Ticks associated with the three largest wild ruminant species in southern Africa

HORAK, I.G., GOLEZARDY, H. & UYS, A.C. 2007. Ticks associated with the three largest wild ruminant species in southern Africa. Onderstepoort Journal of Veterinary Research, 74:231–242 The objective of this study was to assess the host status of the three largest southern African wild ruminants, namely giraffes, Giraffa camelopardalis, African buffaloes, Syncerus caffer, and eland, Taurotragus oryx for ixodid ticks. To this end recently acquired unpublished data are added here to already published findings on the tick burdens of these animals, and the total numbers and species of ticks recorded on 12 giraffes, 18 buffaloes and 36 eland are summarized and discussed. Twenty-eight ixodid tick species were recovered. All stages of development of ten species, namely Amblyomma hebraeum, Rhipicephalus (Boophilus) decoloratus, Haemaphysalis silacea, Ixodes pilosus group, Margaropus winthemi, Rhipicephalus appendiculatus, Rhipicephalus evertsi evertsi, Rhipicephalus glabroscutatum, Rhipicephalus maculatus and Rhipicephalus muehlensi were collected. The adults of 13 species, of which the immature stages use small mammals as hosts, namely Haemaphysalis aciculifer, Hyalomma glabrum, Hyalomma marginatum rufipes, Hyalomma truncatum, Ixodes rubicundus, Rhipicephalus capensis, Rhipicephalus exophthalmos, Rhipicephalus follis, Rhipicephalus gertrudae, Rhipicephalus lounsburyi, Rhipicephalus lunulatus, Rhipicephalus pravus group and Rhipicephalus simus, were also collected.

ple more of these large herbivores has arisen and the present paper reports the results of the latter collections.However, since we thought it unlikely that, in the near future, similar exhaustive tick collections would be made from such large animals in southern Africa, we decided to combine the earlier published data with the more recent findings in order to give a more comprehensive overview of the numbers and species of ticks that may infest giraffes, African buffaloes and eland in a variety of habitats.
Giraffes occur in several associations of dry savanna, varying from scrub to woodland.They do not occur in forest or desert and generally are not found in open plains.They are present in north-eastern Limpopo and Mpumalanga Provinces, South Africa, and in the north-eastern parts of Namibia (Skinner & Smithers 1990), but in recent times have been introduced into a number of regions in South Africa in which they previously did not occur.
African buffaloes prefer savanna-type habitats and need a plentiful supply of grass, shade and water.They occur in herds, which increase in size in the dry season, but become more fragmented during the wet season because of the usual plentiful supply of water and grazing (Skinner & Smithers 1990).The current distribution of African buffaloes in South Africa is mostly patchy.Large numbers are present in the Kruger National Park (KNP) and the Hluhluwe-iMfolozi Park in the north-eastern regions of the Limpopo, Mpumalanga and KwaZulu-Natal Prov inces, with smaller populations in national, provincial and privately owned reserves in these and nearly all other provinces of South Africa.
Eland are gregarious animals usually occurring in small herds, and are as at home in arid semi-desert scrub associations as they are in montane grassland (Skinner & Smithers 1990).Historically they were present virtually throughout South Africa, but overexploitation reduced their numbers.However, because they are a sought after species, reintroductions have resulted in their now occupying virtually the same regions in which they originally occurred.
One of the serious shortcomings of the past and current studies is that they are biased towards localities and seasons at which animals were, or have been, made available for survey purposes and are thus not necessarily representative of the entire ixodid tick fauna present within the geographic distribution of the host species being examined.Nevertheless a remarkably large number of tick species were recovered.Moreover, because of the large size of the hosts, large numbers of adult ticks were collected (Gallivan & Horak 1997), and the greater certainty with which the adult ticks can be identified has augmented the accuracy of our identification of the immature stages, and hence our results.

MATERIALS AND METHODS
The localities at which animals were examined, includ ing those of the earlier studies of Horak et al. (1983Horak et al. ( , 1991aHorak et al. ( , 1992a)), Rechav et al. (1987) and Zieger et al. (1998), are summarized in Table 1.With the exception of Free State and Gauteng Provinces at least one of the three large wild ruminant species was sampled in each province of the Republic of South Africa.In addition, six of the giraffes were exam ined in the Etosha National Park in northern Namibia (Horak et al. 1992a), and two of the eland on a game ranch in Central Province, Zambia (Zieger et al. 1998).
Ticks were recovered from the animals in the earlier surveys as described by the authors of those studies.The carcasses of giraffes, African buffaloes and eland in the present surveys were processed for tick recovery and the ticks identified and counted as described by Horak, Boomker, Spickett & De Vos (1992b).When animals had been immobilized, and not killed, an attempt was made to collect as many adult ticks as possible, with particular attention being paid to the preferred sites of attachment of the various species.
A total of 12 giraffes, 18 African buffaloes and 36 eland were examined, but in the tables devoted to each host species only the results for those animals sampled within a particular tick species' distribution range are given for that particular tick.

