Elephant shrews as hosts of immature ixodid ticks

FOURIE, L.J., HORAK, I.G. & WOODALL, P.F. 2005. Elephant shrews as hosts of immature ixodid ticks. Onderstepoort Journal of Veterinary Research, 72:293–301 Two hundred and seventy-three elephant shrews, consisting of 193 Elephantulus myurus, 67 Elephantulus edwardii and 13 animals belonging to other species, were examined for ixodid ticks at 18 localities in South Africa and Namibia. The immature stages of Ixodes rubicundus, Rhipicentor nuttalli, Rhipicephalus warburtoni and a Rhipicephalus pravus-like tick were the most numerous of the 18 tick species recovered. Substantial numbers of immature Rhipicephalus arnoldi, Rhipicephalus distinctus and Rhipicephalus exophthalmos were also collected from elephant shrews at particular localities. Larvae of I. rubicundus were most numerous on E. myurus in Free State Province from April to July and nymphs from June to October. Larvae of R. nuttalli were most numerous on these animals during April, May, August and September, and nymphs in February and from April to August. The immature stages of R. warburtoni were collected from E. myurus only in Free State Province, and larvae were generally most numerous from December to August and nymphs from April to October.


INTRODUCTION
The ixodid ticks that infest elephant shrews in southern Africa have been recorded by Theiler (1962), who listed 14 species, and reviewed by Fourie, Du Toit, Kok & Horak (1995), who list 22 species.The ticks that infest these small mammals are of more than purely academic interest in that rock elephant shrews, Elephantulus myurus, are the preferred hosts of the immature stages of three ticks capable of inducing paralysis in domestic animals (Fourie, Horak & Van Den Heever 1992a;Fourie, Horak, Kok & Van Zyl 2002).These ticks are Ixodes rubicundus, responsible for massive annual mortality amongst sheep (Spickett & Heyne 1988), Rhipicentor nuttalli that can cause paralysis in dogs (Perchman 1976;Norval & Colborne 1985), and Rhipicephalus warburtoni (then referred to as a tick belonging to the Rhipicephalus pravus group) that has been incriminated in paralysis in goat kids (Fourie, Horak & Marais 1988a).
The hosts of the immature and adult stages of I. rubicundus have been recorded by Stampa (1959) and Horak, Moolman & Fourie (1987a), and the role of E. myurus in the life cycle of this tick, colloquially known as the Karoo paralysis tick, has been highlighted by Du Toit, Fourie & Horak (1994a, b) and Fourie & Horak (1994).The hosts in Zimbabwe of adult R. nuttalli have been listed by Norval & Colborne (1985), while in South Africa the hosts of both adult and immature ticks have been recorded by Fourie et al. (2002), who established the details of its life cycle.Walker, Keirans & Horak (2000) have summarized the host records obtained by Fourie and his co-workers for R. warburtoni during extensive surveys they conducted in Free State Province between 1985 and 1991.Fourie et al. (1992aFourie et al. ( , 2002) ) have also documented the seasonal occurrence of the immature stages of the latter three ticks on E. myurus.
The economic importance of these ticks and the pivotal role of E. myurus in their life cycles prompted further surveys on these animals and on other species of elephant shrews, and the objective of this study was to determine both the species composition and seasonality of ticks that infest them.
Fleas were also collected during the surveys and have been recorded by Beaucournu, Horak & Fourie (2003).

MATERIALS AND METHODS
Ticks were collected by one of two methods from elephant shrews.In the first E. myurus were trapped in box traps each month from August 1994 to June 1995 on the farm Spes Bona in central Free State Province.They were transported to the laboratory and individually caged above trays from which engorged larvae or nymphs that had detached were collected daily.Once all larvae and nymphs had detached, the elephant shrews were returned to their original habitats on the farm and released.The following month's trapping commenced a week after this release so that if the same shrews were recaptured they would have had adequate time to become re-infested with ticks.Despite intensive efforts no elephant shrews were trapped during July 1995.

