Bovine respiratory syncytial virus infection

Tick identification - The basics

"A rose by any other name would smell as sweet"

– Romeo and Juliet

Whilst some confusion in the naming of roses may not lead to serious consequences in a romantic setting, the same is not true for the specific designation of living organisms in the realm of scientific investigation. Phylogeny, systematics and taxonomy – utilising distinct principles – are all disciplines targeted at scientific classification, with the purpose of ordering and naming organisms as explicit entities – i.e. species. Such classification is the basis upon which all research outcomes related to a particular species, albeit biological, ecological, epidemiological or molecular, are grounded – with major significance for effective monitoring, surveillance and pragmatic control strategies of vector and disease organisms. By employing detailed morphological descriptions, familial relationships, biological descriptors, and, more recently molecular characterisation or genetic markers, the species entity is defined (and sometimes redefined with the advent of new knowledge) – with resultant discrepancies in the numbers of tick species currently recognised. Little difference in interpretation exists at the higher levels of classification (although the class Arachnida is designated by some as the subphylum Chelicerata). However, changes or additions – descriptions of new species, re-description of existing entities or novel discoveries – in the lower echelons, at genus and species level, may spark some controversy and even heated debate. Recent cases in question (mostly resulting from interpretations of molecular studies) involve disagreement concerning the genera in the family Argasidae (Guglielmone et al. 2010) and, in the family Ixodidae, elimination of the genera Aponomma, Anocentor and Boophilus (the latter delegated to a subgenus of Rhipicephalus). The contention is that these entities are still considered valid by some authors. Also within the family Ixodidae, revision of Hyalomma and the renaming of some species of Haemaphysalis – as recently as during the past decade – has resulted in the raising of some sub-species to species level, and the removal of others. Only time and the generation of additional knowledge will attest to the validity and overall acceptance of these decisions by the scientific community. These taxonomic changes may sometimes have far-reaching implications for the interpretation of extensive research on a particular species, which is accepted (deduced) as being equivalent to or similar to the same species elsewhere – should the former species be renamed as a separate entity.

Despite these changes and controversies, the species concept remains paramount, and fortunately, the major ixodid ticks of economic importance remain firmly ensconced as recognisable entities – with the designations herein following those proposed by Guglielmone et al. (2010) and Barker and Murrell (2004). Currently, South Africa hosts 85 species within the family Ixodidae, 21 species of Argasidae, and one species of Nuttalliellidae (as mentioned previously). The family Ixodidae includes the genera Amblyomma (9 species – inclusive of 3 from the now defunct genus Aponomma); Cosmiomma (1 species, Cosmiomma hippopotamensis, a rhinoceros tick, sadly on the brink of extinction in southern Africa, if not already extinct); Dermacentor (1 species, Dermacentor rhinocerinus, also a rhinoceros tick, still extant); Haemaphysalis (11 species); Hyalomma (3 species); Ixodes (23 species, mostly parasitic on birds, bats and rodents); Margaropus (1 species, Margaropus winthemi, the so-called winter horse tick, which also parasitises cattle); Rhipicentor (2 species); and Rhipicephalus (33 species, including the 2 controversial species, Rhipicephalus decoloratus and Rhipicephalus microplus of the subgenus Boophilus). The family Argasidae includes the genera Argas (13 species); Ornithodoros (7 species), and Otobius (1 species, Otobius megnini). Although many literature sources are available [e.g. Estrada-Pena et al., 2004; Hoogstraal, 1956; Walker et al., 2000 (Rhipicephalus species); Walker et al., 2003 (an excellent, very informative and practical guide to African ticks)] to those eager to attempt it – tick identification remains a specialist task and, generally, identifications are available as a diagnostic service. However, some salient morphological features used in tick identification are illustrated in Figure 1 – which will also serves to acquaint the reader with tick taxonomic terminology.

Figure 1 Dorsal and ventral aspects of an adult female tick, illustrating features and terminology.