RESULTS AND DISCUSSION
The species and numbers of ticks collected from the giraffes, buffaloes and eland are summarized in Tables 2, 3 and 4, and the total numbers of male and female ticks recovered and, where it was possible to calculate this, the ratio of males to females for each species are summarized in Table 5.
A calculated total of 450 709 ticks, belonging to 28 species and three subspecies, were collected from the 66 animals examined.Of these 57 688 were adults, of which at least half were identified and counted.Although this may seem like a large number of ticks, probably three times as many would have been recovered had the digestion technique of Van Dyk & McKenzie (1992) been used.However, the fine structures of tick larvae and nymphs are often damaged during the period of digestion required in the latter technique, and thus, although tick recovery may be more complete, it is achieved at the expense of accurate species determination.
Two of the 28 species recovered are one-host ticks, namely Margaropus winthemi and Rhipicephalus (Boophilus) decoloratus.Five are two-host ticks, these being Hyalomma glabrum, Hyalomma marginatum rufipes, Hyalomma truncatum, Rhipicephalus glabroscutatum and Rhipicephalus evertsi of which both subspecies of the latter, namely evertsi and mimeticus were collected.The remaining 21 species are all three-host ticks.With the exception of ticks of the I. pilosus group and I. rubicundus, of which more females than males were recovered, considerably more males than females of all other species, of which both sexes were present, were collected.Mating in Ixodes species may occur in the preparasitic phase of the life cycle (Fourie & Horak 1994), and many males thus never attach.This behaviour is probably largely responsible for the female-biased parasitic populations of the two ticks in this genus in the present study.The male-biased populations of the other tick species is due to the propensity of parasitic male ixodid ticks of several species to spend extended periods on their hosts (Londt 1976;Jordaan & Baker 1981), whereas the females may require only a few days to two weeks to mate and engorge before detaching.Furthermore the larger size of engorging females is likely to make them more susceptible to removal by grooming or predation than the considerably smaller males.

Amblyomma species
The larvae of Amblyomma hebraeum infest a wide variety of hosts, including ungulates, carnivores, lago morphs and birds, and all stages of development, but particularly the adults, infest very large hosts (Horak, MacIvor, Petney & De Vos 1987a).
The males may remain attached for several months (Jordaan & Baker 1981), thus augmenting the already male-biased population of adult ticks.Ambly- Amblyomma marmoreum is known as the South African tortoise tick, and all stages of development may be found on a variety of these reptiles, with leopard tortoises, Geochelone pardalis, generally the most heavily infested (Horak, McKay, Heyne & Spickett 2006).The larvae infest a wide variety of mammals and birds, and are often found on mammals and birds of several species that are present within the tick's distribution range (Horak et al. 2006).

Amblyomma variegatum does not occur in South
Africa, but is present in most sub-Saharan countries to the north (Walker & Olwage 1987).Its host spectrum is similar to that of A. hebraeum and its presence on the two eland examined in Zambia is thus to be expected.

