New host–parasite associations included Trichostrongylus deflexus from blue wildebeest, Agriostomum gorgonis from black wildebeest, Stilesia globipunctata from the waterbuck and Fasciola hepatica in a kudu. The mean helminth burden, including extra-gastrointestinal helminths, was 592 in impalas, 407 in kudus and blue wildebeest, 588 in black wildebeest, 184 in gemsbok, and 2150 in the waterbuck. Excluding Probstmayria vivipara, the mean helminth burden in warthogs was 2228 and the total nematode burden in the bushpig was 80. The total burdens and species richness of the helminths in this study were consistently low when compared with similar studies on the same species in areas with higher rainfall. This has practical implications when animals are translocated to areas with higher rainfall and higher prevalence of helminths.

Little work has been conducted on the helminth parasites of artiodactylids in the northern and western parts of the province. The aims of this study were to determine the species and numbers of helminth that occur in different wildlife hosts in the area, and to determine whether any zoonotic helminths were present. Tothis end, a total of 37 animals from various localities in the Limpopo province were examined and their parasites identified and counted.

Materials

The western parts of the province are semi-arid and the vegetation type varies between Sweet Bushveld and Mixed Bushveld (Acocks 1988). Rainfall from July 2006 to July 2007 in the Lephalale area was 178 mm (South African Weather Service 2007). The summers are hot and the winters cool.

Carcasses that were destined for export were not skinned until they reached the abattoir. No incisions were made into the muscles, except for the masseter and the diaphragm. The heads and capes of animals hunted for trophies were preserved; therefore, no incisions of the masseter muscles or tongues could be made. The intestinal helminths as well as those in the heart, lungs and liver of the antelopes were collected as described by Boomker, Horak and De Vos (1989) but digests of abomasal and intestinal mucosae were not performed. Depending on the volume of ingesta of the different parts of the gastrointestinal tract, aliquots of a quarter, a tenth or a 25th were made and examined. The entire abomasal content of the bushbuck (Tragelaphus scriptus) was examined.

The helminths of warthogs and the bushpig (Potamochoerus porcus) were recovered as described by Boomker et al. (1991a). In addition, muscle samples from the diaphragm and intercostal and masseter muscles were crushed (between glass slides) and examined under a stereoscopic microscope for the presence of Trichinella spp.

Live adult cestodes were relaxed in water in Petri dishes. Once all movement had ceased they were fixed in 5% formalin for 24 h and further preserved in 70% ethyl alcohol. Scoleces were dissected out of the metacestodes and mounted en face in Berlese’s fluid under slight pressure from a cover slip. Adult cestodes were stained in carmalum or Mayer’s acid haemalum, cleared in xylene and mounted on glass slides in Canada balsam (Gibbons, Jones & Kahlil 1996).

Cooperia hungi was most prevalent, followed by Impalaia tuberculata, Oesophagostomum columbianum and Trichostrongylus deflexus. Haemonchus krugeri had the highest mean intensity (375 worms), followed by C. hungi (280 worms) and I. tuberculata (140 worms).

Impala and their parasites have been studied by several authors and some significant contributions have been made by Anderson (1992), Heinichen (1973), Horak (1978, 1980, 1981) and Mönnig (1933) in South Africa and Gallivan et al. (1989) in Swaziland. Because of their feeding ecology, impala are exposed to the helminths of both browsers and grazers. Impala also share pastures with domestic livestock on many game ranches in South Africa and considerable overlap between thehelminth fauna of sheep, cattle and impalas occurs (Horak 1978).

Cooperia hungi is considered a definitive parasite of impalas and the other nine nematode species all occurred in five or fewer animals, which classifies them as eitheroccasional or accidental parasites (Horak 1980).

In Horak’s (1978) study on impala at Nylsvley, more than 90% of the worms were retarded in the fourth stage at different times of the year. As digests were notcarried out in this study, the recovery rate of larval stages was low, which may account for the low total helminth counts. The harsh environment in the northern and western parts of the Limpopo province would necessitate helminth parasites to employ strategies to protect the vulnerable, free-living larval stages, not only during winter when temperatures and rainfall are low, but also during summer, when temperatures are high and rainfall often low. Owing to the higher rainfall and milderclimate at Nylsvley it is doubtful whether the same levels of larval retardation exist for worms in the current study area.

