- Infectious Diseases of Livestock
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- Vectors: Ticks
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NJ Maclachlan and M-L Penrith (Editors). F Jongejan and G Uilenberg, Vectors: Ticks, 2018.
Previous authors: R A I NORVAL† AND I G HORAK
F JONGEJAN - Director, Utrecht Centre for Tick-borne Diseases, Faculty of Veterinary Medicine, Utrecht University, Yalelaan 1, Utrecht, The Netherlands / Extraordinary Professor, Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Private Bag X04, Onderstepoort, Pretoria, South Africa
G UILENBERG - Retired, PhD, A Surgente, Route du Port, Cargese, Corse, 20130, France
Ticks and tick-borne diseases are ranking high in terms of their impact on animal and human health worldwide. They are efficient vectors of a variety of pathogenic protozoa, rickettsiae, spirochaetes and viruses, which are causing major diseases affecting livestock, humans and companion animals. In livestock, diseases transmitted by ticks constitute a major constraint to animal production in particular in tropical and sub-tropical areas of the world.89 Moreover, there is a great impact of ticks on public health primarily in the northern hemisphere due to Lyme borreliosis and zoonotic tick-borne illnesses of viral origin. This mounting array of tick-borne zoonotic diseases in the temperate regions of the world poses an ever increasing public health risk.38 Also, companion animals are at risk, in particular dogs pay a heavy toll to protozoan and rickettsial tick-borne diseases.13
Globally, there are 896 species recognized in three families. 57 The Nuttalliellidae is monotypic, containing a single species Nuttalliella namaqua. The Argasidae, the soft ticks, consist of 193 species, whereas the hard ticks, the Ixodidae, count 702 species in 14 genera according to a list of valid tick species names published in 2010 and based on an earlier list published in 2002.57, 69
The focus of this chapter is on ticks of African livestock. Since previous editions of this chapter, some changes in tick taxonomy and nomenclature have occurred or have become more generally accepted. Where relevant these changes have been incorporated. At least 200 hard tick species occur in the Afrotropical region, whereas around 40 soft tick species occur here. Interesting, the single representative of the Nuttalliellidae, N. Namaqua, has recently been rediscovered in South Africa and, due to its intermediate characteristics between hard and soft ticks, is considered a “living fossil”.99, 110, 111 As far as African livestock is concerned, the relevance of the Ixodidae is far greater than the Argasidae, although the latter contains important disease vectors in the genera Ornithodoros and Argas.
Hard ticks are the main contributors as vectors of diseases of domestic livestock and of commercially farmed wildlife in the Afrotropical region. The Ixodidae are divided into 12 different genera, including Amblyomma, Hyalomma and Rhipicephalus (among which are the five species from the former genus Boophilus, which is still considered valid by some authors since they differ quite distinctly from the other Rhipicephalus species). Ticks of the genera Ixodes, Dermacentor, Margaropus, Cosmiomma, Haemaphysalis and Rhipicentor all occur in the Afrotropical region, but most are either geographically limited or prefer other hosts over livestock. The remaining three genera, Nosomma, Anomalohimalaya, Bothriocroton are not found on the African continent and also not on domestic animals.57
The only species of the genus Dermacentor that infests domestic livestock in Africa is D. marginatus, but it is not of major economic importance in Africa, where it only occurs in vert limited regions of Morocco and Tunisia.186 Its vector capabilities do not appear to have been thoroughly investigated.
There are no Haemaphysalis spp. in Africa of major importance to domestic livestock. H. punctata is one of the few species in Africa known to feed on livestock and is found only in the more humid parts of North African countries (Morocco, Algeria, Tunisia and Libya). This 3-host tick is a vector of a Babesia and a non-pathogenic Theileria of small ruminants (B. motasi, causing small ruminant babesiosis, but the Theileria has so far not received a valid name) and of a usually non-pathogenic species of Theileria of cattle, T. buffeli, which may cause confusion when studying bovine tropical theileriosis (T. annulata). It has also been found infected with Rickettsia spp. Its range extends from western and southern Europe, through northern Africa to western and central Asia. H. punctata does not occur south of the Sahara, and theileriosis in cattle by T. buffeli, must be transmitted by other ticks. A second tick of this genus found on livestock in Africa is H. sulcata. It has approximately the same geographical distribution as H. punctata: northern Africa (Morocco, Algeria, Tunisia, Libya), southern Europe, and much of Asia. The adults of this 3-host tick feed on large animals, the immatures are mainly parasites of reptiles.186 Ticks of the H. leachii group occur all over Africa, but parasitise mainly carnivores, including dogs, and transmit a particularly virulent form of canine babesiosis (Babesia rossi). Those in South Africa have been distinguished from H. leachii under the old name of Haemaphysalis elliptica by,7 and this means that the results of transmission experiments carried out in South Africa are no longer valid for H. leachii. 7
In this chapter, descriptions of the most important ticks infesting livestock in Africa are provided. Information on the identification, hosts, life cycle, seasonal occurrence, distribution and disease transmission of each tick vector species and remarks on the control of some are given. A section on the control of ticks and some general remarks on that of tick-borne diseases follows: this covers also the history of tick and tick-borne disease control in southern Africa, acaricidal tick control as well as non-acaricidal control methods including anti-tick vaccines, the control of ticks on wildlife and some concluding remarks.
An excellent guide for the identification of ticks of domestic animals in Africa is compiled by Alan Walker and colleagues published in 2003, updated in 2013 and available online.186 A monograph with illustrated maps on the ixodid ticks of major economic importance and their distribution in South Africa has been compiled by Arthur Spickett and published in 2013.173 Very recently, a comprehensive review of the Ixodid ticks of southern Africa has been published in 2018 in a book, wherein much more detailed information can be found than in this chapter.75 A guide entirely dedicated to ticks of the genus Rhipicephalus was compiled by Jane Walker, James Keirans and Ivan Horak and published in 2000.189 Older valuable books on African livestock ticks are from Harry Hoogstraal (1956) with particular reference to ticks of the Sudan,60 The Ixodid ticks of Uganda by Matthysse and Colbo (1987)115 and the Ixodid ticks of Kenya (1974)187 to name a few, although this list is far from exhaustive.
Here, we have included a simplified key to the identification of the presently recognized genera of adult Ixodidae of domestic animals.
Key to the presently recognized genera of adult Ixodidae (hard ticks) of domestic animals
|1a||Anal groove curves around in front of anus; inornate; eyes absent||IXODES|
|1b||Anal groove behind anus, may be difficult to distinguish or absent||2|
|2a||Palps longer than wide; eyes present or absent||3|
|2b||Palps wider than long or only slightly longer than wide; eyes present or absent||4|
|3a||Palpal article 2 less than twice as long as article 3; ventral plates present in males; scutum inornate; festoons present, not always well –developed, sometimes fused, irregular; eyes present, hemispherical, orbited||HYALOMMA|
|3b||Palpal article 2 at least twice as long as article 3; ventral plates absent in males; festoons well developed, regular; scutum usually ornamented; eyes present||AMBLYOMMA|
|4a||Basis capituli rectangular dorsally; scutum ornate or inornate; festoons (11) present; large ticks||DERMACENTOR|
|4b||Palps longer than basis capituli; scutum and palps ornamented; palpal segment II with a dorsal and a ventral rim-like projection; male with ventral plates; India only||NOSOMMA (*)|
|4c||Moderately sized or small ticks; scutum usually inornate; festoons present or absent||5|
|5a||Small ticks; festoons absent; inornate; anal groove faint or obsolete; males very small||6|
|5b||Festoons present; anal groove distinct; males moderate in size||7|
|6a||Legs IV of males greatly enlarged; limited to southern Africa||MARGAROPUS|
|6b||Legs IV of males normal||BOOPHILUS (■)|
|7a||Palpi short, with segment II as broad or much broader than long, projecting beyond lateral margin of basis capituli||HAEMAPHYSALIS|
|7b||Palpal segment II not projecting beyond lateral margin of basis capituli; spiracular plates with tail-like protrusion; basis capituli hexagonal||8|
|8a||Inornate; male without ventral plates; coxa IV of male greatly enlarged||RHIPICENTOR (●)|
|8b||Usually inornate; males with ventral plates; coxa IV of male normal||RHIPICEPHALUS (except subgenus Boophilus)|
(*) Nosomma ticks occur in India only, one or perhaps two species.
(■) Boophilus is considered, on phylogenetical grounds, as a subgenus of Rhipicephalus . The phylogeny of Margaropus has not yet been examined.
(●) Rhipicentor ticks occur in Africa only (two species, of which one is found occasionally on dogs).
The genera Anomalohimayala, Cosmiomma and Bothriocroton have not been found on domestic animals.
Main African tick vectors
Only a relatively small number of ticks are major disease vectors or causes of diseases, because of their large geographical distribution, their important vector capability, or the direct losses and toxicoses of livestock in Africa they induce. These are the Amblyomma spp., (particularly A. hebraeum, A. lepidum and A. variegatum), Hyalommaspp., (particularly H. anatolicum, H. dromedarii, H. scupense and H. truncatum), Ixodes rubicundus,Rhipicephalus spp. (particularly Rhipicephalus (Boophilus) annulatus, Rh. appendiculatus, Rh. (B.) decoloratus, Rh. evertsi, Rh. (B.) geigyi, Rh. (B.) microplus, Rh. zambeziensis and argasid ticks of the Ornithodoros moubata/porcinus complex. However, several other species also serve as vectors, but to a lesser degree or in a more geographically localized context.
It is customary to consider domestic animals as the preferred hosts of those tick species that transmit diseases to them. However, the only ticks that nearly exclusively parasitize these animals in Africa are the introduced Asiatic blue tick, Rhipicephalus (Boophilus) microplus, of cattle and the shiny Hyalomma, H. scupense (= formerly detritum), in north Africa. The vast majority of indigenous ticks in the sub-Saharan region are parasites of wildlife, and indeed a large number of species would be unable to complete their life cycles if there were no wild hosts available. Many of the tick species deemed to be parasites of domestic cattle, sheep, goats, horses and pigs are frequently more abundant or prevalent on equivalently sized or even smaller wild animals. Thus, giraffe (Giraffa camelopardalis), African buffalo (Syncerus caffer) and eland (Taurotragus oryx) are excellent hosts of all stages of development of A. hebraeum and A. variegatum; impala (Aepyceros melampus), eland, bushbuck (Tragelaphus scriptus), greater kudu (Tragelaphus strepsiceros) and sable antelope (Hippotragus niger) of R.(B.) decoloratus; giraffe, African buffalo and eland of adult Hyalomma rufipes and H. truncatum; caracal (Caracal caracal) and mountain reedbuck (Redunca fulvorufula) of adult I. rubicundus; African buffalo, eland, male nyala (Tragelaphus angasii), greater kudu and sable antelope of all stages of development of R. appendiculatus; zebra (Equus spp.) and eland of all developmental stages of R. evertsi; zebra, black rhinoceros (Diceros bicornis), eland and gemsbok (Oryx gazella) of Rhipicephalus pulchellus; large carnivores, zebra and wild suids of adult Rhipicephalus simus; impala and greater kudu of all stages of R. zambeziensis; and warthog (Phacochoerus africanus) of ticks of the O. moubata/porcinus complex. Gerbilline rodents are hosts of the immature stages of H. truncatum and murid rodents the preferred hosts of those of R. simus. Scrub hare (Lepus saxatilis) are preferred hosts of all parasitic stages of Rhipicephalus warburtoni, as well as the immature stages of H. rufipes and H. truncatum. They are also good hosts of the immature stages of A. hebraeum, R. appendiculatus, R. evertsi evertsi, R. pulchellus and R. zambeziensis. Rock elephant shrews (Elephantulus myurus) are excellent hosts of the immature stages of I. rubicundus and of R. warburtoni. Helmeted guinea fowl (Numida meleagris) and leopard tortoise (Geochelone pardalis) are good hosts of the immature stages of A. hebraeum, and ground-frequenting birds of those of H. rufipes.