Haemaphysalis species
The two male Haemaphysalis aciculifer recovered from an eland in the KNP during September 1979 (Horak et al. 1983; Table 4), were the only specimens of this species reported in the park until 2000, when Horak, Braack, Fourie & Walker (2000) recorded 13 males and two females from a honey badger, Mellivora capensis.This tick is seldom recovered in large numbers but appears to be present in north-eastern Mpumalanga Province and thence along the eastern and southern coastal and adjacent inland regions to the south-western region of the Cape Province (Theiler 1962;Horak, Keep, Spickett & Boomker 1989;Horak & Boomker 1998).
Haemaphysalis silacea is present in north-eastern KwaZulu-Natal and in the Eastern Cape Provinces (Walker 1991), and is associated with vegetation classified as Valley Bushveld (Acocks 1988) and with greater kudus, Tragelaphus strepsiceros, common duikers, Sylvicapra grimmia, Cape grysbok, Rhaphicerus melanotis, and helmeted guineafowls, Numida meleagris (Horak & Knight 1986;MacIvor & Horak 2003).Seven of the 18 buffaloes and all four eland examined in Valley Bushveld-type vegetation in the north-eastern KwaZulu-Natal and the Eastern Cape Provinces were infested.
Hyalomma species Delpy (1949) described the tick now known as Hyalomma glabrum as Hyalomma rufipes glabrum, and the latter name persisted until Theiler (1956) raised it to species level as Hyalomma glabrum.In the same year Hoogstraal (1956) synonymized it with Asian Hyalomma marginatum turanicum, and since then it has been considered identical to the latter tick.Recent studies have, however, revealed that it is a separate taxon, and Apanaskevich & Horak (2006) have subsequently reinstated it as Hyalomma glabrum.Howell, Walker & Nevill (1978) have illustrated its distribution (as H. m. turanicum) in the central and western regions of South Africa.The adults prefer large animals such as eland and Cape mountain zebras, Equus zebra zebra, and its immature stages infest scrub hares, Lepus saxatilis, and ground-frequenting birds (Apanaskevich & Horak 2006).The distribution of Hyalomma marginatum rufipes is more extensive than that of H. glabrum, which it almost entirely overlaps (Howell et al. 1978).Its host preferences are the same as those of the latter tick (Walker 1991), but include giraffes and buffaloes, which are generally not present within the distribution range of H. glabrum (Tables 2 and 3).
With the exception of the eastern coastal regions and some adjacent inland areas and the southern coastal regions, Hyalomma truncatum is present virtually throughout the country (Howell et al. 1978).
The adults are found on the same large hosts as the former two ticks, and its immature stages infest scrub hares and rodents (Walker 1991).

Ixodes species
Ticks of the Ixodes pilosus group are present in the southern coastal and adjacent regions of the Western and Eastern Cape Provinces and in southeastern KwaZulu-Natal Province, where all stages of development may be encountered on antelopes, caracals, Caracal caracal and domestic dogs (Horak, Jacot Guillarmod, Moolman & De Vos 1987b;Horak et al. 1989;Horak & Boomker 1998;Horak & Matthee 2003).

Margaropus winthemi
This tick is commonly known as the winter horse tick, and its distribution in the cooler higher-lying regions of the country suggests that its original hosts Total (excluding Ixodes spp.) 42 805 14 682 2.92 1.0 were Cape mountain zebras, on which it still occurs in very large numbers during the winter months (Horak et al. 1991a).The burdens of the eland (Table 4), examined at the same time as zebras in the Mountain Zebra National Park, although large, did not nearly approach those of the latter animals.