The relatively few helminth species recovered could also be due to a smaller diversity of antelope species in the sampling areas. Where a large number of antelopespecies are present, cross-transmission can take place more readily (Boomker, Anthonissen & Horak 1988), which increases the diversity of parasite species.

Although two impalas from Nwanedi in the Soutpansberg had eosinophilic granulomata in the lungs, no parasites were recovered from these lesions. The mostcommon gross lesions associated with the lungworm Pneumostrongylus calcaratus in impalas in Swaziland were firm nodules along the lateral borders of the caudal lung lobes (Gallivan et al. 1989). Those authors recorded an 85% prevalence of this nematode in impalas in Mlawula Nature Reserve, Swaziland. Pneumostrongylus calcaratus has been found to be prevalent in the eastern Transvaal Lowveld (now Limpopo and Mpumalanga) as indicated by Ortlepp (1962) and Young and Wagener(1968), and in the northern part of KwaZulu-Natal (Anderson 1992). Young and Wagener (1968) found a high prevalence in impala in the southern Kruger National Park, whereas Horak (1978, 1980) did not recover lungworms from impalas at Nylsvley Nature Reserve or from Pafuri in the northern Kruger National Park. Horak (1981) ascribed this difference in prevalence to climate. He suggested that Pneumostrongylus is restricted to warm, moist regions, where the mollusk intermediate host(Urocyclus [Elisolimax] flavescens) occurs.

The kudu with the highest burden had 2690 worms, of which 2425 were Haemonchus contortus. Excluding this kudu, the mean burden for the remaining seven kuduswas 81 worms. This is a classical example of overdispersion of the parasites. The lowest burden was six worms, comprising the two species Elaeophora sagitta and Fasciola hepatica, which both use intermediate hosts. The mean helminth burden, including E. sagitta and F. hepatica, was 407 worms.

Haemonchus contortus was the most prevalent worm and was recovered from six of the eight kudus, followed by E. sagitta recovered from three kudus.

According to the criteria of Horak (1980), Haemonchus vegliai, Cooperia neitzi, Cooperia acutispiculum, E. sagitta and T. deflexus are definitive parasites of kudus in theKruger National Park (Boomker et al. 1989) and in the Eastern Cape (Boomker, Horak & Knight 1991b). The amphistomes, Schistosoma mattheei, Moniezia benedeni, Taenia larvae, I. tuberculata, Agriostomum gorgonis and Strongyloides papillosus are considered occasional parasites in kudu (Boomker et al. 1991b).

Kudus are known to harbour parasites from other species of antelopes. Boomker et al. (1991b) found that kudus in the Addo Elephant National Park harbouredNematodirus helvetianus and Dictyocaulus spp., thought to originate from cattle in the area. The H. contortus recovered in the current study probably originated from goats. Cooperioides hamiltoni, a parasite described from impalas, was recovered from kudus in this study and is considered an occasional parasite of kudus (Boomkeret al. 1988).

Except for one kudu from the Soutpansberg area, the helminth burdens were relatively low but the range was similar for that of kudu sampled in the Etosha GameReserve (Boomker et al. 1988) and the Eastern Cape (Boomker et al. 1991b). This is in contrast to kudus sampled in the Kruger National Park (Boomker et al. 1989), which showed much higher burdens. The kudus were mainly from the southern region of the park, which has an annual rainfall of 600 mm – 700 mm. The dry climate of the localities in the present study area is more similar to that in Etosha and the Eastern Cape and is too harsh for the survival of the free-living infectivestages of helminths (Boomker et al. 1989).

Of the helminths considered definitive parasites of kudu in the Kruger National Park (Boomker et al. 1989) only C. neitzi and E. sagitta were recovered from the kudus in this study. However, C. neitzi was recovered only in one kudu and in small numbers. Elaeophora sagitta was recovered from three kudus from two of the localities in this study and also not in significant numbers. Their presence is an indication of the abundance of their intermediate host (Boomker 2007).