 

Table 1. Morphological characters of the ixodid genera of southern Africa.

TAXONOMIC KEY: THE IXODID
  IXODES AMBLYOMMA AMBLYOMMA
(APONOMMA)
HYALOMMA COSMIOMMA
PALPS Long Long Long Long Long
ENAMELLED
PATTERN
Absent Present Absent /
Present
Absent Present
EYES Absent Flat to
hemispherical
Absent Orbited Hemispherical
ELEVEN
FESTOONS
Absent Present Present Usually
reduced
in number
Present
ANAL
GROOVE
Anterior
to anus,
semi-circular
open /closed
Posterior
to anus
Posterior
to anus
Posterior
to anus
Circular
around anus
ADANAL
PLATES
Several
flat plates
Absent Absent Anals,
accessory +
sub-anals
Anals
LEGS Slender,
uniform
Annulated Uniform Annulated Dorsal strip
FEMALES:
OTHER
FEATURES
        Alloscutum:
Soft patches
MALES:
OTHER
FEATURES
         
GENERA OF SOUTHERN AFRICA
DERMACENTOR RHIPICEPHALUS RHIPICEPHALUS
(BOOPHILUS)
MARGAROPUS RHIPICENTOR HAEMAPHYSALIS
Medium Medium Very short Short Short, spur
on article I
dorsally
Short,
triangular
Present Absent /
Present
Absent Absent Absent Absent
Present Flat to orbited Present Present Present Absent
Present Present Absent Absent Present Present
Posterior
to anus
Posterior
to anus
Indistinct
(posterior to
anus if visible)
Indistinct /
Absent
Posterior
to anus
Posterior
to anus
Absent Anals,
Accessory
+ / -
Anals +
accessory
anals
Anals +
accessory
anals
Absent Absent
Annulated Uniform /
annulated
  Yellow-brown,
annulated,
strongly
beaded
Uniform Slender,
uniform
Alloscutum:
Setous patches
         
Enlarged
coxa IV
Caudal
process:
+ / -
Caudal
process:
Present
Enlarged leg
IV
Enlarged coxa
IV, long spurs
 

Tick biology - life cycles, sex and more

“Ticks are generated from couch grass ... the ass has no lice or ticks, oxen have both ... among dogs Cynorhaestes are plentiful ”, Cynorhaestes interpreted to be ‘ricinus’ and considered as a ‘disgusting parasitic animal ’."

– Aristotle (355 BC) in Historia Animalium

“An animal living on blood with its head always fixed and swelling, being one of the animals which has no exit [anus] for its food, it bursts with over repletion and dies from actual nourishment. This [animal] never occurs on mules [and it is] frequent on cattle, sometimes on dogs on which all [kinds of lice] are found; on sheep and goats [ticks] only are found ”.

Pliny (AD 77) in Historia Naturalis [Quote from one of the ‘greats’ in tick literature: Don R. Arthur, 1965. Ticks in Egypt in 1500 B.C.? Nature, 206 (4988)]

Our understanding of the life histories of ticks has come a long way thanks to dedicated research spanning more than a century in South Africa. For one, we now know that a tick does indeed have an anus – for another, that Aristotle’s ‘couch grass’ is not the source of their ‘generation’ in a creative sense, but merely the substrate used by ixodid ticks to quest for a suitable host. For the rest, it is fortunate that ixodid tick biology may herein be described at the level of detail that requires little conjecture – thanks to the many research workers who have made this possible.

The Ixodidae

Ticks belonging to the family Ixodidae – which contains most ticks of veterinary importance – have four life stages: the egg, larva, nymph and adult (male and female). The last three stages feed during their parasitic phase, which they do by imbibing blood from a host through mouthparts of varying lengths. The mouthparts of Ixodidae are visible from the dorsal surface in all stages, and are superbly adapted for piercing and sucking (see Figure 2). During the feeding process, substances in the saliva cause ‘cementation’ of the tick to the host, so ensuring a solid attachment. Other salivary components cause the lysis or biochemical breakdown of host blood. Transmission of disease organisms occurs during the bloodsucking process. Concentration of the blood meal results in blood-meal-derived ‘water’ which ixodid ticks secrete back into the host via their salivary glands. Respiration or the exchange of gases takes place via an elaborate system of tubes or tracheae that have their origin on an external spiracular plate situated in the body wall, under leg IV (see Figure 3). The excretion of waste products – mainly guanine, which is a white creamy substance – takes place through the anus.

