Small mammals as hosts of immature ixodid ticks

HORAK, I.G., FOURIE, L.J. & BRAACK, L.E.O. 2005. Small mammals as hosts of immature ixodid ticks. Onderstepoort Journal of Veterinary Research, 72:255–261 Two hundred and twenty-five small mammals belonging to 16 species were examined for ticks in Free State, Mpumalanga and Limpopo Provinces, South Africa, and 18 ixodid tick species, of which two could only be identified to genus level, were recovered. Scrub hares, Lepus saxatilis, and Cape hares, Lepus capensis, harboured the largest number of tick species. In Free State Province Namaqua rock mice, Aethomys namaquensis, and four-striped grass mice, Rhabdomys pumilio, were good hosts of the immature stages of Haemaphysalis leachi and Rhipicephalus gertrudae, while in Mpumalanga and Limpopo Provinces red veld rats, Aethomys chrysophilus, Namaqua rock mice and Natal multimammate mice, Mastomys natalensis were good hosts of H. leachi and Rhipicephalus simus. Haemaphysalis leachi was the only tick recovered from animals in all three provinces.

The adults of some of the tick species that infest these small animals as larvae or nymphs are important vectors of disease or toxins to domestic livestock, whereas others are of little or no economic consequence.Thus murid rodents are among the preferred hosts of the immature stages of Haemaphysalis leachi, whose adults parasitize and transmit canine babesiosis to domestic dogs (Lewis, Penzhorn, Lopez-Rebollar & De Waal 1996), and of Rhipicephalus simus, whose adults parasitize cattle, horses and domestic dogs and transmit anaplasmosis to cattle and produce a toxin causing paralysis in calves and lambs (Walker, Keirans & Horak 2000).Rock elephant shrews, Elephantulus myurus, are the hosts most favoured by the immature stages of Ixodes rubicundus and Rhipicephalus warburtoni, whose adults cause paralysis in sheep and goats (Stampa 1959;Walker et al. 2000), and scrub hares, Lepus saxatilis, by the immature stages of Hyalomma marginatum rufipes and Hyalomma truncatum, whose adults are parasites of domestic cattle, sheep and goats.The former tick transmits anaplasmosis and Babesia occultans to cattle, and the latter secretes a toxin that is the cause of sweating sickness in these animals (Walker, Bouattour, Camicas, Estrada-Peña, Horak, Latif, Pegram & Preston 2003).The objective of the present paper is to present recent data on the ixodid ticks that infest small mammals in three of the nine provinces of South Africa, and to supply the geographic coordinates of the localities at which the ticks were collected for future mapping purposes.

MATERIALS AND METHODS
Two hundred and twenty-five small mammals, belonging to 16 species, were collected in Free State, Mpumalanga and Limpopo Provinces, South Africa and processed for tick recovery as described by Horak et al. (1986).One hundred and sixty-three of these animals belonging to 10 species were examined in Free State Province and 62 belonging to 11 species were examined in Mpumalanga and Limpopo Provinces (Table 1).

RESULTS AND DISCUSSION
The ticks collected in Free State Province are summarized in Tables 2 and 3, and those from animals in the north-eastern regions of Mpumalanga and Limpopo Provinces in Tables 4 and 5.

Dermacentor rhinocerinus
The hosts of the immature stages of this tick were unknown until Horak & Cohen (2001) collected larvae and nymphs from rodents in Mpumalanga Province.For the sake of completeness we have repeated their findings here because other tick species, recovered from the same hosts, were not listed in the earlier publication.Dermacentor rhinocerinus is a host-specific parasite of rhinoceroses (Keirans 1993), of which there are several in the Mthethomusha Reserve, Mpumalanga Province.These animals must have been the source of infestation reflected in the burdens of immature ticks of five of the 38 rodents examined in the reserve (Table 4).There are rhinoceroses in the Willem Pretorius Nature Reserve in Free State Province, but it is not known whether D. rhinocerinus is also present.

Haemaphysalis leachi
Domestic dogs and the larger wild felids are the preferred hosts of adult H. leachi, while its immature stages occur mainly on murid rodents (Norval 1984;Braack et al. 1996;Horak et al. 2000).Its widespread distribution in the present survey confirms Norval's (1984) assertion that provided hosts for its adults and immature stages are present, almost any locality in southern Africa can be regarded as suitable.Furthermore the large range of carnivore and rodent species parasitized by its adult and immature stages, respectively (Norval 1984;Horak et al. 2000; Tables 2 and 4) and their widespread distribution, ensure that should H. leachi be introduced into a region it would readily become established.This assumption is corroborated by its extensive but discontinuous distribution in South Africa (Howell, Walker & Nevill 1978).
Haemaphysalis leachi transmits Babesia canis, the cause of canine babesiosis in domestic dogs in South Africa (Lewis et al. 1996).Judging by the host preferences of the adult and immature stages of the tick it would seem that transmission mostly takes place via the adults with infection passing transovarially from adult ticks of the previous generation without it being lost when the immature stages feed on rodents.