Because kudus are browsers and roam considerably they are subject to reinfection with their own parasites only to a limited extent (Boomker, Horak & De Vos 1986). However, animals that roam are more likely to become infected with accidental parasites (Horak 1980). Agriostomum gorgonis and Oesophagostomum spp. are considered accidental parasites as they occurred only in one kudu each and in low numbers.

The highest total burden in an animal was 550 worms. The mean helminth burden of the four blue wildebeest was 407 worms. The species with the highest intensity was H. contortus (500 per individual), followed by Haemonchus bedfordi (375 per individual). This parasite appears to be common in blue wildebeest and has been recovered from animals from the Kruger National Park (Horak, De Vos & Brown 1983b) as well as from the Kalahari Gemsbok National Park (now Kgalagadi Transfrontier Park) (Boomker et al. 1986).

Cooperia connochaeti was recovered from three of the four blue wildebeest in this study. It is considered a definitive parasite for this species. The seasonal patterns of several parasites of wildebeest from the Kruger National Park have been attributed to a combination of climatic factors and migratory patterns of the wildebeest in the park (Horak et al. 1983b). On small game farms animals generally have limited migration patterns and therefore the risk of becoming reinfected from the contaminated pastures increase.

The helminths of black wildebeest have received little attention (Boomker et al. 2000). Wildebeest appear to be fairly resistant to parasitic infections, as animals fromthe Golden Gate Highlands National Park and Rietvlei Nature Reserve harboured relatively low burdens of only a small number of helminth species when compared with blue wildebeest from the Kruger National Park (Horak et al. 1983b). In an earlier study, Boomker et al. (2000) found that a black wildebeest from the Mountain Zebra National Park harboured a single Taenia sp. larva, 26 Haemonchus spp. females and one Haemonchus spp. larva. Neither of two black wildebeest from the KarooNational Park sampled during that study harboured any worms (Boomker et al. 2000).

The larval stages of T. hydatigena were found attached to the mesenterium and liver of all three gemsbok. The T. hyaenae larvae occurred in the triceps and heartmuscles. The metacestodes were identified according to the number and size of their rostellar hooks (Verster 1969).

Although gemsbok are relatively common in the Limpopo province, they are historically not endemic to this region. The translocation of antelopes to climatic orvegetation regions where they did not occur historically can be hazardous to their health (Boomker et al. 2000). Earlier studies found the total helminth burden of gemsbok from the West Coast National Park, where the antelopes do not naturally occur, to be 28 681 (Boomker et al. 2000), compared with 5877 for gemsbok from the Kalahari Gemsbok National Park (now Kgalagadi Trasfrontier Park) (Boomker et al. 1986). The high burden for gemsbok in the West Coast National Park isattributed to the climatic conditions in the area, as the climate appeared to favour parasites but caused stress in the gemsbok (Boomker et al. 2000). In the Limpopo province the climate is rather similar to that of the Kalahari, which may be the reason for the small numbers of helminths recovered from gemsbok in the present study.

The helminth with the highest intensity was P. vivipara, with burdens ranging between 276 000 and 825 000 per host. The helminth with the second highest intensity was O. mwanzae, with a total burden of 3700 recovered from one warthog.

The highest total helminth burden that included P. vivipara, was 825 940 including for warthog BWh1. However, warthog BWh3 had the highest helminth burden (5920) that excluded P. vivipara.

No Trichinella were found in any of the carcasses.

Four of the warthogs originated from Bushman’s Safaris, two of which were examined in August 2006 and two in August 2007. The two warthogs from the 2006 sample harboured Murshidia spp. but no O. mocambiquei, but the converse was true for the warthogs examined in 2007. The two warthogs sampled in 2006 also had lower total helminth burdens (excluding P. vivipara), namely 162 and 702, respectively. The warthogs sampled in 2007 had total burdens (excluding P. vivipara) of 5920 and 4810, respectively. It is possible that although Lephalale had below-average rainfall during the 2006/2007 season, rain during the dry season in 2007 could have affected the abundance of parasites in the region.