Figure 2 Ventral view of ixodid-tick mouthparts, showing palps (1) and hypostome (2) with recurved denticles that aid in securing attachment, and dorsal view of cheliceral sheaths with their minute denticles (3) and chelicera (4) – the ‘cutting edge’ that penetrates the host’s skin, enfolded by the cheliceral sheaths.

Figure 3 Scanning electron micrographs of spiracle (left) and enlargement of spiracular plate (right), illustrating tracheal apertures.

Ixodid ticks possess a hard dorsal shield (scutum) covering the entire dorsal surface of the adult male and about one-third of the area behind the head (or capitulum) of the female, nymph and larval stages. The remainder of the body wall or integument (alloscutum) is leathery in appearance and capable of extreme expansion – which enables the intake of relatively large volumes of blood. Male ticks, with the dorsal shield covering their dorsal surface, are rather restricted in their blood intake – however, this is not of concern as they only need sufficient energy to help them copulate frequently with available females (see Figures 4 and 5).

They mate by transferring sperm via a spermatheca from their genital opening – using their mouthparts – to the genital opening of the female. Most ticks mate on the host while members of Ixodes, can mate off-host. Mating during active-female feeding has a biological function, in that it signals the final phase of rapid female engorgement to repletion. The males of most ixodid species actively search for females that have commenced feeding, and females probably emit chemical recognition signals to searching males. After attachment to the host and an initial short period of feeding, males of the Bont tick, Amblyomma hebraeum, secrete a pheromone which attracts females (as well as nymphs and other males) to attach in their immediate vicinity. This may also result in clusters of feeding ticks, leading to extensive direct damage. Female ticks need a large blood meal, which provides the necessary protein for the production of eggs – ranging from c. 2 500 for smaller species to c. 25 000 for a fully-fed female tick (Amblyomma marmoreum, whose adults feed almost exclusively on tortoises). The number of eggs produced by a female ixodid tick is linearly directly correlated to her engorged mass (see Figure 6). The high reproductive capacity is to offset a low survival rate, estimated at less than 1% for ixodid-tick progeny. This low survival rate relates to the fact that they fail to encounter and successfully feed to repletion on hosts. When engorged and detached from the host, the female drops to the ground and deposits eggs as a batch of several thousand – depending on the species. She does this in a sheltered spot, waxing each egg individually for protection against the elements – by passing the eggs over her secretory Gene’s organ, which is situated dorsally at the base of her mouthparts. Egg-laying is preceded by a preoviposition period of varying length, dependant on the species, and, importantly, environmental conditions – primarily temperature and humidity – after which the expended female dies. Males may remain on-host for up to a few months, seeking newly attached and feeding females with which to mate before their energy is exhausted and they die. Egg development may take several weeks, or even months, again dependant on the tick species and environmental conditions. If the environmental conditions are suitable, the eggs hatch into pin-head-sized, 6-legged larvae. A short period of hardening follows after which the larvae climb up grass stems or bushes to form clusters, questing for a suitable host (see Figure 7). After feeding, the larva undergoes metamorphosis, casts off its skin and moults into a slightly larger 8-legged nymph, which in turn feeds for some days and moults into an 8-legged adult male or female – to complete one sequence of the cycle of life.

Figure 4 Fully engorged (fed) Rhipicephalus evertsi evertsi female with male in copulo.

Figure 5 Fully fed Rhipicephalus evertsi evertsi male.

Figure 6 Fully engorged (fed) Haemaphysalis female tick laying eggs.