Hyalomma species
The immature stages of H. marginatum rufipes and H. marginatum turanicum infest Cape hares, scrub hares and ground frequenting birds, and those of H. truncatum hares, gerbils and murid rodents (Rechav, Zeederberg & Zeller 1987;Horak & Fourie 1991;Horak et al. 1991;Braack et al. 1996).The distributions of H. marginatum rufipes and H. marginatum turanicum overlap in the southern Free State (Howell et al. 1978), and as we are unable to differentiate between their immature stages we have assigned 259 only the specific epithet marginatum to the ticks collected from hares and a four-striped grass mouse examined in this region.Both hare species were infested with the larvae and nymphs of H. truncatum and three rodent species with only the larvae of this tick.The immature stages of the three Hyalomma ticks are present on their preferred hosts from early autumn to early summer (Horak et al. 1991;1993;Horak & Fourie 1991), and their presence in any study would thus be influenced by the season in which host animals are examined.

Rhipicephalus evertsi evertsi
The small number of rodents infested, and then only with larvae of this two-host tick, indicates that in contrast to hares, on which both larvae and nymphs were present, they are not good hosts.Although a large variety of domestic and wild ruminants are infested with R. evertsi evertsi, the preferred hosts of all stages of development are domestic and wild equids (Walker et al. 2000).

Rhipicephalus gertrudae
This tick replaces R. simus in the winter rainfall regions of south-western Western Cape Province and in the more arid regions of this province and Northern Cape Province as well as in the central and western regions of Free State Province (Walker et al. 2000).Its adult and immature stages have much the same host preference as R. simus, but in addition, the adults seem to favour primates, including humans (Brain & Bohrmann 1992;Walker et al. 2000;Horak, Fourie, Heyne, Walker & Needham 2002).The recovery of its larvae and nymphs only from A. namaquensis and R. pumilio and not from other small mammals within its distribution range does not necessarily reflect a host preference for these species, but may be influenced by the localities and seasons in which the mice were examined.

Rhipicephalus lounsburyi
The higher mountainous regions of the Eastern Cape Province are one of the preferred habitats of this tick (Walker et al. 2000).It has not previously been recorded in Free State Province, but Platberg, the locality at which it was collected from a fourstriped grass mouse, forms part of the same mountain range in which it has been collected in the Eastern Cape Province.The adults attach around the feet of their antelope and sheep hosts, while the only known host of its immature stages is a fourstriped grass mouse, from which a single nymph was collected (Walker et al. 2000).

Rhipicephalus simus
Of all species collected in the two northern provinces, the immature stages of R. simus has the largest host range, and judging by the numbers of larvae and the fact that nymphs also were recovered, most of the small mammal species examined could be considered as suitable hosts.Although cattle are frequently infested, the adults are parasites of the larger carnivore species, including domestic dogs, and of large monogastric animals such as zebras, rhinoceroses and warthogs (Horak et al. 2000;Walker et al. 2000).

Rhipicephalus warburtoni
The distribution of R. warburtoni is virtually confined to Free State Province (Walker et al. 2000).All stages of development prefer hares as hosts, while the adults are found on domestic and wild ruminants and the immature stages on rock elephant shrews (Walker et al. 2000).Its presence on all the spring hares, Pedetes capensis, and on some of the Namaqua rock mice examined indicates that these animals may also be suitable hosts.The adults, that at the time were identified as belonging to a species similar to Rhipicephalus pravus, produce a toxin causing paralysis in goat kids in the spring and early summer (Fourie, Horak & Marais 1988).

Other species
With the possible exception of those on scrub hares, we consider the remaining species to be accidental parasites or "stragglers" on the small mammals.The immature stages of Amblyomma hebraeum and Amblyomma marmoreum parasitize scrub hares and small carnivores (Horak et al. 1995;Horak et al. 2000), but are hardly ever found on rodents (Howell et al. 1989;Horak et al. 1991;Braack et al. 1996;Petney et al. 2004).The immature stages of I. rubicundus prefer rock elephant shrews and Smith's red rock rabbits, Pronolagus rupestris (Stampa 1959;Fourie et al. 1992), and the one-host ticks, Margaropus winthemi and Rhipicephalus (Boophilus) decoloratus, are parasites of large herbivores (Howell et al. 1978).

TABLE 1
Small mammals and the localities at which they were examined for ixodid ticks

TABLE 4
Ticks, other than Rhipicephalus species, on small mammals in north-eastern Mpumalanga and Limpopo Provinces Rhipicephalus species on small mammals in north-eastern Mpumalanga and Limpopo Provinces I.G.HORAK, L.J. FOURIE & L.E.O.BRAACK TABLE 5