The diseases of major economic importance affecting cattle and transmitted by these and other ticks are heartwater, babesioses (Babesia bigemina and B. bovis), erythrocytic anaplasmosis, theilerioses (East Coast fever [Theileria parva infection] and tropical theileriosis [Theileria annulata]. In certain conditions, eg dermatophilosis, although not transmitted by ticks, may become severe when susceptible cattle are also infested by the tick Amblyomma variegatum, under the influence of saliva of adult ticks. Of lesser importance in cattle are the generally non-pathogenic mild theilerioses, benign erythrocytic and leukocytic anaplasmoses, benign babesiosis and bovine ehrlichiosis.
Sheep and goats are susceptible to the organisms causing heartwater, ovine anaplasmosis and theileriosis, ehrlichiosis and to the virus causing Nairobi sheep disease, while dermatophilosis may become severe when they are infested by A. variegatum.
Horses, mules and donkeys are affected by equine piroplasmosis (Theileria equi and Babesia caballi) and pigs by porcine babesiosis and African swine fever. In addition to transmitting infectious diseases to livestock, some tick species are also associated with toxicoses such as sweating sickness, paralysis (e.g. Karoo paralysis in South Africa). Several wild ruminant species are susceptible to Ehrlichia ruminantium, the causal organism of heartwater (or cowdriosis), or can act as carriers of this organism. Some are also susceptible to certain Theileria spp., while zebra are susceptible to Babesia caballi and Theileria equi, the cause of equine piroplasmosis, and wild suids to Babesia trautmanni, one of the causes of porcine babesiosis, and to infection with the virus of African swine fever.
Zoonotic tick-borne diseases
Ixodid ticks are also important vectors of several organisms causing zoonotic disease in humans in Africa. These are species of the bacterial genus Rickettsia, such as R. conori, the cause of Mediterranean tick-bite fever or tick-bite typhus, and, in particular in sub-Saharan Africa, of the African tick typhus agent, R. africae. The virus causing the important zoonotic disease Crimean-Congo haemorrhagic fever in humans is also transmitted by ticks, particularly Hyalomma spp. In addition, argasid ticks of the Ornithodoros moubata complex can transmit to humans Borrelia duttoni, the cause of African relapsing fever, perhaps the only human tick-borne disease which is not known to be zoonotic.
Most ticks have also been found to be able to harbour Coxiella burnetii, the cause of Q-fever in humans; this will not be mentioned systematically for each tick species and they do not play a major role in outbreaks of the human disease.
Free-living adult ticks are characterized as ‘hunter ticks’ or ‘ambush ticks’. ‘Hunters’ actively seek hosts by scuttling along the ground when stimulated by a host’s presence or by odours including pheromones produced by ticks already attached to a host. Ticks that follow this strategy are in particular the Amblyomma and Hyalomma species. Also some of the Ornithodoros spp. are hunter ticks, such as Ornithodoros savignyi. These ticks will very rarely be collected by “dragging” from the vegetation. In contrast, the ‘ambush’ ticks are questing for hosts from the vegetation and include Haemaphysalis and Ixodes spp., as well as many Rhipicephalus species. Here a detailed account is given of major hard tick species of African livestock with some identification clues, host preference, life cycle, distribution, vectorial capacity and remarks on control. Soft ticks of the Ornithodoros complex are also briefly discussed.
South African bont tick, Suid-Afrikaanse bontbosluis (Afrik.)
Adult A. hebraeum are large, conspicuous ticks with long mouthparts, brightly coloured patterns on the scutum of both males and females, flat eyes, and brown and white banded legs. The males have yellow-coloured festoons (Figures 1, 2 and 3).
The preferred hosts of the adults are the larger domestic and wild ungulates 78, 129 to which they attach in clusters in the groin and axillae as well as on the dewlap, belly, perineum and peri-anal region.156 The larvae and nymphs feed on a wide variety of large and small mammals, birds and tortoises.2, 33, 82, 156 They are very rarely found on murid rodents, even in habitats where large numbers of A. hebraeum larvae are present.20 On domestic livestock nymphs attach most commonly to the feet, and larvae to the face, the dewlap, neck and legs. On the larger ground-frequenting birds the nymphs and larvae attach mainly on the head and neck.82
Amblyomma hebraeum has a three-host life cycle, with larvae, nymphs and adults feeding on separate hosts. On completion of feeding, engorged female ticks leave the host and seek sheltered microhabitats in which to moult or to lay eggs. The developmental periods off the host can be long. In the Eastern Cape Province of South Africa, larvae may take five months to hatch from eggs laid by female ticks that detached from hosts during March or April, and nymphs may remain inactive for two to three months after moulting. However, the life cycle usually lasts one year under field conditions, but may for the above reasons extend for longer. The pattern of seasonal occurrence is dependent on climate and varies considerably throughout the distribution range of the tick. In general, adults tend to be most numerous during the warm, wet summer months, larvae during the colder, dry, late autumn and winter months, and nymphs during the winter and spring months. However, varying numbers of all stages of development can often be found on hosts throughout the year.63 In the warmer, moist, lowveld regions of the KwaZulu-Natal, Mpumalanga and Limpopo provinces in the north-east of South Africa as well as in southern Zimbabwe, the life cycle seems to be continuous with little indication of a definite seasonal pattern of abundance for the various life stages.67
Amblyomma hebraeum is exclusively a southern African tick. It occurs endemically in the coastal regions of the Eastern Cape and KwaZulu-Natal provinces in South Africa, and in southern Mozambique. Its distribution also extends inland through the lowveld areas of Swaziland, the Mpumalanga, Limpopo and North West provinces of South Africa, and eastern Botswana to southern and western Zimbabwe as well as parts of the Zimbabwean highveld.151, 154 It is absent from the highveld regions of South Africa, possibly because these are too cold and treeless, but may survive locally in these regions in wooded habitats such as north-facing gullies, ravines and valleys. It was originally thought that the highveld of Zimbabwe would be unsuitable for A. hebraeum because of its cooler temperatures. However, the Climex model, indicating ecoclimatic suitability, demonstrated that conditions on the Zimbabwe highveld are favourable for its survival.139 Subsequent surveys conducted there confirm this prediction.151, 154 In central Botswana its distribution is limited by increasing aridity, and in northern Zimbabwe and central Mozambique it may be restricted by interspecific competition with Amblyomma variegatum.181 Amblyomma hebraeum is associated with wooded habitats, including coastal bush, riparian woodland, thornveld and mopani woodland. It does not occur in extensive open, treeless areas.
Amblyomma hebraeum is the main vector in southern Africa of Ehrlichia ruminantium, the cause of heartwater or cowdriosis in domestic and wild ruminants. Laboratory studies have demonstrated that A. hebraeum can carry higher infections and also a greater number of strains of E. ruminantium than A. variegatum, the other major vector of this disease.109 In addition, field observations seem to indicate that outbreaks of the disease are more commonly associated with the former than the latter tick and that these outbreaks are also more severe.139 Besides cattle, a number of wild ruminants,152, 153 as well as other animals such as scrub hare, helmeted guinea fowl and leopard tortoise can act as asymptomatic carriers of E. ruminantium. Other organisms transmitted by A. hebraeum are Theileria mutans and Theileria velifera, the cause of benign bovine theilerioses. The occurrence of foot abscesses in goats in the Eastern Cape Province, South Africa, is significantly related to the seasonal abundance of adult A. hebraeum and Rhipicephalus glabroscutatum.105 The attachment sites of these ticks around and between the hooves afford entrance to secondary bacterial infections.
Adult A. hebraeum have long feeding periods and consequently good control of the tick can be achieved by the treatment of cattle with conventional acaricides at two-weekly intervals, if wild ungulates do not constitute reservoir hosts. As the ticks attach predominantly to the undersides of cattle, control can be achieved by localized acaricide application. It should be noted that in endemic heartwater areas control of A. hebraeum on cattle is only necessary when large clumps of adults, forming potential sites for strike by the screw-worm fly (Chrysomya bezziana) occur, or when the udders or teats of heifers or cows are heavily infested. Over-rigorous control is likely to have the negative effect of disrupting the natural transmission of heartwater to young animals and thus reducing levels of naturally acquired immunity, consequently affecting endemic stability to the disease in domestic ruminant populations.129 Regular acaricidal treatment of domestic livestock, and more particularly cattle, can result in the virtual disappearance of all developmental stages of A. hebraeum on sympatric wild animals up to and including the size of greater kudu as well as the disappearance of free-living larvae on the vegetation.77, 80, 155 Larger wild animals such as giraffe, African buffalo and eland, which are excellent hosts of all stages of development of the tick,78, 80 are probably capable of maintaining populations of A. hebraeum on a farm, even though the domestic livestock on the property are being treated with an acaricide. The residual population of ticks on wildlife on such mixed cattle and wildlife farms may serve as an important source of tick infestation, and consequently heartwater infection,152, 153 for the domestic stock on the farm and thus assist in maintaining immunity.
Tropical bont tick, tropiese bontbosluis (Afrik.)
Adult A. variegatum have long mouthparts and banded legs like A. hebraeum, but the colour patterns on the scutum are different and they have beady eyes. In addition, the festoons of the males are dark brown in colour (Figures 4, 5 and 6).
Hosts and life cycle
Amblyomma variegatum has a host range similar to that of A. Hebraeum.156 It is also a three-host tick, but differs from A. hebraeum in that the immature stages have a more clearly defined pattern of seasonal occurrence. In Zambia adults are most abundant in the wet season (October to February), larvae from March to July, and nymphs from May to September.149 This pattern of seasonal abundance can arise from morphogenetic diapause in the females, resulting in a delay in oviposition.148 Similar observations of only one generation per annum have been made in other regions which have a single rainy season.156 In Zimbabwe adults can be present throughout the year, with heavier infestations in the warmer months (September to May), and with nymphs present only from June to September.
Amblyomma variegatum is widely distributed through West, Central and East Africa and in southern Africa extends into north-eastern Botswana, the Caprivi Strip of Namibia, and northern and central Mozambique.191 Since 1986 A. variegatum has spread from the north-western regions of Zimbabwe to the central and eastern Highveld.151, 154 Its spread southwards appears to be limited by interspecific competition with A. Hebraeum181 with which it shares similar habitats, hosts and sites of attachment.156
Ehrlichia ruminantium, the cause of heartwater or cowdriosis; Theileria mutans, T. velifera, the cause of benign bovine theilerioses; probably Ehrlichia bovis, the cause of bovine ehrlichiosis; and the virus causing Nairobi sheep disease. Severe bovine dermatophilosis (Dermatophilus congolensis) is associated with the presence of the tick.
The control of A. variegatum with acaricides is similar to that described for A. hebraeum. However, the more clearly defined seasonality of A. variegatum facilitates strategic control of the adults during the wet season. Important observations on the attachment of adult A. variegatum have been made in Burkina Faso179 and have led to an innovative and relatively inexpensive method of control, an acaricidal footbath during the adult peak season when the animals are returned from pasture in the evening,25 and even to simultaneous control of the tick and of riverine tsetse flies.19 Adult A. variegatum ticks picked up in the pastures first mainly attach to the interdigital areas (87 per cent of the 791 ticks captured), and are still attached there, when the animals return from pasture in the evening; they only later fix themselves to the classical predilection sites. The footbath treatment during the adult peak season is appreciated by the livestock owners as it demands far less acaricide per animal and is much less time-consuming.19, 178
Angolan bont tick
Life cycle, hosts and distribution
This tick has a three-host life cycle similar to those of A. hebraeum and A. variegatum and has a similar host range.156 The adults most frequently attach on the undersides of cattle. It is present in Angola, parts of western Zambia, and in the southern region of the Democratic Republic of the Congo.191 However, unlike other southern African vectors of heartwater, A. pomposum occurs in wet highland areas in savanna and forest. In Angola, nymphs and adults are most abundant during the rainy season, although large variations may occur depending on the region and climate.