Figure 7 An unfed questing Rhipicephalus appendiculatus male.

The length of the life cycle of an ixodid tick is dependent on three prime factors: the species, the availability of suitable hosts, and environmental conditions. The complexities presented by the last two factors, combined with adversity, may extend the life cycles of some species from months to even years, although man has provided suitable hosts for those tick species that favour livestock. A further compounding factor is that of host utilisation during the parasitic phase. This has evolved into three main categories of ixodid ticks:

  • One-host ticks where all three stages remain on the same animal from larval attachment until final drop-off as a fully-fed adult (i.e. moulting takes place on the host while still attached, leading to a relatively short bloodfeeding phase of c. 3 weeks). Representatives of this group in South Africa are Rhipicephalus (Boophilus) decoloratus and Rhipicephalus (Boophilus) microplus, which are known as the blue ticks
  • Two-host ticks are those of which the immatures, larvae and nymphs feed on one animal, and the engorged nymphs drop off to moult to adults that subsequently have to find a second suitable host on which to feed (e.g. Rhipicephalus evertsi eversti, the so-called red-legged ticks)
  • Three-host ticks that require a separate host animal on which to feed – for each stage.

Most ixodids are three-host ticks, with examples being Amblyomma hebraeum, the bont tick that transmits heartwater to ruminants, and Rhipicephalus appendiculatus, the brown ear tick that transmits theileriosis. Larval and nymphal stages do not always share the same palate in host preference as their adult counterparts. For example, all stages of Rhipicepahlus appendiculatus, the brown ear tick, will feed readily on cattle, whereas the immature stages of Hyalomma truncatum, one of the bont-legged ticks, are recorded on hares and rodents, while the adults prefer larger domestic animals and wildlife as hosts. It is therefore understandable that – even with optimal environmental conditions and host availability – the length of the life cycles of the two- and three-host ticks extend well beyond that of the one-host ticks. The length of the attachment and feeding period of the larvae, nymphs and females of most one-host, two-host and three-host ticks, is approximately 7 days for each developmental stage, whereas, as mentioned above, male ticks can remain attached for considerably longer periods.

Host-finding behaviour is fortuitous for most ixodids (by ambush off vegetation onto passing suitable hosts), and has been the subject of research to discover the questing height favoured by the different species, in order to access their preferred host. However, as cautioned by Gertrud Theiler, the esteemed research worker who established the fundamentals of tick ecology in South Africa, it must be remembered that even the tallest of animals have their feet on the ground. Also, whilst questing, ticks will ascend and descend the substrate in order to regulate their water balance according to the humidity, which is higher at the base of the substrate than at the top. Energy is expended during water regulation, so longevity on vegetation is determined by eventual energy depletion and desiccation. The nymphs and adults of Amblyomma hebraeum and the adults of Hyalomma species will actively pursue a potential host when their imminent presence is sensed via vibration and chemical signals (primarily CO) expelled by the host. These stimuli are registered by sensory organs which are illustrated in Figure 8.

There may be interspecific (between individuals of different species) and intraspecific (between individuals of the same species) on-host competition for the same resource. Interspecific competition is resolved to some extent by different species (and sometimes even stages) displaying different attachment-site preferences, although at high infestation levels these predilection sites may spill over into others. For example, on a bovine host, probably regulated by semiochemicals (chemicals that act as messengers within and between species such as pheromones, attractants and repellents) emanating from the host, predilection sites would be as follows:

  • Adults of the three-host bont tick (A. hebraeum) - predominantly on the ventral hairless areas, axillae, udder and perineum, and the immatures on the lower legs and muzzle
  • The one-host blue ticks [R. (B.) decoloratus and R. (B.) microplus] - on the shoulders, upper legs and flanks, with the latter of the two species tending to attach more on the flanks and rear (buttocks)
  • The two-host bont-legged ticks (Hyalomma species) - similar to those of the bont tick and also between the hooves and in the tail switch (Hyalomma truncatum)
  • Adults of the red-legged tick, Rhipicephalus evertsi evertsi - invariably around the anus and on the perineum under the tail, while its immatures attach within the ear canal and pinna – a site shared with the larvae and nymphs of a tampan, Otobius megnini (colloquially known as the spinose ear tick whose adults do not feed)
  • Adults of the three-host tick, Rhipicephalus appendiculatus, the brown ear tick – externally on the ear pinna, at the base of the ear, around the eyes and on the poll, while its immatures attach on the muzzle
  • Adults of the three-host glossy brown tick, Rhipicephalus simus – on the heels and in the tail switch.

Figure 8 Scanning electron micrograph detail of the ixodid tick claw (right) and Haller’s organ (left), which is located on the front legs and contains sensory setae and apertures associated with the recognition of chemical signals.

 

These predilection sites therefore represent areas where the various tick species cause direct damage to the host due to their attachment and feeding (e.g. abscesses in the axillae and on the udder and genitalia, sloughed and bleeding ears, and lameness).

The Argasidae

Ticks of the family Argasidae have a life cycle similar to that of the Ixodidae, although development progresses from the egg to the larval, nymphal and finally the adult stage, and the larvae may feed for several days. The larvae of some species, notably the tampans Ornithodoros savignyi and Ornithodoros moubata, are an exception in that they do not feed, and moult directly to the nymphal stage. Whereas there is only one nymphal stage in the life cycle of the Ixodidae, argasid ticks progress through at least two nymphal stages. The mouthparts of the Argasidae are positioned ventrally, invisible from the dorsal aspect, except in the larval stage, and they do not possess a hardened dorsal shield (scutum). Their highly convoluted, leathery integument thus covers the whole body, which is capable of extreme and rapid expansion to accommodate the rapid intake of blood during short-term (c. 15 minutes to an hour or so) intermittent feeding spells as nymphs and adults (another exception being adults of Otobius megnini, which do not feed, and the larval stage of Argas species that feed for a few days). During the rapid feeding of particularly the adult argasid ticks, the blood imbibed is biochemically processed and concentrated, in order to maintain the water balance. Excess fluid is secreted via coxal organs, and this may be observed during feeding, as an enlarging drop of liquid at the site of excretion. In the ancestral Nuttaliella namaqua, bloodmeal- derived water is secreted via the malpighian tubules. Argasid nymphal feeding is followed by moulting to the next nymphal stage (there may be up to five nymphal stages) or finally to the adults which partake in several brief intermittent blood meals during their lives, with the females laying small batches (hundreds) of eggs after each feed. The Argasidae are more exposed to the physical environment than the Ixodidae, so they need to seek protection in their physical surroundings. Some species shelter underground in sandy soils. The Kalahari sand tampan, Ornithodoros savignyi, can survive in colonies of several thousand for up to four years without feeding – in the sandy soils beneath the shade of a camel-thorn tree. This species is acutely sensitive to the presence of the host: the sensory setae on the first pair of legs detect vibrations, and the CO excreted by the approaching host is detected by Haller’s organ. Animals born and bred in the Kalahari are in fact said to avoid certain areas in order to prevent contact with these parasites. Other argasid species shelter in burrows, birds’ nests and fowl coops (Argas spp.). Argasid ticks mate off-host, and because they spend less time on hosts, the family are less exposed to the effects of acaricides, which makes them more difficult to control.