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Elephant shrews as hosts of ixodid ticks The detached, engorged larvae and nymphs were washed in water to remove traces of urine and prevent the growth of fungi and were maintained at 20 °C and a relative humidity of approximately 90 % in permanent darkness.Once moulting was completed the various species were identified from the newly emerged nymphs or adults and counted.In the second method elephant shrews were captured in box traps, euthanased and their carcasses processed for the recovery of ticks as described by Fourie et al. (1992a).
The seasonal occurrence of the immature stages of I. rubicundus, R. nuttalli and R. warburtoni was determined from the average monthly tick burdens of E.
myurus examined within Free State Province, the only province in which ticks were collected from elephant shrews during every month of the year.

RESULTS AND DISCUSSION
The species of elephant shrews examined, and the localities at which they were trapped are summarized in Table 1.
Tick collections were made at 18 localities from 273 elephant shrews belonging to seven species.
The ticks collected from the elephant shrews are summarized in Tables 2-8.nymphs from June to October (Fig. 1A), matching the seasonal occurrence recorded by Fourie et al. (1992a) on these animals in south-western Free State Province during 1985.The 4-month difference in peak activity between larvae and nymphs (April to August) agrees with the observations of Stampa (1959) and Fourie et al. (1992a) and represents the moulting period of detached larvae and their subsequent attachment to hosts as newly moulted nymphs.
The vast majority of larvae that infest elephant shrews during autumn and early winter originate from eggs deposited by females during the winter of the previous year.These eggs over-summer in a state of diapause and larvae only hatch in autumn (Fourie & Horak 1994).Engorged nymphs that detach from elephant shrews in late winter and spring also over-summer in a state of diapause and only moult to adults during late summer and autumn of the following year (Fourie & Horak 1994).The life cycle thus takes 2 years to complete, with the immature stages present during the cooler months of the first year and the adults during the same months of the second year.Stampa (1959)

Rhipicentor nuttalli
The genus Rhipicentor contains only two species, Rhipicentor bicornis and Rhipicentor nuttalli, whose distributions are restricted to Africa (Theiler 1961(Theiler , 1962)).R. nuttalli has been recorded in the Eastern and Western Cape, Free State, Gauteng, North-West and Limpopo provinces, South Africa (Theiler 1961;Du Toit 1993).In Namibia it occurs north of Windhoek, and it is also present in Botswana and Zimbabwe (Theiler 1961;Norval & Colborne 1985).
In tulus intufi at Erongo, Namibia.R. bicornis occurs in the northern regions of South Africa and in Zimbabwe, northern Namibia and Zambia, and is widely distributed in Central Africa (Theiler 1961;Walker 1991).
The hosts of the immature stages of R. nuttalli were unknown until Du Toit (1993) collected larvae and nymphs from E. myurus in Free State Province.Adult R. nuttalli has been collected from domestic dogs and several wild carnivore species as well as from the South African hedgehog, Atelerix frontalis and porcupine, Hystrix africaeaustralis (Theiler 1961;Walker 1991;Horak et al. 2000).Norval & Colborne (1985) state that whereas R. nuttalli is known in South Africa as the hedgehog tick, their findings in Zimbabwe indicate that the adults are principally parasites of leopards, Panthera pardus, and that its distribution is restricted to the rocky habitats normally favoured by these animals.
The large number of E. myurus infested with R. nuttalli in the present study confirms the observation by Du Toit (1993) that they are hosts of the immature stages of this tick.The collection of nymphs from E. edwardii and E. intufi suggests that these animals, and possibly other species of elephant shrews, are also suitable hosts for the immature stages of this tick, particularly in those regions in which E. myurus does not occur.
Although immature ticks were present on E. myurus throughout the year, the majority of larvae were collected in April and May and during August and September and nymphs in February and from April to August (Fig. 1B).This differs somewhat from the findings of Fourie et al. (2002), also in Free State Province, that larvae were generally most numerous during the period March to September, and nymphs during May to October.Theiler (1962) noted that adult ticks are common on dogs in the Clanwilliam district in the Western Cape Province and in the Omaruru district, Namibia during late summer.
In Gauteng and Free State Provinces adult ticks have been collected from wild carnivores in September, October and December (Horak et al. 2000).
In Zimbabwe, however, Norval & Colborne (1985) found that adult ticks were present throughout the year.