Ehrlichia ruminantium, the cause of heartwater or cowdriosis.
East African bont tick
Life cycle, hosts and distribution
This is a three-host tick and the adults prefer cattle as hosts, although camels (Camelus dromedarius) may also harbour quite large infestations.156 Other domestic animals can also be infested as well as a number of wild ungulates. Adults are predominantly found attached on the ventral surface of the host from the lower dewlap and axillae to the escutcheon. It is widespread in eastern Sudan, Ethiopia, southern Somalia, eastern Uganda, Kenya and the northern region of central Tanzania.191 In Tanzania, which lies south of the equator, adult ticks are most abundant between October and February, beginning either shortly before or shortly after the onset of the rainy season. However, there may be considerable variation in the timing of the peak as well as in the numbers of ticks present. In Ethiopia, north of the equator, adults peak during the rainy season in May to June.
Ehrlichia ruminantium, the cause of heartwater or cowdriosis.
Other African Amblyomma species.
A number of other African Amblyomma spp. have also been implicated in the transmission of heartwater to domestic livestock (see Heartwater). Except under certain unusual circumstances the ability of several of these tick species to transmit heartwater to domestic ruminants is limited because their adults, which appear to be the most efficient vectors, by preference do not feed on these animals,156 or their geographical distribution is limited or covers a region without animal husbandry. The males and females of all these ticks are ornate,191 have long mouthparts, and all have three-host life cycles.156 These ticks include:
- Amblyomma astrion, with African buffalo and cattle being the principal hosts of the adults. It is distributed mainly in the Central African Republic, the northern and western regions of the Democratic Republic of the Congo, north-western Angola and the islands of São Tomé and Príncipe.
- Amblyomma cohaerens, which infests African buffalo, and domestic cattle in regions in which buffalo are, or used to be, common. It has been recorded chiefly in the eastern region of the Democratic Republic of the Congo, western Uganda and central Ethiopia.
- Amblyomma gemma, for which domestic cattle and large, wild herbivores are the preferred hosts of the adults. It is mainly distributed in eastern Ethiopia, northern and southern Somalia, Kenya and north-eastern Tanzania.
- Amblyomma marmoreum, of which all stages of development, and most particularly the adults, feed on tortoises and large varanids. Adults very rarely parasitize domestic livestock but the immature stages, especially larvae, are frequently encountered on these animals. This tick is widespread in Zimbabwe and South Africa and is probably more prevalent in Mozambique, Botswana and Namibia than current records seem to indicate.
- Amblyomma sparsum, of which the adults prefer large reptiles, but black rhinoceros and African buffalo may also be important hosts. It rarely infests domestic hosts. Most records of this tick’s occurrence are from southern and western Kenya, northern and central Tanzania and north-western Zimbabwe.
- Amblyomma tholloni, of which the preferred hosts of the adults are African elephant (Loxodonta africana) and hippopotamus (Hippopotamus amphibius). Although larvae and nymphs have been collected from cattle, sheep and goats, domestic stock are not common hosts. This tick has been recorded in the Ivory Coast and adjacent countries to the west, and throughout Central Africa to the eastern coastal regions from Kenya in the north to northeastern South Africa in the south.
Hyalomma anatolicum and Hyalomma excavatum
For a long time there has been confusion over the names. They have been considered as synonyms, or both were considered as subspecies of H. anatolicum or of H. excavatum, but it has finally been universally recognised that there are two different species, H. anatolicum and H. excavatum.6 A peculiarity is that the adults of H. anatolicum are smaller than those of H. excavatum, but the size of the immatures (larva and nymph) of H. anatolicum is greater than that of the immatures of H. excavatum.
Life cycle, hosts and distribution
Both occur in Northern Africa, but their greatest area of distribution is in Asia. H. excavatum has also been found in south-eastern Europe. The geographical distribution of H. anatolicum exceeds that of H. excavatum.In north-eastern Africa, H. anatolicum has succeeded in establishing itself south of the Sahara, probably penetrating the great desert along the Nile. Both species are sympatric in large parts of their geographical distribution. Nymphs and larvae of H. anatolicum mainly feed on medium-sized and large mammals, while those of H. excavatum are parasites of small mammals. The adults of both species feed mainly on large ungulates (such as cattle). They are usually three-host ticks, occasionally two-host.
Disease transmission. Both species are vectors of bovine tropical theileriosis (Theileria annulata), and in the Sudan H. anatolicum is the main vector of this bovine disease in the delta between the Blue and the White Nile.
Small smooth bont-legged tick, sweetsiektebosluis (Afrik.)
Adults of H. truncatum are medium-sized ticks with long mouthparts and dark-brown bodies, beady eyes, and long, red and white banded legs. The posterior surface of the scutum in males is characterized by a depression containing numerous large punctations, otherwise it is comparatively smooth (Figures 11 and 12).
The preferred hosts of the adults are large ungulates, both domestic and wild.60, 65, 131 They attach in the tail switch, around the anus, on the lower perineum, and on the legs, including around the feet. The immature stages feed on hares and on certain rodents, particularly gerbils.20, 62
Hyalomma truncatum has a two-host life cycle, which normally takes a year to complete under field conditions in South Africa. Adults occur in the greatest numbers in the late wet summer months and the immature stages in the dry autumn to spring months.63, 81, 162
This tick is adapted to dry climates and is absent in Lesotho and, with the exception of the Eastern Cape, the eastern half of the Free State, south-eastern Gauteng and Mpumalanga, and southern KwaZulu-Natal, it is present throughout South Africa, Zimbabwe and much of Mozambique. It is also present in south-eastern and north-western Botswana; central and northern Namibia; southern Angola; western, southern, central and eastern Zambia; central and southern Malawi; south-western and north-eastern Tanzania; southern, central and western Kenya; and eastern Uganda.54, 149 It also occurs in many countries in north-eastern, Central and West Africa. Hyalomma nitidum has for a long time been considered as a synonym of H. truncatum, until it was clearly characterized and distinguished from H. Truncatum 183 mainly on the basis of the shape of the gonopore of the female, and the absence of the clear white rings of H. truncatum on the legs. It is also different in its environmental preferences. It is a West and Central African tick, for which the isohyet of 900-1000 mm is about the lower limit, while H. truncatum is usually found in lower rainfall areas. H. nitidum has also been redescribed in detail.8 Molecular studies might indicate if and how closely H. nitidum and H.truncatum are related. At a local level the abundance of H. truncatum is influenced by the abundance of hares, which are the preferred hosts of the immature stages.
Babesia caballi, the cause of equine piroplasmosis. Because the immature stages of H. truncatum do not feed on horses the transmission of B. caballi by this tick has of necessity to take place transovarially. Hyalomma truncatum also transmits the virus causing Crimean-Congo haemorrhagic fever (CCHF) in humans, and the toxin causing sweating sickness in cattle and especially in young calves. Only certain strains of H. truncatum produce this toxin and then it is only female ticks that do so. The long mouthparts of the ticks, as well as their tendency to form clusters, can cause tissue damage resulting in secondary bacterial infections and abscess formation. The attachment of adult ticks to the interdigital clefts and fetlocks of lambs almost always causes lameness.
Hyalomma nitidum has been reported to be infected with the virus of CCHF.
Hand-dressing of the preferred attachment sites with an acaricide will assist in controlling the adults. It is impractical to control the immature stages because of their preference for hares and rodents.
The coarse bont-legged tick, groot bontpootbosluis (Afrik.)
Adult H. rufipes are large ticks with dark-brown bodies, long mouthparts, a scutum that is heavily punctate, beady eyes, and long, red and white banded legs. They differ from those of H. truncatum in that the whole scutum is punctate and in the males it is more circular than the rather elongate shape of the latter tick. However, it is virtually impossible to distinguish between the two species by means of the naked eye.
Adults parasitize domestic and wild ungulates, showing a preference for the larger species.65, 131, 187 They attach mainly in the hairless peri-anal region and on the lower perineum and genitalia. The immature stages are parasitic on hares, particularly scrub hares, as well as on ground-frequenting birds.62, 131, 162
Hyalomma rufipes has a two-host life cycle, which under field conditions in South Africa takes a year to complete. The adults are most numerous in the early part of the wet season and the immature stages in the dry season.63, 106, 133
This tick is widely distributed in southern Africa, and appears to be absent only from the winter rainfall areas of the Western Cape Province, the mountainous areas of Lesotho and KwaZulu-Natal where snow falls in winter, and some humid, subtropical habitats along the east coast and in the north-east. It is also present in the drier regions of the southern and north-western provinces of Mozambique, south-eastern and north-western Botswana, central and northern Namibia, southern Angola, most of Zimbabwe, southern and western Zambia, central and north-eastern Tanzania, central and southern Kenya, western Burundi, eastern Uganda, and in Somalia, Sudan, Ethiopia and in West Africa.60, 84, 92, 131, 147, 149, 187 Parasitism of birds by the immature stages undoubtedly contributes to the extensive distribution of this species.
Babesia occultans, the cause of benign bovine babesiosis; Anaplasma marginale, the cause of bovine anaplasmosis; and the virus causing Crimean-Congo haemorrhagic fever. Secondary bacterial infection of tick attachment sites can lead to the formation of abscesses in cattle. It is frequently transported, even to northern Europe, on migrating birds, and occasionally adults of this species can be found there after nymphs from birds have moulted.
Can be accomplished by localized acaricide treatment. Hyalomma rufipes is difficult to control on cattle herds even by regular acaricide application as engorged nymphs are continuously being brought in from other areas by birds.
The shiny Hyalomma
Adult H. scupense (syn. H. detritum)are medium-sized ticks with long mouthparts, a very dark-brown, smooth, shiny scutum, and long reddish or yellowish-brown legs which may have paler bands.60
Domestic cattle and horses are the most common hosts, but sheep, goats and camels may also be infested.60 All stages of development feed on the same host species. Adults attach on the inner thighs, udder, scrotum and perineum of cattle.18
Life cycle and distribution
Hyalomma scupense usually has a two-host life cycle with the adults feeding in summer and the larvae and nymphs in autumn.60 The detached engorged nymphs undergo a winter diapause and moult to adults the following summer.18, 60 The life cycle is often associated with barns, stables and sheds, and livestock become infested when they are housed in these structures. This Hyalomma is present along the Mediterranean coast of Africa as far as Algeria and Morocco in the west.60 It is also present in sub-Saharan Africa in north-central Sudan, which it may have invaded from the Red Sea coast or via the Nile River Valley.60 Its geographic distribution also encompasses much of Asia (the Near and Middle East, Central Asia, extending even to China). Under certain circumstances H. scupense may adopt a one-host life cycle, and this has been the cause of much confusion concerning its nomenclature, which now appears to be resolved.5 Curiously, the adult ticks are active all the year on Corsica, where cattle are kept outdoors throughout the year.55
Theileria annulata, the cause of tropical theileriosis. In those regions in which this tick is the vector of T. annulata, tropical theileriosis frequently occurs on small farms where livestock are closely associated with barns and stables and the ticks hides in cracks. It also transmits Theileria equi, the cause of equine piroplasmosis and is probably also a vector of CCHF virus.
