyclus auriculatus Cylicocyclus triramosus Cylicodontophorus reineckei Cylicodontophorus schuermonni Cy/icostephanus bidentatus Cy/icostephanus ca/icatus Cylicostephanus /ongiconus Cylicostephanus minutus Cylindropharynx sp. (? intermedia) Strongylinae Craterostomum acuticaudatum Triodontophorus n. sp. (A) Triodontophorus n. sp. (B) Triodontophorus serratus Oxyuridae Oxyuris equi L 4 Oxyuris equi adults Onchocercidae Setaria equina Su =Summer, W =Winter, S =Spring Ol N.D.=Notdetermined Ml 4WM 213/821Su N.D.<) M2 4Wf /Su 1 M3 121M 12nt82/W N.D.<) M4 M5 M6 3!&F 13/M 13/F 12!7/82/W 22//821S 22111/82/S Total Zebras positive TABLE 4 Total nematode burdens of Atractidae and Habronematidae recovered from Burchell's sebras (B), Otjovasandu and Okaukuejo, Etosha, MarchNovember 182 (*B 1 /BuBrOkaukuejo an:a) Zebra No. *Bt B2 Bl B B *B6 B, Bs *B Date Killed 3/82 3/82 3/82 7/82 7/82 7/82 11/82 11/ Atractidae Crossocepha/us viviparus 23 4** ** ** 8 16** * ** ** 6** Probstmoyria vivipara Habronematidae Draschia megastoma Habronema n. sp. (A) Habronema majus **Division of C. vivipa Y =Young rus according to sex and F = Female stages FP= Female bearing young M =Male Total Zebras Positive Range & & Range ;>?<:! P' :n
6 STUDES ON THE PARASTES OF ZEBRAS. V TABLE 5 Total nematode burdens of Atractidae and Habronematidae recovered from mountain zebras (M), Otjovasandu, Etosha, MarchNovember 182 Zebra No. Ml M2 M3 Date Killed /82 M4 M5 M ll/82 ll/82 Total Zebras positive Range Atractidae CrossocepMius viviparus Probstmayria vivipara 2* Habronematidae Draschia megastomn 2 Habronemn n. sp. (A) Habronemn mnjus 652 *Division of C. vivipa Y =Young rus according to sex and F = Female stages FP =Female bearinj young M= ale * S ,,:L = ' ,...,._.(2) Dorsal colon... Caecum C!l CTi'l FG. 7 The distribution of cyathostomes in the intestinal tract of Burchell's zebras, Etosha, 82. = preferred site. l. Cyatlwstomum alveatum, 2. Cyatlwstomum montgomeryi, 3. Cyathostomum tetracanthum, 4. Cylicocyclus adersi, 5. Cylicocyclus auriculatus, 6. Cylicocyclus triramosus, 7. Cylicodontoplwrus reineckei, 8. Cylicodontoplwrus schuermnnni,. Cylicostephanus bilkntatus, 1. CylicostepMnus calicatus, l. CylicostepMnus longiconus, 12. Cylicostephanus minutus, 13. CylindropMryrvc sp. (? intermedia) ( ) and Probstmayria vivipara ( ). Three of the above cyathostome species Cylicocyclus triramosus ( ), Cylicostephanus minutus ( ) and Cylindropharynx sp. (?intermedia) (35 325), were also abundant in Etosha's mountain zebras. That Cylicostephanus calicatus and Cylicostephanus minutus were recovered from the ventral colon confirms Theiler's (123) earlier findings for zebras and Hasslinger's (163) for horses. The presence of Poteriostomum ratzii in the dorsal colon of the zebra is also in agreement with the findings of Ogbourne (176) for domestic equids. However, Theiler (123) recovered Poteriostomum ratzii from both the ventral and dorsal colon in zebras. Peak numbers of L 4 cyathostomes in the gut wall occurrred in early winter in Burchell's zebras in Etosha and in both early winter and spring in the Etosha mountain zebras. This follows the pattern of previous surveys (Scialdo et al., 182; ScialdoKrecek et al., 183) and corroborates Ogbourne's (171) and Poynter's (154) fmdings in which L 4 cyathostomes were thought to overwinter in the gut wall. n addition, in mountain zebras more L 4 were present in the wall of the small intestine than in either the caecal or colonic wall. Apart from Cylicocyclus adersi (Boulenger, 12), Cylicocyclus auriculatus, Triodontophorus n. sp. (B) and Triodontophorus serratus, all nematode species were