The helminths of warthogs in southern Africa have been described by several authors, including Boomker et al. (1991a), Horak et al. (1983a, 1988) and Ortlepp (1964). The helminth parasites of warthogs as listed by Round (1968) include parasites from across Africa. However, many helminths occur only in certain regions as is evident from the work of Ortlepp (1964), Horak et al. (1983a, 1988) and Boomker et al. (1991a).

The total worm burden of the bushpig was low compared with that of warthogs. Ortlepp (1964) made no note of the burdens of the worms he recovered from bushpigs. Because only one animal was examined, a low burden due to underdispersion could not be ruled out.

Little work has been conducted on the helminth parasites of bushpigs. Ortlepp (1964) examined material from Mozambique and the northern Transvaal (now Limpopo), which has been included in the list of helminth parasites of Round (1968). Bushpigs are difficult to sample because of their largely nocturnal activity andtheir relatively limited distribution in forested areas.

In the present study, C. hepaticae was recovered from only two impalas and both had very small burdens. One reason for the low prevalence and intensity could bethat the animals sampled were all adults and thus would have had an acquired immunity. Also, the animals were all sampled before the start of the rainy season and therefore the peak burdens of this parasite might have been missed. The dry climate of the study area will affect the survival of free-living stages of the parasites.

At Langgedachte, H. contortus was collected from three blue wildebeest and three kudus. At this game farm, domestic livestock and game are kept together.Haemonchus contortus is considered a parasite of domestic animals and the high prevalence is possibly due to cross-transmission from domestic animals and the high stocking densities on the farm.

Both O. mwanzae and O. mocambiquei have been recovered from warthogs from Hoedspruit (Boomker et al. 1991a), the Kruger National Park (Horak et al. 1988) and Pilgrim’s Rest (Ortlepp 1964). Both species were also recovered in this study from animals that originated from the Musina and Lephalale areas. It would appear thatthese are the only two Oesophagostomum species that occur in warthogs in the Limpopo and Mpumalanga provinces. Although O. mwanzae is the dominant of the two species, both can be considered definitive parasites of warthogs in the area.

Many Trichuris spp., of which T. globulosa is the most widespread, have been reported to occur in antelopes in southern Africa (Ortlepp 1937). Trichuris spp. are of greater concern in enclosures and zoos than in open spaces owing to their monoxenous life cycle and thick-shelled eggs (Boomker 2007). Environmental build-up ofthe parasite is not likely to happen in a free-range system.

In this study Stilesia hepatica was recovered from only one impala. Gallivan et al. (1996) reported no difference between seasons or sexes, but in their study adult animals had larger burdens, possibly indicating that it is an accumulative infection.

Taenia hyaenae utilises many ruminant species as intermediate hosts. The definitive hosts for this species are hyaenas and African wild dogs (Lycaon pictus) (Loos-Frank 2000). Spotted hyaenas, brown hyaenas (Hyaena brunnea), African wild dogs, black-backed jackals and leopards (Panthera pardus) are all known to frequent the farm from which these gemsbok came. Cysticerci that resemble this species in the number and shape of the rostellar hooks have previously been recovered from impalasand sable antelopes (Hippotragus niger) (Verster 1969). Macroscopically it cannot be distinguished from the cysticerci of other Taenia spp., including Taenia saginata. Only microscopically can T. saginata be identified by the absence of rostellar hooks, an important consideration during meat inspection. Humans are the definitive hosts for the latter cestode, which has been recovered from various game species. Larval T. saginata has been found in several hosts in Africa; for example Graber(1959) found the species in Dorcas gazelles (Gazella dorcas), red-fronted gazelles (Gazella rufifrons) and Gazella spp. in Chad, Le Roux (1937) observed it in oribis (Ourebia ourebi) in Zambia, Sousa Dias (1950) found it in Cape buffaloes (Syncerus caffer) in Angola and Nelson, Pester and Rickman (1965) in bushbuck in Kenya. Also, the metacestodes of Taenia solium have been found in warthogs in Africa (Bain 2001) and in wild boars (Sus scrofa) in Europe (Eslami & Farsad-Hamdi 1992). Itis evident that there is a potential public health risk associated with the consumption of venison infected with metacestodes.