The camel Hyalomma
Adult H. dromedarii are large ticks with long mouthparts. The scutum of the male is characterized by posterior grooves and ridges. The colour of these ticks varies from yellow-brown to nearly black. The legs are paler than the scutum and may be ringed by paler bands.60
The preferred hosts are camels, but cattle, sheep, goats and horses may also be infested.61 Adults attach on the inner thighs, udder and scrotum of camels. The larvae and the nymphs feed on small burrowing animals and hares, but the nymphs may also infest camels, cattle and horses.
Life cycle and distribution
Hyalomma dromedarii has a two- or a three-host life cycle. The larvae may feed and moult to nymphs on small mammal or leporid hosts and the adults feed on large herbivores, in particular camels. The larvae may also feed on small mammal hosts, drop off and moult to nymphs, which can then either attach to other small mammal hosts or feed on the same large animals as the adults.60 The life cycle appears to be continuous throughout the year.
This tick is common wherever camels occur in the Far, Middle and Near East. It is also present in Mauritania in West Africa and in Morocco, Algeria, Tunisia and Libya in North Africa and is well-adapted to an arid and even desert environment.24 In north-eastern and East Africa it occurs in Sudan, Eritrea, northern, eastern and southern Ethiopia, northern Kenya and north-eastern Uganda.60, 115, 147, 187
The tick is an effective vector of Theileria annulata, the cause of tropical theileriosis, and is apparently the main one of tropical theileriosis of cattle in Mauritania.
Other Hyalomma species
The subspecies of Hyalomma marginatum are now considered as full species,9 H. marginatum marginatum = H. marginatum, H. marginatum rufipes = H. rufipes (which has been treated separately, above), H. marginatum isaaci = H. isaaci and H. marginatum turanicum = H. turanicum.
Hyalomma marginatum occurs in several countries of north Africa and Europe, extending through southern Russia and the Near East through central Asia, up to China. It is a major vector of CCHF and can transmit B. caballi. It is a two-host, sometimes three-host tick, with the adults feeding on large ungulates, but the hosts of the immatures are more frequently found on small wild mammals and birds.
Hyalomma isaaci and H. turanicum are exclusively Asian ticks. Until recently it was believed that the latter also occurred in certain areas of South Africa, but the name Hyalomma glabrum was revalidated for this South African tick.6
Several other Hyalomma spp. are much more localized and rarely encountered on domestic animals.
Karoo paralysis tick, Karoo-verlammingsbosluis (Afrik.)
Sheep and goats are the preferred domestic hosts of the adults, on which they attach to the ventral parts of the body, neckline and upper half of the legs.49 Wild hosts include Caracalla and mountain reed buck.79 The preferred hosts of the immature stages are rock elephant shrews and red rock rabbits (Pronolagus rupestris).49, 73, 79
Ixodes rubicundus has a three-host life cycle that takes two years to complete. Larvae are active in autumn and winter, nymphs during winter and spring of the same year as the larvae, and the adults in late summer, autumn or early winter of the following year.49, 73, 79
This tick is associated with the southern slopes of hilly or mountainous terrain and occurs in Karroo vegetation types in the semi-arid interior of South Africa. It is present in the Western and Northern Cape provinces, through much of the interior of the Eastern Cape, in the central and southern parts of the Free State, and in southern and western Gauteng in the Heidelberg and Bronkhorstspruit districts.84, 175
Karoo paralysis (toxicosis) is caused by the engorging females and occurs most commonly in late summer, autumn and early winter when these ticks are present. The colder the mean minimum atmospheric temperatures during the two months preceding tick activity, the earlier this activity commences.47 Paralysed animals will usually recover if the attached adults are removed or killed using rapid-acting acaricides, but severe losses in sheep, goats and even young calves can occur if preventive measures are not taken.84, 175 Wild animals such as springbok (Antidorcas marsupialis) can also be affected.45
The control of I. rubicundus includes acaricidal treatment of sheep and goats prior to the onset of the cooler months of the year. These animals should also be moved from mountain camps with a southern aspect to other grazing from late summer to spring. The underbrush of trees or shrubs, which give protection not only to the free-living stages of the tick but also to the small mammal hosts of the immature stages, can be removed.49, 175 This can be accomplished by pruning, or fire, or by allowing goats to browse during the summer months. Cattle and sheep can be used before winter to keep the grass cover short, thereby creating conditions unsuitable for tick survival or for questing for hosts.49, 170 Fire can also be used for this purpose.
Other Ixodes species
The common European tick, I. ricinus, has long been considered to be confined to Europe and part of the Arabian peninsula, but recently it was discovered in northern Africa, mainly Tunisia, Morocco and Algeria.186 Some of the disease agents it is known to transmit in Europe were also discovered in northern Africa (B. burgdorferi s.l., Babesia divergens and Anaplasma phagocytophilum).186
Brown ear tick, bruinoorbosluis (Afrik.)
Adults of R. appendiculatus are medium-sized brown ticks with short mouth parts. The legs of the males increase markedly in size from the first to the fourth pair and engorged males have a slender caudal process (Figures 15, 16 and 17). These ticks are frequently seen questing for hosts on blades of grass during the early part of the wet season.
This species has a wide host range. Adults parasitize medium-sized to large ruminants while the immature stages feed on most ruminant species and a variety of other mammals, including equids, carnivores and hares.142, 196 Among domestic animals, cattle are the preferred hosts and can become very heavily parasitized with all stages of development., Several wild ruminant species, such as impala, African buffalo, eland, male nyala, bushbuck, greater kudu and sable antelope, can also be heavily infested.142, 196 Female nyala harbour few adult ticks but are good hosts of the immature stages.67 Adults attach in the highest numbers to the ears of their hosts but are also found on other parts of the body.106 The proportion that attaches to the ears varies between host species and is also dependent on the availability of attachment sites on the ears. Larvae and nymphs may attach to the ears as well as to other parts of the body such as the head, legs, neck and dewlap.
Rhipicephalus appendiculatus is a three-host tick with a strictly seasonal, single annual life cycle in southern Africa. Adults are most abundant during the rainy period in summer (December to April), larvae in the late summer and cool period after the rains (April to August), and nymphs in the winter and early spring (June to October).159, 169 The pattern of seasonal occurrence is regulated by the unfed adults, which enter diapason and do not engage in host seeking until the rains start.168 In countries close to the equator more than one life cycle can be completed annually and no clear pattern of seasonal abundance may be evident.92, 118
Rhipicephalus appendiculatus is an eastern, central and southern African tick.100 Its distribution extends from southern Sudan, Uganda, south-western Kenya, eastern Democratic Republic of the Congo, Rwanda and Burundi to northern, north-eastern, central and southwestern Tanzania. Further south it is confined to the wetter areas, which include the highlands of Malawi, Zambia, Zimbabwe and the Angonia and Chimoio provinces of Mozambique. The extent of its distribution in the coastal areas of Mozambique is unknown. It is also present in eastern Botswana and in Swaziland. In South Africa it occurs in the Limpopo, North West, Gauteng and Mpumalanga provinces, along the east coast of KwaZulu-Natal and nearly throughout the southern Eastern Cape Province.
This tick survives best in woodland and woodland savannah regions with good vegetation cover. It tends to disappear if overgrazing occurs and it does not survive on open plains. Its distribution may vary with rainfall. It was introduced into the south-eastern lowveld of Zimbabwe during the commencement of a wet cycle in 1973, and by 1982 it was estimated that more than 1 million ha of the lowveld was infested.135 The tick started to disappear from this region towards the end of a dry cycle in 1983 and by 1985 it could no longer be found. 138 In eastern Zambia, R. appendiculatus spread southwards between 1972 and 1982 and then westwards during the 1980s and 1990s. 11
Rhipicephalus appendiculatus is the chief vector of strains of Theileria parva that cause East Coast fever, other strains of T. parva that cause Zimbabwe theileriosis and yet others that cause Corridor disease. This tick also transmits Theileria taurotragi, the cause of benign bovine theileriosis; Ehrlichia bovis, the cause of bovine ehrlichiosis; the virus causing Nairobi sheep disease; and when large numbers of ticks are present they may produce sufficient toxin to cause brown ear tick toxicosis. Infection with T. taurotragi may cause severe or even fatal disease in eland.Exotic Bos taurus cattle suffer serious production losses and can become secondarily infested with the larvae of the screw-worm fly if heavily infested with adult ticks. In small wildlife parks situated in high rainfall regions large infestations with R. appendiculatus can constitute a serious problem in several antelope species.102
Exotic cattle should receive acaricide protection throughout the summer months. African zebu (Bos indicus) cattle and indigenous Sanga breeds become fairly resistant to the tick and so require fewer acaricide treatments.141, 160 In the absence of theilerioses, adequate control of adults can usually be accomplished by localized application of acaricides to the ears or head. Larvae and nymphs are considerably less damaging to cattle than adults, and do not require treatment if adequate control of the adults is achieved. Heavy infestations with adult R. appendiculatus can also occur on horses, and these may require treatment with acaricides during the summer. Control on other domestic livestock species is unnecessary.
Regular acaricidal treatment of cattle on a mixed cattle and game ranch in Central Province, Zambia, resulted in a significant reduction in all stages of development of R. appendiculatus on sympatric impala and on the vegetation of the ranch.197 Should infestation with adult R. appendiculatus become a problem on wildlife in small reserves, control can be achieved by various methods based on the principle of self-application of acaricide.36, 172
Angolan brown ear tick
Identification, life cycle, hosts and distribution
Rhipicephalus duttoni is an ear tick that closely resembles R. appendiculatus in appearance. It is a three-host species of which the adults parasitize particularly domestic cattle and African buffalo. It occurs in the coastal and adjacent inland regions of Angola, particularly in the south. Its southern and northern distributions extend to the north-western border of Namibia and the western coast of the Democratic Republic of the Congo respectively.
In Angola R. duttoni is considered to be the vector of strains of Theileria parva causing Corridor disease.
Lowveld brown ear tick, laeveldse bruinoorbosluis (Afrik.)
Rhipicephalus zambeziensis and R. appendiculatus are morphologically very similar. The major morphological difference between the adults of the two species is that those of R. zambeziensis have a more conspicuously punctate scutum.190
Hosts and life cycle
Its host range, attachment sites, life cycle and pattern of seasonal abundance are also similar to those of R. appendiculatus.81, 142 However, on impala the vast majority of adult ticks attach around the muzzle as opposed to the ears,114 and a larger proportion of nymphs attach to the lower legs of greater kudu than do those of R. appendiculatus.142
The distribution of R. zambeziensis differs from that of R. appendiculatus.100 It replaces the latter tick in the hot, dry river valley systems of south-eastern Africa (e.g. Luangwa, Kafue, Zambezi, Limpopo and Sabi rivers) which separate the major highland areas. In contrast to R. appendiculatus, it occurs in the fairly dry environments of northern Namibia and in the lowland areas of the Mozambique interior. It is also present in southern Angola, western and south-eastern Zambia, and in Tanzania north of Lake Malawi. The distributions of R. zambeziensis an R. appendiculatus overlap where there are gradual transitions between wet and dry areas. This occurs in parts of the Eastern and Southern provinces of Zambia bordering the Zambezi Valley, in eastern Botswana, and in the North West, Limpopo and Mpumalanga provinces of South Africa.68, 100 In these situations some interspecific hybridization may occur.198 Rhipicephalus zambeziensis is absent from semi-desert and desert areas.
Strains of Theileria parva causing Corridor disease; strains of Theileria parva causing Zimbabwe theileriosis; Theileria taurotragi, the cause of benign bovine theileriosis; and Ehrlichia bovis, the cause of bovine ehrlichiosis. Although R. zambeziensis can, in the laboratory, transmit strains of T. parva associated with Zimbabwe theileriosis, it is not associated with outbreaks of the disease in the field.135 However, the presence of T. parva group antibodies in cattle in buffalo-free areas, in which the tick occurs in southern Zimbabwe, suggests that it does transmit subclinical infection.135
Rhipicephalus zambeziensis differs from R. appendiculatus in that its populations never build up to numbers that could be expected to cause significant production losses in cattle. For this reason there is little, if any, need to direct specific control measures against this tick species, other than to protect cattle from infection with the T. parva group of organisms where contact with buffalo occurs.