Rhipicephalus species
Rhipicephalus (Boophilus) decoloratus.Using molecular analyses supported by an analysis of morphological characters Murrell, Campbell & Barker (2000) and Beati & Keirans (2001) decided that the genus Rhipicephalus is paraphyletic with respect to the genus Boophilus and consequently Murrell & Barker (2003) proposed the use of the above nomenclature.
We have chosen to follow their proposal, although many people prefer to retain Boophilus as a generic name.Giraffes and eland can generally be considered as good hosts of this tick, whereas Afri can buffaloes appear to be resistant to infestation, with more than half of the adult ticks reported here coming from a single, approximately 6-month-old calf.Norval (1984) and Horak, Golezardy & Uys (2006) have discussed the apparent resistance of African buffaloes to artificial and natural infestations with this tick, and it would seem that this resistance is acquired, rather than innate.
Adult Rhipicephalus appendiculatus are common parasites of African buffaloes, eland, greater kudus, male nyalas, Tragelaphus angasii, and domestic cattle in wooded savannas from south-eastern South Africa in the south to Kenya and Uganda in the north (Walker, Keirans & Horak 2000).The immature stages are found on the same hosts as the adults, but also infest smaller antelopes and scrub hares (Walker et al. 2000).The eland included in the present study and more particularly those from Zambia, were heavily infested with adult ticks (Table 4).The buffaloes, which were examined mainly during the early winter months, harboured very large numbers of larvae (Table 3).
Excluding the deserts and regions of high rainfall, the former tick is found throughout sub-Saharan Africa, whereas the latter is confined to the arid and semi-arid regions of Namibia, western Botswana and parts of Angola (Walker et al. 2000).
The adults of Rhipicephalus exophthalmos parasitize antelopes, domestic ruminants and scrub hares in the south-eastern and north-western regions of South Africa and in a broad, central band from the south to the north of Namibia (Walker et al. 2000).Its immature stages prefer elephant shrews, El ephantulus spp., as hosts (Fourie et al. 2005).
The two-host tick, Rhipicephalus glabroscutatum, is present in the fynbos and Karoo regions of the Western Cape Province, and also in the Karoo and the Valley Bushveld regions of the Eastern Cape Province (Walker et al. 2000).It is a common parasite of the feet and lower legs of small and large antelope in these regions (Horak & Boomker 1998;MacIvor & Horak 2003).Infestation with its adults is a contributory cause of foot abscess in domestic goats in the Valley Bushveld regions of the Eastern Cape Province (MacIvor & Horak 1987).
The distribution in South Africa of Rhipicephalus maculatus and Rhipicephalus muehlensi is confined to the coastal bush and adjacent inland regions of north-eastern KwaZulu-Natal (Walker et al. 2000).
The recovery of an R. maculatus nymph from the vegetation and adults from an elephant, Loxodonta africana, in the southern regions of the KNP (Braack, Maggs, Zeller & Horak 1995), and of R. muehlensi adults from one of the buffaloes examined in the Mtethomusha Nature reserve, just south of the KNP, suggest that they have been introduced into these reserves on animals translocated from north-eastern KwaZulu-Natal.All stages of development of both ticks may infest the same host species, but the adults of R. maculatus prefer thick-skinned animals such as buffaloes and bush pigs, Potamochoerus larvatus, and those of R. muehlensi nyalas (Horak, Boomker & Flamand 1991b;1995).
Rhipicephalus longiceps is a rarely encountered tick and apparently is present only in certain regions of Namibia and Angola (Walker et al. 2000).
Rhipicephalus lounsburyi prefers the higher mountainous regions of the Eastern Cape Province (Walker et al. 2000) and two eland in the Mountain Zebra National Park were infested.The adults attach around the feet of their antelope and sheep hosts, while the only known hosts of its immature stages are four-striped grass mice, Rhabdomys pu milio, from which a larva and two nymphs have been collected (Walker et al. 2000;Horak, Fourie & Braack 2005).
Although Rhipicephalus lunulatus is fairly widespread in sub-Saharan Africa its distribution in South Africa is limited to the eastern regions (Walker et al. 2000).The adults have a wide host range and would seem to attach around the feet and lower legs of their hosts (Walker et al. 2000).The eland examined in Zambia had fairly large burdens of adult ticks (Table 4), while a multimammate mouse, Mastomys sp., and a scrub hare examined on the same ranch as the eland were infested with nymphs (Zieger et al. 1998).
Ticks belonging to the Rhipicephalus pravus group have been collected from scrub hares in the KNP (Horak, Spickett, Braack & Penzhorn 1993), and were assigned to Rhipicephalus sp.near pravus by Walker et al. (2000).However, the ticks collected in the same park from three of the giraffes, appear to us to be very similar, if not identical to the true R. pravus of East Africa.
The immature stages of Rhipicephalus supertritus are unknown, but are assumed to be similar in appearance to those of R. appendiculatus.It is apparently commonest in Central Africa, including northern Zimbabwe and Mozambique, parts of Zambia and southern Tanzania (Walker et al. 2000), and both eland examined in Zambia were infested.

TABLE 1
Localities at which large wild ruminants were examined for ixodid ticks

TABLE 2
Giraffes examined and the number infested within the distribution range of each tick (Walker & Olwage 1987)alker & Olwage 1987).

TABLE 3
African buffaloes examined and the number infested within the distribution range of each tick

TABLE 4
Eland examined and the number infested within the distribution range of each tick

TABLE 5
Male to female ratios of tick species collected from giraffes, African buffaloes and eland in southern Africa Rhipicephalus capensis occurs almost exclusively in the western coastal regions of the West ern Cape Province, South Africa; R. gertrudae is present in the same western regions, but its distribu tion extends east to the southern and southern-central regions of the country and north into Namibia; R. follis is only found in South Africa and is present to the east and north-east of R. gertrudae's distribution range and generally in mountainous terrain; while, with the exception of the more arid regions of central and western South Africa and southern Namibia, the distribution range of R. simus effectively overlays those of the other three species and extends north into Africa to a latitude of approximately 9° south.