present in higher infestations in Burchell's zebras. Since there were greater numbers of 4th stages (L 4 ) and fewer numbers of 5th and adult stages in mountain zebras, it appears that the larval stages of the cyathostomes may be overwintering in greater numbers in the gut wall and not developing further. Hence, lower total burdens of the 5th and adult stages occur in the lumen of the gut of this host. t is postulated, therefore, that these 4 nematode species have adapted in the mountain zebra to overwinter longer than in the Burchell's zebra, that is, these immature nematodes (L 4 ) encyst in nodules in the intestinal wall for a prolonged period: This adaptation thus provides an extension (or interruption) of the nematode's life cycle. Whereas both host species depend on water the Burchell's zebra is more waterdependent (Smithers, 183). Furthermore, Smithers states that it is a savanna species, partial to open areas of woodland, open scrub and grassland where water is available. Hence, this zebra is never more than 112 km from water. According to Smithers (183), the Hartmann's mountain zebras in contrast generally inhabit mountains, deserts and open sandy plains (lona National Park, southwestern Angola) and are known to travel 1 km to seek water. The same author states that this host has evolved a behavioural adaptation to dig underground with its hooves for water if surface water is nonexistent. t is possible that the cyathostome species, infesting mountain zebras which have adapted to a more arid environment than Burchell's zebras, liave adjusted their strategy for survival. Perhaps seasonal variations applying to their host triger these nematodes to invade the small and large intestmal walls in the "dry" season, emerge from their larval stages in spring and develop to adults when they receive and respond to the appropriate cues. Parasitic nematodes in their normal defmitive host (the host in which parasites reach maturity and reproduce sexually) do not always reach adulthood within a developmental period of characteristic length, and prolonged interruption of the life cycle is a frequent alternative 76
7 ROZNA C. SCALOOKRECEK, R. K. RENECKE & F. S. MALAN til '" c: c: Q) a! "... "' : :.O.c 3 Q).:=:.. " a!... +".o a! Q) E N Q)"O c: Q) c: +" a! "' 1, 75 Q) 5 a5 «i 25 > Q)... a FG. 8 Mean nematode burdens (C) and prevalence ( ) of mountain zebras infested with 12 species of cyathostomes, Etosha, Cyathostomum alveatum, 2. Cyathostomum montgomeryi, 3. Cyathostomum tetracanthum, 4. Cylicocyclus adersi, 5. Cylicocyclus auriculatus, 6. Cylicocyclus triramosus, 1. Cylico<kntophorus schuermanni, 8. Cylicostephanus bidentatus,. Cylicostephanus calicatus, 1. Cylicostephanus longiconus, 11. Cylicostephanus minutus, 12 Cylindropharynx sp. (? intermedijj) 1,51 1, o..'..,.r;:a...,5 2.t :! 5 E.., c 5, :;. 4, L.o c ill ::; 2, 1, * ""M.m,.,..,a... :=frt.r;;bw""' t Descending colon * * Ventral colon * Caecum :J fej 1 i Fig. The distribution of cyathostomes in the intestinal tract of mountain zebras, Etosha, 182. *=preferred site. 1. Cyathostomum alveatum, 2. Cyathostomum montgomeryi, 3. Cyathostomum tetracanthum, 4. Cylicocyclus adersi, 5. Cylicocyclus auricula us, 6. Cylicocyclus triramosus. 1. Cylicodontophorus schuermanni. 8. Cylicostephanus bidentatus.. Cylicostephanus calicatus, 1. Cylicostephanus longiconus, 11. Cylicostephanus minutus, 12. Cylindropharynx sp. (? intermedia) (Schad, 177). According to Horak (18) a number of factors or cues have been proposed which may explain this interruption or arrested (inhibited) development. t should be emphasized that thus far the most comprehensive studies investisating arrested develoyment have been with parasites m the diestive tract o ruminants. Such factors fall into 3 categones: 1. External environmental factors acting on the freeliving stages (e.g. aging oflarvae, chilling and reduction in photoperiod). 