Red-legged tick, rooipootbosluis (Afrik.)
The preferred hosts of the adults are domestic and wild equids (horses, donkeys, mules and zebras) although cattle, sheep, goats and a number of antelope species, particularly eland, are also frequently parasitized.60, 71, 76, 130 The adults attach in the peri-anal and inner thigh regions of their ungulate hosts. Larvae and nymphs feed deep in the external ear canals, and are found most commonly on the same ungulate hosts as the adults, as well as on hares.81, 130
Rhipicephalus evertsi has a two-host life cycle in which the larvae moult to nymphs on the first host, the nymphs engorge, detach, fall off and moult, and the adults attach to the second host. With the possible exception of some of the colder regions the tick can complete more than one generation per year.134 All stages may be present on hosts throughout the year, but their abundance can vary from season to season.
Of the 60-odd Rhipicephalus spp. present in sub-Saharan Africa, R. evertsi is the most widespread. It is most common in the eastern half of the continent, from Eritrea and Sudan in the north to South Africa in the south.189 It tolerates a wide range of climatic conditions and in southern Africa the main factor limiting its distribution in the west is increasing aridity, with the critical rainfall level being about 250 to 280mm per annum.84
Anaplasma marginale, the cause of bovine anaplasmosis; Babesia caballi and Theileria equi, the cause of equine piroplasmosis; Theileria separata, the cause of benign ovine theileriosis; Borrelia theileri, the cause of borreliosis or spirochaetosis; and the toxin causing spring lamb paralysis. This tick can also experimentally transmit Babesia bigemina, the cause of bovine babesiosis.21 In the eastern highveld regions of the Mpumalanga and Free State provinces in South Africa, the synchronous moulting during spring of over-wintered nymphs gives rise to large numbers of adults,83 and these may infest newly born lambs. As the females engorge they secrete a toxin which causes paralysis. Locally this is known as spring lamb paralysis because of the season of its occurrence and the age of the animals affected.
Adult R. evertsi ticks are easily controlled by localized application of acaricide to the peri-anal area. Usually no specific control measures are taken against the immature stages, but these could be controlled by the topical application of acaricides to the inner surface of the ears and to the ear canals. The danger of piroplasmosis in thoroughbred racehorses often warrants the expense of treatment, in which case both the immature and adult ticks should be controlled.
Rhipicephalus bursa is a large light-brown species. The scutum is covered with numerous fine punctations. The bulging eyes constitute a distinctive feature. In engorged males, the light tan body wall expands laterally and posteriorly beyond the darker scutal margins.
All stages of development feed on cattle, sheep, goats, horses and camels.189 Adult ticks attach mainly on the inner surface of the ears of sheep but can also attach on the dorsal outer surface, as well as in the perineal and inguinal regions of these animals.189
Rhipicephalus bursa has a two-host life cycle that takes a year to complete. Adult ticks are most abundant on sheep during summer in the northern hemisphere (June and July).189
The Mediterranean, Adriatic and Aegean basins, and in Libya, Tunisia, Algeria and Morocco in North Africa. Rhipicephalus bursa is also present in some countries in southern Europe as well as in the Near East.189
Babesia bigemina, a cause of bovine babesiosis, viz. African redwater; B. bovis, causing another form of bovine babesiosis; B. ovis and probably some strains of B. motasi, causes of ovine babesiosis;Babesia caballi (experimentally) and Theileria equi, the cause of equine piroplasmosis; Ehrlichia ovina (experimentally), the cause of ovine ehrlichiosis; Anaplasma marginale and A. ovis, the causes of erythrocytic bovine and ovine anaplasmosis, respectively.
Acaricide can be applied to the ears of sheep during the summer months.
Zebra tick, yellow-backed tick
Adults of R. pulchellus are medium-sized to large ticks with a characteristic dark brown-and-ivory pattern on the scutum of the male, while the scutum of the female is predominantly ivory-coloured with anterior dark markings (Figures 20 and 21).
The adults prefer cattle, on which they may occur in large numbers, as well as camels, sheep and goats.147, 187, 189 They attach primarily on the ears and the underside of the body, including the chest, belly, genital and peri-anal areas. Their preferred wild hosts are zebra, black rhinoceros, eland and gemsbok. The immature stages feed on these animals as well as on hares.147, 187, 189
Life cycle and distribution
Rhipicephalus pulchellus has a three-host life cycle. The adults appear to be most active during the rainy season.147 It is one of the most common ticks present in the Horn of Africa, as well as in and to the east of the Rift Valley from Eritrea in the north to north-eastern Tanzania in the south.189
Theileria taurotragi, the cause of benign bovine theileriosis; and the virus causing Nairobi sheep disease.
Strategic control of the adults can be achieved by acaricidal treatment during the rainy season.
Glossy brown tick, blinkbruinbosluis (Afrik.)
Adults of R. simus are large, dark-brown ticks. The scutum has a glossy appearance and there are four longitudinal rows of large punctations on the scutum of the male.
The preferred domestic hosts of the adults are cattle, horses and dogs.137, 150 The adults attach in the tail brush and around the feet of cattle and horses and around the head and neck of dogs.106, 189 Monogastric wild animals, such as the larger wild carnivores, zebra, rhinoceros, warthog and bushpig, are particularly good hosts of the adults.66, 71, 76, 129
The immature stages are parasitic on murid rodents.66, 137, 159 Adult abundance appears to be limited by the availability of hosts for the immature stages.128
Life cycle and distribution
Rhipicephalus simus is a three-host tick of which the adults are most abundant during the warm, wet summer months, and the immature stages during the cooler, dry autumn to spring seasons.20, 66, 106, 159 It is widely distributed in the moderate to high rainfall areas of Angola, Zambia, Zimbabwe, Malawi and Mozambique in the north to South Africa in the south,189 but rarely occurs in large numbers. In the north-east of the continent it is replaced by Rhipicephalus praetextatus and in the north-west by Rhipicephalus muhsammae, both ticks that are very similar in appearance to R. simus and with which it has been confused in the past.189
Anaplasma marginale, the cause of bovine anaplasmosis; Anaplasma centrale; Babesia trautmanni, the cause of porcine babesiosis; and a toxin causing paralysis in calves and lambs.
Although transstadial transmission of A. marginale to cattle is possible, this hardly seems likely to occur in the field as the immature stages feed virtually exclusively on rodents. Intrastadial transmission by infected adult ticks, and more particularly males, wandering from one host to another seems a more likely route of infection. Infection of suids with B. trautmanni would seem to occur by the Babesia being passed transovarially from one generation of adult ticks to the next generation of adult ticks, which then feed on susceptible animals.32
Except as a measure to prevent anaplasmosis in susceptible cattle and occasionally to prevent paralysis in calves and lambs, acaricidal control of this species is probably not justified.137
Rhipicephalus turanicus is a moderate- sized, reddish-brown tick, which even under a stereoscopic microscope is difficult to differentiate on morphology from the kennel tick Rhipicephalus sanguineus, with which it has been confused in the past.146 The latter tick virtually exclusively parasitizes domestic dogs.189
The domestic animals from which adult R. turanicus have most frequently been collected in sub-Saharan Africa are cattle, sheep and dogs, with no collections from pigs and only a few collections from horses. Its favoured wild hosts are the larger carnivores, hares and some of the larger ground-feeding birds, with a few collections from zebra and warthog.146, 189 The hosts of the immature stages include hedgehogs, shrews, gerbils, murid rodents and hares.189
Life cycle and distribution
Rhipicephalus turanicus is a three-host tick of which the adults generally are most numerous during the late rainy to early dry seasons.81, 146 In sub-Saharan Africa the majority of records originate from the eastern parts of the continent from Sudan, Ethiopia and Somalia in the north to South Africa in the south. However, several collections have also been made in northern Namibia. This tick occurs in several of the Mediterranean countries as well as in their immediate neighbours and also in Russia, India and Pakistan.189
Babesia caballi and Theileria equi (both suspected), the cause of equine piroplasmosis; and Babesia trautmanni (experimentally), the cause of porcine babesiosis.
Because R. turanicus has frequently been confused with R. sanguineus, reports of the transmission of equine piroplasmosis by R. sanguineus could have referred to R. turanicus. However, attempts to transmit B. caballi and T. equi to horses transstadially from nymphs to adults with a South African strain of R. turanicus have been unsuccessful. Transovarial transmission of B. trautmanni by adult R. turanicus seems the most likely possibility in the field, because the immature stages of this tick do not normally feed on pigs.
Rhipicephalus (Boophilus) decoloratus
African blue tick, bloubosluis (Afrik.)
The tick genus Boophilus has become integrated into the genus Rhipicephalus, and is at most presented as a subgenus of Rhipicephalus 123 therefore all species of Boophilus have become Rhipicephalus spp. The species of Rhipicephalus which used to be assigned to a separate genus Boophilus because they share a one host type of parasitic behaviour (i.e. moulting from larva to nymph and from nymph to adult takes places on the same host animal), the anal groove is only faintly or not visible, and the males are abnormally small, are R. annulatus (the only species of this group occurring in southern Europe, northern Africa and northern sub-Saharan Africa), R. decoloratus (only in sub-Saharan Africa), R. geigyi (western and central sub-Saharan Africa), R. microplus (southern Asia, and from there transported by humans to many parts of the world, including parts of sub-Saharan Africa), R. australis (in Australia, New Caledonia and parts of Indonesia), as well as a little-known species confined as far as is known to small ruminants in the Middle East, R. kohlsi. There is little doubt that they are phylogenetically near to the classical Rhipicephalus spp., although they differ considerably in morphology and biology from other species of Rhipicephalus. Of the species occurring on cattle, R. annulatus, R. australis, R. decoloratus and R. microplus are all known to transmit Babesia bigemina, but only R. annulatus, R. australis and R. microplus are also vectors of the more pathogenic Babesia bovis, while the vector role of R. geigyi is not definitely known. The possible vector role of R. kohlsi is unknown.