Rhipicephalus arnoldi
This tick utilizes Smith's red rock rabbits as hosts for all its developmental stages (Horak et al. 1991;Horak & Fourie 1991), but large numbers of immature ticks have also been collected from rock das- sies, Procavia capensis (Horak & Fourie 1986;Horak et al. 1991).It has been suggested by Horak & Fourie (1986) that, even if those on rock dassies are taken into account, the low ratio of immature to adult ticks implies that some other animal could also harbour considerable numbers of immature ticks of this species.It would now appear as if rock elephant shrews might fulfil this role in Free State Province.
As their common names imply rock dassies, red rock rabbits and rock elephant shrews inhabit the same rocky habitats (Skinner & Smithers 1990), and since they all have dense pelts it is not surprising that they host some tick species in common.However, whereas rock dassies are also hosts of adult Haemaphysalis hyracophila and adult R. distinctus, and red rock rabbits of adult R. arnoldi (Horak & Fourie 1986, 1991;Horak et al. 1991), rock elephant shrews harbour only the immature stages of these species.

Rhipicephalus distinctus
This is a tick of rock dassies (Horak & Fourie 1986;Walker et al. 2000), and sympatry between these animals and elephant shrews probably contributed to its presence on 11 E. edwardii in the Western Cape Province (Table 2) and on six E. myurus in Free State Province (Tables 4 and 5).

Rhipicephalus exophthalmos
Two E. edwardii examined in the Western Cape Province were infested with larvae and one with a nymph of R. exophthalmos (Table 2).The immature stages of this tick were also present on Elephantulus rupestris at Avis, Namibia, and on the single Macroscelides proboscideus examined at Victoria West, Northern Cape Province (Table 8).Scrub hares, Lepus saxatilis, which incidentally are also hosts of adult R. exophthalmos, are the only other animals recorded as hosts for the immature stages of this tick (Walker et al. 2000).Theiler (1962) lists nearly all elephant shrew species as hosts of the immature stages of a closely related species, namely Rhipicephalus oculatus.It is, however, possible that several of her records refer to R. exophthalmos, which has only recently been described (Keirans, Walker, Horak & Heyne 1993).

Rhipicephalus gertrudae
The adults of R. gertrudae feed on domestic and wild ruminants and carnivores and its immature stages on murid rodents (Walker et al. 2000;Horak & Matthee 2003) and the presence of its immature stages on E. edwardii in the Western Cape Prov-ince is possibly accidental (Table 2).This tick occurs in the southern, central and western regions of South Africa and in Namibia (Walker et al. 2000).

Rhipicephalus kochi
Although widespread elsewhere in East Africa, R. kochi has been collected only in the far north-east of Limpopo and KwaZulu-Natal Provinces in South Africa.The preferred hosts of all stages of development are medium-sized and larger antelopes and scrub hares (Walker et al. 2000).Judging by the single larva and large number of nymphs collected from the single four-toed elephant shrew examined at Pafuri in north-eastern Limpopo Province (Table 8), these animals appear to be good hosts of the immature stages of R. kochi.

Rhipicephalus pravus group
The immature stages of this R. pravus-like tick were present on E. myurus in northern Gauteng Province and north-eastern Limpopo Province, and its nymphs on E. myurus and Elephantulus brachyrynchus in North-West Province (Tables 7 and 8).All its parasitic stages have been collected from scrub hares at Shingwedzi and Pafuri in the Kruger National Park in north-eastern Limpopo Province, and on farms in the north-west of this province (Horak, Spickett, Braack & Penzhorn 1993;Horak, Spickett, Braack, Penzhorn, Bagnall & Uys 1995).Walker et al. (2000) place R. arnoldi, R. exophthalmos, R. kochi, R. oculatus, R. pravus and R. warburtoni in the R. pravus group of ticks on the morphological characters of their immature stages and suggest that these stages favour macroscelids as hosts.The validity of their grouping is supported by the present study in which, with the exception of those of R. oculatus, the immature stages of all these ticks were collected from elephant shrews.