2. Host factors, which determine the host's suitability for further development, and which, when adverse 77 conditions may load to arrest (e.g. host's diet, age of the host, acquired resistance, endocrine changes in the host and environmental factors acting on the host) and 3. Parasiterelated factors which are either genetic or densitydependent (e.g. number of larvae dosed or presence of adult worms). Horak (18), however, proposed a different approach to the subject of arrested development. He included 2 types of inhibition, nonspecific and seasonal arrested development. The latter is C:lefined as occurring annually during the same season and is generally dependent upon the nematodes affected being adapted to a particular environment (Horak, 18; 183). He suggested that these nematodes were susceptible to 1 or several seasonal external environmental stimuli acting upon the infective larvae and resulting in arrest in a later stage of development. We are in agreement with Horak (18, 183), as the arrested larval development in the zebras is seasonal. The numbers of larvae and adult nematodes recovered from the 2 zebra host species differ, and therefore each responds to the cues that result in the arrested devel. opment of L 4 cyathostomes. ACKNOWLEDGEMENTS The authors wish to thank the University of Pretoria for fmancial assistance; the late Dr J. M. Hofmeyr for his cooperation and his staff for their assistance throughout this study; the Department of Agriculture and Nature Conservation of South West Afric8/Namibia; Drs An de Ruyck, Robin Kirkpatrick, Martin Schulman, Mr. L. de Villiers, Dr H. C. Biggs of the Directorate of Veterinary Services, Mrs Dagmar Rautsch and Mr N. Anthonissen of the Central Veterinary Laboratory, Mr Jan le Roux, Mr. T. E. Krecek and Mmes Daleen Lombard and Bonny Roper for technical assistance. REFERENCES BERRY, H. H., 18. Behavioural and ecophysiological studies on blue wildebeest (Connochaetes taurinus) at the Etosha National Park. Ph.D. thesis, University of Cape Town. 8ULENOER, C. L., 12 a. Sclerostomes of the donkey in Zanzibar and East Africa. Parasitology, 12, BOULENOER, C. L., 12 b. On some nematode parasites of the zebra. Parasitology, 12,817. CRAM, ELOSE B., 124. A new nematode, Cylindropharynx ornata, from the zebra, with keys to related nematode parasites of the Equidae. Journal of Agricultural Research, 28, 66H572. GESS, W., 171. A preliminary vegetation map of South West Africa. DinteriJJ, 4, 514.
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The strongylids and other nematodes parasitic in the intestinal tract of South African equines. Report of the Director of Veterinary Education and Research, Union of South Africa, 11, YEH, LANGSHENG, 15. A revision of the nematode genus Setaria Viborg, 175, its hostparasite relationship, speciation and evolution. Journal of Helminthology, 33, 18. YORKE, W. & MAcFE, J. W. S., 118. Strongylidae in horses. ll. Cylicostomum minutum sp. n. Annals of Tropical Medicine & Parasitology, 11, 454. YORKE, W. & MACFE, J. W. S., 12. Strongylidae in horses. Xll. Cylindropharynx rhodesiensis sp. n. Annals of Tropical Medicine & Parasitology, 15, Printed by the Government Printer, Private Bag X85, Pretoria, 1. 78
Introduction. Elizabeth N. Wambwa 1, *, W.O. Ogara 2, Dennis Mudakha 1
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