Rhipicephalus decoloratus adults are small, inconspicuous ticks with short mouthparts and slender legs. The males, which are usually considerably smaller than the females, are brownish-yellow in colour and the darker coloured intestine is visible through the lightly sclerotized scutum (Figure 22). They can usually be found paired with the females. The engorged females are bluish-brown (Figure 23) and can be seen attached particularly to the face, neck, shoulders and escutcheon of cattle. (Figure 24)
Rhipicephalus decoloratus prefers cattle as hosts. In addition to cattle it frequently parasitizes horses, donkeys, sheep and goats.83, 113, 187, 191 Contrary to earlier observations it is commonly present in large numbers on several wild ungulate species, including Burchell’s zebra (Equus burchellii), impala, bushbuck, greater kudu, eland and sable antelope.66, 68, 80, 82 Rather unusually, African buffalo do not appear to be good hosts.74, 80, 106, 113
Rhipicephalus decoloratus has a one-host life cycle, in which moulting from larva to nymph and nymph to adult takes place on the host. The time spent on the host, from attachment of the unfed larva until detachment of the engorged female, is approximately three weeks, and that spent off the host, from pre-oviposition until larval hatching and maturation, approximately five weeks. Because of this short life cycle the tick is able to pass through more than one generation annually, and is usually present in varying numbers throughout the year. In southern Africa low winter temperatures synchronize egg development and larval hatching. Consequently large numbers of larvae are present on the vegetation when the weather warms in spring.177 Waves of larvae then occur throughout the summer and into the cool months of May and June. In South Africa the largest numbers of ticks are usually present on cattle during the summer and autumn to early winter months,35, 159 but a spring peak in abundance may also occur. In Zambia a spring peak may be followed several months later by a considerably larger late summer or winter peak.149 In Nigeria, north of the equator, R. decoloratus is most abundant on cattle during autumn, while in the Gambia peak burdens are present on these animals during the rainy season.116 On wild herbivores in South Africa the highest burdens are usually recorded in spring and, unless these animals are stressed because of disease or drought or other conditions, their late summer and autumn burdens are low.68, 71 Because of its one-host life cycle all stages of development occur on the host at the same time and the presence on a single host of approximately 70 engorged females can represent a total parasitic population exceeding 10 000 ticks.68
This tick is distributed throughout most of the moister regions of South Africa, except for areas where it has been replaced by R. microplus, and also occurs in cold mountainous regions such as the Drakensberg range and parts of Lesotho. It is absent from those parts of South Africa that receive an average annual rainfall of less than 380 mm, including the western Free State, and the western regions of the Northern Cape Province.84 In the semi-arid to arid territory of Namibia it is present only in localized areas in the north, and in Botswana it is restricted to the higher rainfall eastern border areas and a few scattered northern localities.188 Rhipicephalus decoloratus is also present in southern Mozambique, Zimbabwe, particularly the eastern regions, Angola, much of Zambia, Malawi, south-western and northern Tanzania, Burundi, Uganda, western Kenya, the Sudan and in the wetter highlands and sub-highlands of Ethiopia.113, 115, 147, 187 In Central and West Africa it is replaced by R. geigyi. It occurs in various vegetation types, including coastal mosaic, grassland, Cape shrubland, bushland, woodland and in undifferentiated montane vegetation.
Babesia bigemina, the cause of bovine babesiosis or African redwater; Anaplasma marginale, the cause of bovine anaplasmosis. Eland can be asymptomatic carriers of A. marginale and could thus serve as a reservoir of infection for domestic cattle. Rhipicephalus decoloratus is also suspected of being a vector of Babesia trautmanni, the cause of porcine babesiosis. However, the small numbers encountered on warthog, even in regions where large numbers of this tick are present, make this seem unlikely under field conditions.
Because R. decoloratus spends approximately 21 days on its hosts to complete its parasitic life cycle it can effectively be controlled by acaricide treatment of cattle at three-weekly intervals. Bos indicus and Sanga-type cattle develop a considerably better resistance to this tick than European Bos taurus cattle 160, 161, 174 and consequently require fewer acaricide treatments.
Rhipicephalus (Boophilus) microplus
Asian blue tick, Asiatiese/pantropiese bloubosluis (Afrik.)
Adults of R. microplus are slightly larger than those of R. decoloratus, and are slightly more red in colour, but are otherwise very similar in general appearance.
In sub-Saharan Africa domestic cattle are virtually the only hosts and other livestock species and wild ungulates are rarely parasitized, and then only if cattle infested with this tick are present.113
Rhipicephalus microplus has a one-host life cycle, and like R. decoloratus is able to complete more than one generation in a year. In Zimbabwe it appears to be present in variable numbers throughout the year.113 In south-eastern KwaZulu-Natal, South Africa, it is most abundant on cattle from mid- to late summer.
Hoogstraal60 postulated that R. microplus was introduced into East and South Africa from Madagascar, where it had originally arrived with cattle from southern Asia. In South Africa it is now established in scattered areas along the southern and eastern coasts of the Western and Eastern Cape provinces and of KwaZulu-Natal. It is also present in the coastal regions of Mozambique, Tanzania and Kenya. In the interior of the subcontinent it is found in scattered localities in the Mpumalanga and Limpopo provinces of South Africa, in both the south and north of eastern Zimbabwe, in parts of the Eastern and Central provinces of Zambia, throughout Malawi and to the east and north of Lake Malawi in Tanzania.83, 113, 187 There is evidence that where favourable moist and warm climatic conditions exist it competes with and is able to replace the indigenous R. decoloratus.113, 177 Rhipicephalus microplus spread into Zimbabwe in the 1970s, when dipping was disrupted during the pre-independence war, and replaced R. decoloratus in several areas.113 Longterm surveys conducted in eastern Zambia revealed that R. decoloratus had almost completely been replaced by R. microplus in the 10 years between 1972 and 1982,11 and its westward spread appears to be continuing.88 The spread of R. microplus in Zimbabwe has been accompanied by heavy mortality in cattle due to B. bovis infection, which is not transmitted by R. decoloratus.135
The known distribution and ecological preferences of Boophilus ticks as compiled and published in 2005 has dramatically changed.39 Importantly, R. microplus was introduced inadvertently with imported Brazilian cattle into West African countries, initially into Ivory Coast, which was reported in 2007 16, 108 and in the years thereafter quickly spread further into Mali, Burkina Faso, Togo and Benin.107 Although R. microplus had not been found in Nigeria in a survey conducted in 2010,103 the tick was discovered among other livestock ticks collected from cattle during a more recent nationwide survey conducted between April 2015 and March 201593 and it has recently been discovered in Angola. Important also is that the population of ticks introduced into Ivory Coast with Brazilian cattle is multi-resistant to acaricides. The spread of R. (B). microplus ticks on cattle is dramatic 10, 16, 107, 108 and has now replaced most indigenous R. decoloratus populations in large geographical areas throughout West, East and southern Africa.104 It is likely that the tick has already spread further unnoticed. For instance, the tick was reported not to have reached Cameroon as part of a tick surve conducted between March 2012 and February 2013. However, there is no reason to believe that it will not have done so in the meantime. Another example concerns Uganda, where it was recently discovered that R. microplus replaced B. decoloratus in the southeastern part of the country where it had not been reported before.115 (F.Jongejan and D.Muhanguzi, unpublished findings, 2017).
Babesia bovis, the cause of bovine babesiosis or Asiatic redwater; Babesia bigemina, the cause of bovine babesiosis or African redwater; Anaplasma marginale, the cause of bovine anaplasmosis. Because this tick transmits both B. bovis and B. bigemina it poses a greater potential threat to livestock production than R. decoloratus. Despite this fact, the recent spread of R. microplus has not been reported to be associated with any significant disease outbreaks of bovine babesiosis, as has been previously reported from Zimbabwe 135 and Zambia.86 Since these outbreaks have occurred in improved cattle breeds, it is likely that the indigenous cattle breeds have a genetic capability to cope with the disease.
The control of R. microplus is similar to that of R. decoloratus. Bos indicus-type cattle develop a considerably better resistance to this tick than European Bos taurus-type cattle and consequently the number of acaricide treatments required can be reduced on these animals.144 However, because R. microplus feeds virtually exclusively on cattle, the whole parasitic population is exposed to acaricidal intervention at any particular location as there are no alternative hosts. Because of this and its slightly shorter life cycle it would appear as if R. microplus is more prone to resistance to acaricides more rapidly than is R. decoloratus.
Rhipicephalus (Boophilus) annulatus
This is the only species of the subgenus Boophilus that occurs in the Mediterranean area, but scattered populations also occur in the north of sub-Saharan Africa, co-existing with R. decoloratus and/or R. geigyi.
It is very similar to R. decoloratus, but could be more important as it is a good vector of B. bovis. Like the other species it also transmits bovine erythrocytic anaplasmosis.
Rhipicephalus (Boophilus) geigyi
Rhipicephalus geigyi replaced R. decoloratus in western and central sub-saharan Africa. It can be distinguished on morphological grounds from this species. Little is known of its vectorial role but it is likely a vector of at least B. bigemina. Rhipicephalus geigyi was reported for the first time on a tiang (Damaliscus lunatus tiang) in the Sudan.90
Other Rhipicephalus species
Two Rhipicephalus spp., other than those already mentioned, have been implicated as the cause of livestock paralysis (toxicosis), namely, Rhipicephalus warburtoni (previously recorded as an undescribed species of the R. pravus group or as R. punctatus) and R. praetextatus (previously recorded as R. simus).
The adults of R. warburtoni prefer domestic goats as hosts and the immature stages rock elephant shrews.46 However, all stages may be encountered on scrub hares and Cape hares (Lepus capensis).72 On very young Angora goat kids adult ticks attach to the head and ears, while on older goats they attach here as well as on the neck and the brisket.48 Rhipicephalus warburtoni is a three-host tick of which the adults are most abundant on goats from September to February, and the larvae ( from December to July) and nymphs (from April to October) on elephant shrews.46 In South Africa, it is found only in the Free State and Northern Cape provinces.189 Acaricide can be applied to the heads and ears of very young goat kids to prevent paralysis.
Rhipicephalus praetextatus adults and immature stages have a host preference similar to that of R. Simus.150 On cattle the adults attach mainly to the tail brush and the feet. Rhipicephalus praetextatus is a three-host tick, and its adults are most abundant during the rainy season.150 This tick is widespread in north-eastern Africa from Egypt to Tanzania.189, 150 Not only can it cause paralysis, but it can also transmit the virus causing Nairobi sheep disease.
Several other Rhipicephalus spp. have a more local distribution, or are rarely encountered on domestic animals.
Ornithodoros moubata and O. porcinus
In general, the Argasids or “soft” ticks are not of great importance in Africa for livestock, apart from two species (Ornithodoros moubata and O. porcinus) of the Ornithodoros moubata complex.
The eyeless tampans belonging to the argasid complex lack the sclerotized dorsal scutum that characterizes the hard ticks, and their integument has a mammilated appearance (Figure 25). Male and female ticks can only be differentiated with certainty under a stereoscopic microscope.
Hosts and life cycle
Ticks of the O. moubata complex are parasites of warthog, and complete their life cycle in warthog burrows. The adult female tick lays a batch of eggs in a sheltered locality in the burrow after each blood meal. After hatching the larvae do not feed, and they moult to the first nymph stage after one or two days. The first nymph stage seeks a warthog host on which it feeds briefly before moulting to the second nymph stage in the burrow. This process is repeated for each of the four or five nymph stages, with the last nymph stage moulting to an adult. The feeding periods of the various nymph stages and the adults are of short duration (approximately 30 minutes), and feeding takes place when the warthog hosts are at rest in their burrows. The nymphs can survive for two years without feeding and the adults even longer.
The only host of O. porcinus in Madagascar appears to be the domestic pig. The ticks live in walls and cracks of pigsties. Warthogs are absent from the country.
The distribution of ticks of the O. moubata complex follows that of their warthog hosts, which still occur in large areas of southern Africa. However, as the density of human habitation increases, these areas are decreasing in size and in number. The ticks are spread via their nymphal stages, which are commonly found on foraging warthogs.66, 182
The virus causing African swine fever (ASF) is spread from male to female ticks by means of the spermatophore during matin.157 It is transmitted transstadially and transovarially by the ticks. 158 Some other species of Ornithodoros can also maintain the infection; ticks of the O. erraticus complex occur in western and northern Africa, the Iberian peninsula and western Asia. They often live as endophilic ticks, in the walls of pig-sties, and appear to be able to maintain ASF indefinitely. African swine fever virus is also easily transmitted directly by contact without tick vectors.
Warthogs should be sprayed with an acaricide prior to translocation.
Other members of the Argasidae are not of great economic importance.186 Ornithodoros savignyi (eyed tampan) can infest animals and humans resting in the shade in some desert or semi-desert areas of Africa. It doesn’t transmit any infectious agents but causes stress and toxaemia in its victims. Otobius megnini, refer to as the spinose ear tick, has been introduced accidentally from the New World into South Africa. The larvae enter the ear cavities of their host, usually a large mammal, where they moult and develop to nymphal stages. The last nymphs drop several months after the larvae entered the ear cavity and moult to adults that do not feed and the females oviposit outside the host. The nymphs have external spines that irritate the host. Otobius megnini also occurs in Madagascar, several countries in southern Africa and Kenya.