Hydatid material of human origin collected in sub-Saharan Africa all conform to the sheep strain of E. granulosus (MacPherson & Wachira 1997). However, this doesnot prove non-infectivity of other E. granulosus strains, species or subspecies to humans. Because of the seriousness of Echinococcus spp. infection, meat inspection should be thorough and the necessary precautions should be taken when handling carnivores (Young 1975).

The Nwanedi Nature Reserve, where the infected kudu was examined, has a large dam that is fed by the Nwanedzi river. This creates a favourable environment for the freshwater snail that serves as intermediate host to the flukes. Domestic stock have previously had access to the reserve and are currently kept upstream from the dam, which could be a possible source of contamination. Wildlife that have been introduced to the reserve are other possible sources. Fasciola gigantica is the most common liver fluke in domestic ruminants in Africa and accounts for most liver fluke infections in wild animals (Hammond 1972).

For the study area as a whole, comparisons with other studies provided valuable information. The total burdens and species variation of especially the adult helminths in this study were consistently lower compared with studies in areas with higher rainfall.

The only trematode recovered was F. hepatica from a kudu at Nwanedi. The dry climate is not conducive to the survival of freshwater snails that act as intermediatehosts. These parasites typically occur in areas with wetter or more humid conditions.

There are practical implications for the low prevalence and species variation of helminths. When animals are translocated from the drier parts of the Limpopoprovince to areas with higher rainfall, they will be relatively naive to the higher parasite loads in those areas and/or completely naive to other parasites, such as lungworms. On the other hand, animals originating from areas with higher rainfall are likely to harbour higher parasite loads. They should be dewormed prior to translocation to dry areas, because the stress of the dry climate and change in vegetation can cause them to succumb to the parasite loads they already harbour. At the same time, new parasites could be introduced, with variable results to the wildlife already present.

Game is kept together with domestic stock on many farms in the province. Helminths that typically occur in domestic stock were recovered from some antelope species. Haemonchus contortus was recovered from all the kudus and blue wildebeest from Langgedachte. High stocking densities of animals on this farm likely contributed to the frequency of cross-transmission of parasites between species. With parasites that have a high fecundity, such as Haemonchus or Oesophagostomum, environmental build-up may become considerable under certain conditions or specific times of the year. This will impact on worm control programmes for domestic animals, but may also cause morbidity in game at times.

Some parasites are more problematic in intensive situations, for example when animals are kept in a boma or very small camps. This is especially true for parasites with a monoxenous life cycle such as Trichuris spp. Animals that are kept intensively should be dewormed to prevent environmental build-up of the parasite. Under extensive conditions, these parasites are unlikely to cause any problems.

The only known zoonotic helminth recovered was E. granulosus from the lungs of a warthog. The infective stage for humans is the egg that is deposited by the final host – dogs – which are often fed uncooked offal. One should be aware that the parasite can become established in the local human population through this route, especially in communal areas where people live in close association with their animals.

Cysticerci of T. hyaenae and T. hydatigena were recovered from the gemsbok. Although these tapeworms are not known to be zoonotic, the cysticerci are notmacroscopically distinguishable from the zoonotic cysticeri of T. solium or T. saginata. This has public health implications because the cysticerci render the meat aesthetically unacceptable and, in addition, a lack of proof of non-infectivity does not prove that these cestodes are not in fact infective to humans.

The host species included in the study are some of the more common ones that occur on game farms in the Limpopo province. The parasites of many wildlife species, including relatively common species such as giraffes (Giraffa camelopardalis), common reedbuck (Redunca arundinum) (Boomker et al. 1984) and grey rhebuck (Pelea capreolus) (see Boomker et al. 2000) but also scarcer game such as red duikers (Cephalophus natalensis) (see Boomker et al. 1984), have not been studied extensively, particularly in the Limpopo province. Because these animals all share the same, mostly confined environment, scientific game farming practices require more knowledge on the parasites, including the helminths, of these species.