The impact of ticks in South Africa

(The good, the bad and the ugly)

“There will be no sores and the wool will be more plentiful and in better condition and the ticks (ricini) will not be troublesome”

– M. Porcius Cato (c. 200 BC)

Ixodid ticks are amongst the most economically important external parasites of livestock in the tropical and subtropical regions of the world – including South Africa. Heavy infestation can cause loss of blood, reduce the rate of live-weight gain, and lower milk yield, while the long-mouthpart ticks downgrade the quality of hides and cause abscesses due to secondary bacterial infections and blowfly strike (myiasis). Ticks are also recognised world-wide as major vectors of a number of diseases of man and domestic and wild animals – ranging from arboviruses, rickettsiae and spirochaetes, to parasitic protozoa. They act as reservoirs and/or multipliers of these organisms and transmit a number of important diseases of livestock – such as heartwater, babesiosis (redwater), anaplasmosis (tick-borne gallsickness) and theileriosis (so-called ‘Corridor disease’ in South Africa). Some ixodid ticks also produce toxins which cause paralysis – for example, Karoo paralysis and the dermatitis called ‘sweating sickness’ in calves.

Research on ticks and tick-borne diseases since the time of Arnold Theiler in the early 20th Century, has ensured that South Africa has an extensive understanding of its ticks and the diseases they transmit. These findings are documented in a wide range of publications, including Coetzer & Tustin (2004) and Walker, Keirans & Horak (2000). In the South African context, some 85 ixodid and 21 argasid tick species have been identified. Of these, some 35 ixodids and 5 argasids are normally associated with domestic animals, and approximately 10 ixodids are considered to be of major economic importance. These species transmit or are associated with some 24 diseases/disease syndromes. The livestock diseases of economic importance, animals affected, and the association with tick species, are summarised in Table 2.

Table 2 List of economically important diseases, livestock hosts affected, and tick species incriminated in South Africa.

Transmissible diseases
Disease (organism) Animals affected Vectors
Heartwater
(Ehrlichia ruminantium)
Cattle, sheep, goats Amblyomma hebraeum, the South African bont tick
Babesiosis or African redwater
(Babesia bigemina)
Cattle Rhipicephalus (Boophilus) decoloratus, the blue tick
Rhipicephalus (Boophilus) microplus, the Asiatic blue tick
Babesiosis or Asiatic redwater
(Babesia bovis)
Cattle Rhipicephalus (Boophilus) microplus, the Asiatic blue tick
Anaplasmosis, tick-transmitted
gallsickness
(Anaplasma marginale)
Cattle Rhipicephalus (Boophilus) decoloratus, the blue tick
Rhipicephalus (Boophilus) microplus, the Asiatic blue tick
Hyalomma rufipes, the large, coarse bont-legged tick
Anaplasmosis
(Anaplasma centrale)
Cattle Rhipicephalus simus, the glossy brown tick
Rhipicephalus decoloratus, the blue tick
Corridor disease
(Theileria parva – ‘buffalo
associated’)
Cattle,
(African buffalo as carriers)
Rhipicephalus appendiculatus, the brown ear tick
Rhipicephalus zambeziensis
Benign bovine theileriosis –
mild gallsickness
(Theileria mutans)
Cattle Amblyomma hebraeum, the South African bont tick
Rhipicephalus appendiculatus, the brown ear tick
Rhipicephalus evertsi evertsi, the red-legged tick
Equine biliary fever
(Babesia (Theileria) equi)
Horses, mules, donkeys Rhipicephalus evertsi evertsi, the red-legged tick
Crimean Congo Hemorrhagic
Fever virus
Humans,
ostriches, cattle and
wildlife act as reservoirs
Hyalomma rufipes, the large, coarse bont-legged tick
Hyalomma truncatum, the small, smooth bont-legged tick
Hyalomma glabrum, the enamelled bont-legged tick
African Swine
Fever virus
Pigs Ornithodoros moubata (porcinus), the eyeless tampan
Canine biliary (Babesia rossi
previously Babesia canis)
Dogs Haemaphysalis elliptica (previously H. leachi), the yellow dog tick
Rhipicephalus sanguineus, the kennel tick
Tropical canine pancytopaenia –
rickettsiosis
(Ehrlichia canis)
Dogs Rhipicephalus sanguineus, the kennel tick
Spirochaetosis
(Borrelia theileri)
Cattle, sheep, horses
donkeys, mules, goats
Rhipicephalus decoloratus, the blue tick
Rhipicephalus evertsi evertsi, the red-legged tick
Fowl spirochaetosis
(Borrelia anserina)
Fowls Argas walkerae (previously persicus), the fowl tampan
Fowl aegyptianellosis
(Aegyptianella pullorum)
Fowls Argas walkerae, the fowl tampan
Tick-bite fever – Mediterranean
spotted fever
(Rickettsia conori)
Humans Amblyomma hebraeum, the South African bont tick
Haemaphysalis elliptica, the yellow dog tick
Hyalomma rufipes, the large, coarse bont-legged tick
Rhipicephalus appendiculatus, the brown ear tick
Rhipicephalus evertsi evertsi, the red-legged tick
Rhipicephalus sanguineus, the kennel tick
Rhipicephalus simus, the glossy brown tick
African tick-bite fever
(Rickettsia africae)
Humans Amblyomma hebraeum, the South African bont tick
Diseases attributable to tick toxins or mechanical damage (Otobius)
Disease Animals affected Vectors responsible
Karoo paralysis Mainly sheep and goats Ixodes rubicundus, the Karoo paralysis tick
Spring-lamb paralysis Lambs and sometimes calves Rhipicephalus evertsi evertsi, the red-legged tick
Rhipicephalus evertsi mimeticus, the Namibian red-legged tick
Sweating sickness Cattle, especially calves Hyalomma truncatum, the small, smooth bont-legged tick
Brown ear tick toxicosis Cattle Rhipicephalus appendiculatus, the brown ear tick
Tick toxicosis Cattle and sheep, especially young animals Ornithodoros savignyi, the sand tampan
Tick paralysis Humans Hyalomma truncatum, the small, smooth bont-legged tick
Rhipicephalus simus, the glossy brown tick
Tick paralysis Calves, lambs Rhipicephalus simus, the glossy brown tick
Otitis (tampans) Various domestic animals Otobius megnini, the spinose ear tick