Control of ticks and tick-borne diseases
Cattle have been present in Africa for more than a thousand years, and until the twentieth century survived without specific control measures against ticks and tick-borne diseases. It is now known that cattle can develop resistance to ticks, with the level of resistance developing in indigenous Sanga and Zebu breeds being much higher than that in European Bos taurus cattle;141, 160, 161, 174 indigenous Zebu and Sanga cattle will also acquire immunity to the indigenous tick-borne diseases if exposed to them at an early age, at a much higher level of immunity than imported Zebu or European Bos taurus can acquire.132 Situations in which cattle acquire immunity to tick-borne diseases through natural exposure as calves are called endemically stable. Most losses due to tick-borne diseases occur in endemically unstable situations, where there are insufficient infected ticks to ensure that all calves receive challenge. Endemic instability exists in areas that are only marginally suitable for the survival of the tick vectors or where tick populations have been suppressed but not eradicated through the use of acaricides. Tick-borne diseases also cause losses if they are introduced, together with their vectors, to new regions and spread through susceptible livestock populations, or if susceptible animals, especially exotic breeds, are moved to endemic areas.
Control measures against ticks and tick-borne diseases were only instituted on a large scale in southern Africa following the introduction of East Coast fever (caused by strains of Theileria parva) from East Africa. Prior to that, tick-borne diseases had not been reported as problematic in indigenous cattle, although losses caused by babesiosis and heartwater had been experienced in imported exotic cattle.151 One of the most serious tick-borne disease problems of the nineteenth century was the spread of heartwater through the coastal areas of the Eastern Cape Province because of the spread of the vector A. hebraeum, introduced by cattle which had been taken to KwaZulu-Natal for winter grazing. The other was the occurrence of babesiosis in cattle imported for restocking following the rinderpest pandemic of 1896.151
East Coast fever eradication
East coast fever which was introduced to Mozambique, Zimbabwe and South Africa in 1901/02, caused mortality of around 95 per cent in the herds of susceptible cattle (indigenous and exotic) to which it spread. It caused serious economic losses, affecting agriculture, mining and commerce, all of which still used ox-drawn transport. Considerable effort was therefore devoted to the development of control measures. Early attempts at vaccination by the eminent microbiologist Robert Koch and later by Sir Arnold Theiler were largely unsuccessful. However, once it was shown by Lounsbury that the disease was transmitted by the brown ear tick, R. appendiculatus, more successful control measures based on tick control, quarantine procedures, pasture spelling, slaughter, and dipping in arsenic solutions were instituted. Dipping proved to be the most practical and effective measure. It was widely adopted and later made compulsory. As a result, the disease was brought under control fairly rapidly and then progressively eradicated. Complete eradication of East Coast fever from southern Africa was considered to have been achieved by 1960.
Other tick-borne diseases
After the eradication of East Coast fever two options were open to southern African countries. They could either control the remaining major tick-borne diseases (babesiosis, anaplasmosis and heartwater) by vaccination and move towards reduced tick control and endemic stability, which had previously existed, or they could continue to control the diseases by intensive dipping. In South Africa, compulsory dipping was first abolished on commercial cattle farms and the choice of control strategies was left to individual farmers. In the communal grazing regions of the Eastern Cape Province the management of the dipping service was handed over to the former homeland administrations during the 1970s. Although the service was maintained by these administrations, enforcement of the dipping programme was gradually relaxed and abolished after independence of the Transkei and Ciskei in 1975 and 1981 respectively. When these regions were reincorporated into South Africa in 1994 the Provincial Departments of Agriculture assumed responsibility for the dipping service and supplied both personnel and chemicals. Despite the relaxation of enforcement 98 per cent of livestock owners interviewed continued to partake in all dipping events, with disease control given as the main reason for participation.112 Compulsory dipping has now been abolished throughout South Africa. However, the provinces of KwaZulu-Natal and Mpumalanga still provide personnel and chemicals in the communal grazing areas and report good attendance at each dipping event.
The dipping policy in South Africa has had mixed results. Some progressive farmers took advantage of the availability of vaccines against babesiosis, anaplasmosis and heartwater, used them effectively, and were able to adopt flexible dipping regimes. Others, for reasons that were probably only partially understood, practised little or no tick control and contained tick-borne diseases through the maintenance of endemic stability. The majority, however, continued to treat cattle at regular intervals with acaricides. Few actually succeeded in eradicating ticks or tick-borne diseases,29, 30 and frequently the effect in endemic areas was to maintain instability where stability would otherwise have existed. In these circumstances losses due to tick-borne diseases commonly occurred if vaccines were not regularly used.
In Zimbabwe compulsory dipping continued to be enforced after the eradication of East Coast fever. However, it should be noted that Zimbabwe theileriosis caused by strains of T. parva persisted and it was partly for the control of this disease that compulsory dipping was continued. For 20 years after the eradication of East Coast fever, tick-borne diseases were effectively controlled in Zimbabwe by dipping. Control was particularly good in the communal farming areas, where dipping, together with overgrazing, which rendered the environment less suitable for tick survival, frequently resulted in the localized eradication of ticks. However, this situation came to an end in the mid-1970s with the disruption of dipping in these areas during the pre-independence war. Large epidemics of tick-borne diseases occurred and losses over a five-year period amounted to more than a million head, which was one-third of the cattle owned by traditional farmers.129, 151 These losses caused the Zimbabwe veterinary authorities to re-assess the national policy on tick and tick-borne disease control. After independence in 1980, dipping was reintroduced in the traditional farming areas, but was not strictly enforced. From 1985, a similar approach was adopted for commercial farmers, who were only required to have tick-free cattle if the animals were to be moved off their properties.
Intensive dipping is still practised in Swaziland, but is not as strictly enforced as in the past. In other countries in the region, including Namibia, Botswana and Angola, intensive dipping is not widely practised or enforced. It has been more extensively used in Malawi, Zambia and Mozambique for the control of theileriosis and heartwater, but not throughout each of these countries.
No movement away from intensive tick control can be made unless it is possible to control tick-borne diseases of cattle (and sometimes those of other livestock) by immunization, and then to manage the diseases to ensure continuing immunity. Management may involve regular immunization of calves or simply the maintenance of endemic stability through tick exposure. Fortunately, in East Coast fever-endemic areas the infection and treatment method to induce immunity against the disease is now commercially available in East Africa. A detailed account of the biology of Theileria parva and control of East Coast fever (see East Coast fever) is provided elsewhere.127
Debate in southern Africa on the role of acaricides for the control of tick-borne diseases was most intense in the early 1980s. By then there was considerable evidence from epidemiological studies that endemic stability was more widespread than previously believed and that intensive dipping frequently contributed to problems with tick-borne diseases.29, 30, 88, 135 It was argued by many people that strict tick control was necessary to prevent large production losses.
Tick resistance in various breeds of cattle has been compared in several countries in sub-Saharan Africa. These comparisons have demonstrated that Sanga and Zebu cattle are considerably more resistant to the commonly occurring tick species than are European B. taurus cattle, and that crossbred cattle show intermediate resistance.140, 160, 161, 171, 174 In fact, farmers in the traditional sector almost entirely rely on the enhanced genetic resistance of their animals to ticks and tick-borne diseases in sub-Saharan Africa. This also implies that upgrading their stock with more productive genetic traits is severely limited by ticks and associated diseases.121
Acaricidal tick control
Classes of acaricides. The control of ticks infesting livestock almost entirely depends on the usage of commercial, synthetic acaricides. The acaricides that are available on the market throughout Africa for farmers consist of five major classes of molecules. Organochlorines such as lindane and dieldrin, are excluded from this list, since they have now been banned due to their toxicity and prolonged persistence in the environment. Organophosphates (such as coumaphos, dichlorvos and diazinon), all acetylcholine esterase inhibitors, carbamates (carbaryl), a cholinesterase inhibitor, the synthetic pyrethroids (cypermethrin, deltamethrin and many others) are sodium channels modulators. Amitraz is the best know acaricide of the formamidine class, which act as octopamine agonists. The fifth class is the macrocyclic lactones (avermectines and milbemycins), acting as chloride channel activators.12
It should be noted that there are additional classes of acaricidal compounds that have not been used against ticks on African livestock for various reasons. These include the phenylpyrazoles (fipronil as best known compound) which binds to GABA-gated chloride channels and pyriproxyfen which is an insect growth regulator of the juvenile hormone analogue group.
Isoxazolines the recently discovered ixoxazolines have caused a “revolution” in the control of ticks and flies on companion animals as they can be administered orally and have a long- lasting efficacy.52, 167 Importantly, one of the recently discovered isoxazolines was topically applied to cattle and proved highly effective against Haematobia irritians (horn fly).
It will probably be only a matter of time before fipronil, pyriproxifen and the novel isoxazolines become available against African livestock ticks.
Acaricide resistance. Acaricide resistance against cattle ticks is a major concern in the one-host Rhipicephalus (Boophilus) ticks and in particular R.(B.) microplus.1 Two- and three-host ticks are much less exposed to acaricidal treatments and have therefore a lower probability of developing resistance.124, 143 Management of acaricide resistance is a global problem and has been extensively discussed and reviewed,25, 43 including intervention strategies (e.g. rotational acaricidal usage, co-formulations and applications, such as plunge baths, pour-on, spray-races and footbaths).1, 53 Integrated tick management strategies for the control of R. (B.) microplus ticks and resistant to conventional acaricides and macrocyclic lactones have been reviewed recently.164
In brief, acaricides from different chemical groups or combinations of acaricides can be applied alternately. When resistance is already present, animals must not be treated with an acaricide from the chemical group to which resistance is evident before moving them to clean or rested pasture, as this will result in the new pasture becoming contaminated with resistant ticks. An acaricide from a completely different group should be used in such an event. Experience with acaricide resistance management elsewhere in particular in Latin America and India could also be useful for the control of African livestock ticks.1, 126
Strategic tick control
Acaricides are applied during strategic times of the year in order to control seasonal peaks in tick abundance. It is aimed mainly at adult ticks to decrease numbers to levels at which economic damage is less than the cost of control. On the other hand, acaricidal applications can be opportunistic and applied only when tick numbers are considered to exceed the economic threshold. This strategy is effective when animals possess a high level of resistance to ticks or in regions where ticks are only sometimes a problem because of favourable climatic conditions. Furthermore, only those animals with tick burdens considered to be above the economic threshold should be treated. This is more easily achieved with small herds of cattle and should reduce both treatment costs and delay the development of acaricide resistance.
Adult Amblyomma variegatum ticks infest the feet of cattle while they graze and as many as 90 per cent of the ticks move during the night to their predilection sites. Making cattle walk through a footbath when returning from pasture at night, will decrease the adult A. variegatum burden considerably and reduced amount of acaricide will be used.28, 179 A further field assessment in Burkino Faso indicated that, despite the scientific evidence of the efficacy of this approach to control A.variegatum, large scale adoption of it was constrained by the traditional husbandry system that is based on cattle transhumance where a fixed footbath device did not fit.28
Alphametrin-impregnated eartags that have been developed and tested against various tick species on cattle revealed a superior efficacy against the brown ear tick, R. appendiculatus, whereas little or no effect was seen against adult R.(B).decoloratus, R. evertsi and A. hebraeum.165 Interesting these eartags could not prevent the transmission of East Coast fever in a field trial in Kenya.195 Despite this, there seems to be an opportunity to target an important vector tick, such as Rhipicephalus appendiculatus, which exclusively feeds in and around the ears of cattle.