Rhipicephalus warburtoni
This tick has only recently been described (Walker et al. 2000).It was previously variously referred to as an atypical strain of Rhipicephalus appendiculatus (Theiler 1949); as Rhipicephalus pravus (Theiler 1962); as an R. pravus-like tick (Fourie et al. 1988a, b); as an Rhipicephalus punctatus-like tick (Fourie & Horak 1990); and as Rhipicephalus punctatus in several publications by Fourie & Horak and their coworkers.The preferred hosts of the adults are domestic and wild ruminants and hares, and elephant shrews and hares are the preferred hosts of the immature stages (Fourie et al. 1992a;Walker et al. 2000).Its distribution is virtually confined to the central and southern regions of Free State Province (Walker et al. 2000), and its presence on 171 of the 182 E. myurus examined in this province is thus not unexpected (Tables 3-6).
Larvae were generally most numerous from December to August and nymphs from April to October (Fig. 1C).With the exception of April, when larval numbers were exceptionally high, this pattern of seasonality is fairly similar to that recorded by Fourie et al. (1992a).Most adults of this species are present on Angora goats in south-western Free State Province from September or November to February (Fourie & Horak 1991), and it was during this period that paralysis was observed in goat kids (Fourie et al. 1988a).

Other species
The immature stages of the remaining tick species should all be considered as "stragglers".Adult Amblyomma marmoreum infests tortoises and its immature stages are found on these animals as well as ground-frequenting birds, hares, carnivores and ruminants (Norval 1975;Horak, MacIvor, Petney & De Vos 1987b).Adult and immature H. hyracophila are parasites of rock dassies (Horak & Fourie 1986), whereas adults of Haemaphysalis leachi are parasites of carnivores and its immature stages of murid rodents (Norval 1984;Fourie et al. 1992a).However, the latter may also occur on the same hosts as the adults (Horak & Matthee 2003).Adult Hyalomma marginatum rufipes and Hyalomma truncatum infest large herbivorous animals and their immature stages infest hares (Norval 1982;Horak & Fourie 1991).All stages of development of Ixodes bakeri infest shrews and rodents, with a particular preference for Otomys spp.(Walker 1991), while adult Rhipicephalus evertsi evertsi feeds on equids and ruminants and its immature stages on these animals and on hares (Walker et al. 2000).
FIG. 1 The seasonal occurrence of the immature stages of (A) Ixodes rubicundus, (B) Rhipicentor nuttalli, and (C) Rhipicephalus warburtoni on rock elephant shrews in Free State Province, South Africa

TABLE 1
Elephant shrews and the localities at which they were examined for ixodid ticks

TABLE 3
Ixodid ticks collected from 24 Elephantulus myurus on the farm Môreson (28°48´S, 27°13´E) in Free State Province Ixodid ticks collected from 54 Elephantulus myurus on the farm Langberg (29°36´S, 25°28´E) in Free State Province * = Although ticks were collected from 86 animals, only those from 72 animals were identified ** = Engorged larvae and nymphs of I. rubicundus that detached from 21 heavily infested animals were used for experimental purposes without their numbers being recordedEighteen tick species were recovered and the immature stages of I. rubicundus, R. nuttalli, R. warburtoni and a Rhipicephalus pravus-like tick were the most numerous of these.However, substantial numbers of immature Rhipicephalus arnoldi, Rhipicephalus distinctus and Rhipicephalus exopthalmos were also collected from elephant shrews at particular localities.Ixodes rubicundusLarge numbers of larvae and nymphs of I. rubicundus were collected from E. myurus in Free State Province and from Elephantulus edwardii in Western Cape Province in the present study.Stampa (1959) collected approximately 200 larvae and nymphs from nine Elephantulus spp. in the New