Pheromone/acaricide impregnated tailtags. A combination of biological and acaricidal control has been successfully incorporated in pheromone/acaricide- impregnated plastic tailtag decoys.3 These tags were specifically designed for the control of adult A. hebraeum and A. variegatum, of which the feeding males exude a pheromone that is particularly attractive to other males, females and nymphs of the same species. The incorporation of squalene (a naturally abundant mammalian skin secretion that has a long-distance tick attractant effect on Amblyomma americanum) may provide definite advantages in the control of Argas ticks. Recent research in the Caribbean demonstrated this method to be beneficial 94 and its application should be further investigate in sub-Saharan Africa against a range of Argas spp.
Non-acaricidal tick control
There are several ethno-ecological approaches in use by traditional African farmers in particular.97 Participatory research among these farmers showed that hand picking of ticks are often included as a means to reduce tick burdens.22, 28, 96, 180 If, on a daily basis during milking, in particular Argas female ticks are removed from their predilection sites (udder etc), this should have a significant effect in reducing subsequent tick challenge, provided that those ticks are destroyed rather than left to oviposit in the environment.
This implies to avoid camps that are heavily infested with ticks during certain seasons. For example sheep and goats must not be grazed in camps on the southern aspect of hills or mountains in the Karoo, South Africa, during autumn and winter. The Karoo paralysis tick, I. rubicundus, is most abundant in this type of habitat and is present only from late summer to spring. Goats and cattle can be grazed in sheep camps during summer to denude shrubs and keep the grass short, thus eliminating favourable breeding or questing sites for the ticks.
With ticks, such as two-host Rhipicephalus species, that take less a year to complete their life cycles, pastures can be rested from the end of the season of adult tick abundance until the commencement of the following year’s season of adult abundance. Provided no hosts suitable for the immature stages are allowed on to the pastures during the intervening months, most of these ticks should have died and the numbers of adults present when the livestock are reintroduced should be minimal.
In much of southern Africa it is common practice to burn natural pastures once every two or three years during spring to control shrub invasion and remove dead plant material. These deliberate fires coincide with the post-winter synchronous hatching of R(B). decoloratus larvae and with their questing on the vegetation and consequently many are destroyed. However, the short-term effect on tick abundance does not compensate for the damage inflicted on some vegetation types by regular burning. Ticks hiding in cracks in the soil are not destroyed.
A high stock density may initially favour the propagation of ticks because of the abundance of hosts. However, should stock numbers become too large the habitat may be damaged to such an extent that it becomes unfavourable for the survival of some tick species. Human perturbation of the environment by chopping down trees for firewood or removing them in order to establish pastures can have the same effect.
Although several agents are effective or partially effective for the biological control of ticks it is unlikely that many of these will be commercially viable. Nevertheless, under natural conditions these agents may play a significant role in reducing tick numbers.
Domestic chickens and wild birds
Domestic chickens are opportunistic predators of ticks. The indigenous varieties in particular, if allowed to scavenge amongst cattle, can consume considerable numbers of ticks, especially if the cattle are penned close to dwellings in the late afternoon and during the early morning.34, 58, 59 Moreover, red- and yellow-billed oxpeckers (Buphagus erythrorhynchus and Buphagus africanus), which are virtually obligatory predators of ixodid ticks, take large numbers of these parasites from both domestic cattle and from several wildlife species.14 The red-billed birds favour R. decoloratus and R. appendiculatus as food items.14 whereas yellow-billed oxpeckers prefer the latter tick and Amblyomma spp.185 As an aid to tick control on both wildlife and domestic cattle, red-billed oxpeckers have been reintroduced to several regions in which they originally occurred in South Africa, but from which they had in recent times disappeared.
Chalcid wasps of the genus Ixodiphagus are obligatory parasitoids of ixodid ticks and most species will oviposit and develop only in the nymphal stage of the ticks. Several wasp larvae can successfully develop in a single engorged nymph, which is killed during this process. Two of the seven described species of these wasps occur in Africa, namely Ixodiphagus hookeri and Ixodiphagus theilerae.156 In Kenya adult I. hookeri were released over a period of one year into a field in which there were cattle naturally infested with A. variegatum and R. appendiculatus.125 In addition the field was seeded with nymphs of both tick species. During the period of wasp release 51 per cent of A. variegatum nymphs but no R. appendiculatus nymphs collected from the cattle were infested with the parasitoid. There was also a significant decrease in the numbers of A. variegatum infesting the animals compared to the numbers of ticks prior to wasp release and compared to a control group of cattle.125 In South Africa these wasps mainly parasitize the nymphs of ticks feeding on hares.156 They can be found around the resting places of the hares and parasitize particularly the nymphs of Hyalomma spp.156 which by preference feed on these animals.72, 81
The infective juveniles of nematode species that are pathogenic for insects can also be pathogenic for ticks. In Guadeloupe the infective juveniles of various species of Steinernema and Heterorhabditis had no effect on any of the free-living stages of A. variegatum or R. microplus originating from the island, whereas an imported strain of R. annulatus was susceptible to all of them.117 Unfortunately, despite all efforts, this has never resulted in any practical application available to farmers for tick control under African field conditions.97
These fungi have been used in several countries for the control of agricultural pests and their use for the control of ticks has been investigated at various localities, including South America. In Kenya aqueous formulations of the spores of the fungi Beauveria bassiana and Metarhizium anisopliae induced a high mortality and reduced fecundity and egg hatchability in R. appendiculatus feeding on cattle. These formulations also caused mortalities in all life stages of A. variegatum and R. appendiculatus in the vegetation. The comparative ease with which the spores of these fungi can be produced and artificially disseminated, makes them promising potential agents for the control of ticks, but so far results have been rather variable. Interestingly, Metarhizium anisopliae is now commercially available and being evaluated as part of an integrated tick management programme against Ixodes scapularis in the Eastern United States.37, 194 Moreover, the fungal product is also registered in Europe for the control of insect pests in glasshouses for horticulture.
There have been numerous attempts to develop non-toxic, low cost and environmentally friendly tick control methods based on botanical products as natural acaricides.17, 44 More than 200 plant species, which are traditionally used against ticks by rural communities of Africa, Europe and Asia, were selected. Most of these plants belonged to 7 families (i.e. Asteraceae, Euphorbiaceae, Fabaceae, Lamiaceae, Meliaceae, Apcynaceae and Solanaceae).145 Their acaricidal and repellent efficacy and strategies for their future application have been evaluated. Despite large efforts over several decades, very little if any applications have emerged. However, there are encouraging exceptions for example nootkatone, an extract from citrus and some other plants, has been tested for its repellency and acaricidal properties and has been developed and marketed by a pharmaceutical company.15 It should be remembered that the synthetic pyrethroids were originally derived from the active ingredients, pyrethrins from the flower heads of Chysanthemum species. Many factors may influence the activity and concentration of plant-derived products in plants including season, geography, type of soil, growth stage and part of the plant.
The only commercially available anti-tick vaccine is based on the recombinant antigen BM86 (Gavac). This field was first pioneered by the Australians who discovered a ‘concealed’ antigen, which is located on the surface of the digest cells that line the gut of R. microplus (australis), which could be used to immunize animals against infestation with this tick.95, 193 Bm86-based vaccine formulations have been evaluated for their use against tick species other than those of the R. microplus group. To this end, the original (now not any longer available commercial vaccine TickGARD) was tested for its ability to reduce the feeding success of a range of livestock ticks. It was found that there was a significant reduction in R. decoloratus, H. anatolicum and H. dromedarii, but not in R. appendiculatus and A. Variegatum.31, 163 However, the efficacy of Bm86 -derived from R. microplus (australis) appeared, surprisingly, much higher against R.(B). annulatus. This has led to the use of the Bm86 vaccine as a tool for the integrated eradication of the cattle fever tick, R (B) annulatus in Mexico and southern Texas.4, 120, 192 When this vaccine was tested in some countries in southern Africa, the resident R. microplus populations were compared with the populations from Latin America and Australia, and it was found that the American and African strains were the same, whereas the Australian strain was clearly different.98 This has led to the reinstatement of R (B). australis.40
With respect to the development of effective cattle tick vaccines, there are many candidate antigens available recently reviewed by Valle and Guerrero.184 More information on the development of anti-tick vaccines is provided in the listed references. 23, 26, 27, 31, 56, 87, 120
Control of African livestock ticks will continue to rely on the application of acaricides and other methods, since alternative non-acaricidal control methods such as anti-tick vaccines will not be readily available within the foreseable future. 41, 42, 85, 91, 166
For more information on the control of each of the major tick-borne diseases the respective chapters should be consulted.
Tick control on wildlife
Tick control on wildlife in nature reserves encompassing more than 20 000 ha should not be necessary, particularly if a sustainable number of large carnivores are present to remove stressed, weak, sick or injured animals. Problems with ticks usually occur in small wildlife reserves or on game farms, especially those under 1 000 ha in size, on which it is not practical also to keep the larger wild carnivores. Healthy wild antelopes and equids in Africa normally harbour tick burdens in excess of several thousand. 67, 68, 71 However, with the exception of large animals such as giraffe, African buffalo and eland, which may harbour large burdens of adult ticks, the majority of ticks parasitic on wildlife are usually larvae and nymphs.51, 64, 78 Severe adult tick infestations on wildlife are therefore frequently an indication of some underlying management problem. This might be gross overstocking,62, 102, 136 or overstocking with particular species such as eland, which are large animals that are highly susceptible to tick infestation.73, 101 It could also be due to the introduction of wildlife species not indigenous to a region and hence not adapted to the local tick species. In the latter event these animals may not only acquire enormous tick burdens but could also succumb to diseases such as heartwater or one of the theilerioses.
Before control measures are instituted the underlying cause of the problem should be addressed. One of the first steps in this direction would be to remove any animals that are visually very heavily tick infested as well as any diseased or weak animals. The latter animals are normally severely stressed and consequently harbour large tick burdens that can lead to contamination of their surroundings. Thereafter stocking density should be examined and corrected for each wildlife species in the reserve or on the game farm. Wildlife species that historically did not occur in the region could also be removed.
Provided the habitat is suitable, the introduction of species such as blue wildebeest could be contemplated. These animals have an innate resistance to ticks and remarkably few adult ticks are found on them in their natural habitat.64, 70 The introduction of oxpeckers can also be considered. This would only be feasible if the reserve or farm was located in a suitable habitat and was large enough to accommodate the birds, or if the surrounding cattle farmers use only acaricides that are not toxic to the oxpeckers. Although fire may kill large numbers of free-living ticks present on the vegetation at the time, its long-term effects seem to be limited, particularly if animals are not kept away from the burnt area once there is a flush of new vegetation.122, 176
Should chemical tick control be required, acaricide can be administered by means of a self-medicating applicator coupled to a bin containing licks or food concentrates to which the animals are attracted.36, 172 In South Africa several wildlife species are more inclined to take supplementary feed in such bins during the winter months because of the seasonal shortage of grazing.62 Consequently mainly immature ticks will be killed. Acaricide can be automatically applied to animals by constructing a single entrance to a watering point, thus forcing them to step on a pressureplate or interrupt a light beam that will activate a jetting or pour-on device.50, 119 Domestic cattle that are regularly treated with an acaricide, can also be used to control ticks on a small wildlife reserve. These animals can be introduced in the wet summer months when adult ticks are most abundant and can be herded during the day into those parts of the reserve where ticks are deemed to be most numerous. No new wildlife should be introduced on to a wildlife reserve or a game farm without having first been thoroughly treated with a reliable, broad-spectrum acaricide. This will reduce the risk of introducing ticks into a region in which they did not previously occur, as well as eliminating the stress of preexisting tick burdens on the new introductions.
The regular treatment of domestic animals on mixed cattle and game farms can result in a significant reduction in tick numbers on the wildlife on the farm. Those tick species that use cattle as hosts for all their developmental stages, or that prefer cattle as hosts for their adults are particularly affected by this procedure.77, 197
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