Source: Modified from: Howell, Walker and Nevill (1978). Ticks, mites and insects infesting domestic animals in South Africa. Science Bulletin No. 393. pp. 1-69.

Areas of impact

Ticks impact both directly (by virtue of heavy infestations) and indirectly (through the transmission of tick-borne diseases). Such impact is at the macro-economic level where exports and the commercial production of protein are of major concern, at the micro-economic level where the subsistence economy of the resource-poor farmer may be at risk, and in a social context where human diseases and zoonoses are concerned. Whilst a paucity of actual data exist, it was estimated some 25 years ago that losses attributed to tick-borne diseases in cattle were in the region of R70–200 million per annum, while an FAO panel placed total losses in South Africa at R550 million per annum as early as 1985. However, these are estimations, at best, and many resources would have to be harnessed in order to determine more accurate economic-impact figures for the effect that ticks have on the economy. Only one such study – on one of the most important tick-borne disease in South Africa, heartwater has ever been attempted (Draft Country Report, UF/USAID/SADC Heartwater Research Project, 2005). It estimated total annual losses at R189,6 million.

In South Africa, ticks and tick-borne diseases (T & TBD) impact directly on agricultural production, which represents only 8.5% of the economically-active population, and contributes 2.8% to the Gross Domestic Product (GDP) of the country (Abstract of Agricultural Statistics, 2012). Approximately 82% of the country is suitable for farming, and of this the greatest part (68.8% or 63.3 million hectares) is only suitable for extensive animal production, i.e. cattle, sheep, goats, wildlife or a combination of these.

Tick risk to the livestock industry

An indication of the main livestock entities at risk to T & TBD, are listed in Table 3.

Table 3. Production systems and livestock numbers (x 1 000) in South Africa.

Production System Emergent Commercial Total
Beef
Dairy
Goats
Sheep
5 710
4 485
3 162
8 190
1 080
2 106
21 924
13 900
1 080
6 591
25 086

Source: Abstract of Agricultural Statistics (2012)

It is estimated that South Africa has 35 000 commercial red-meat producers, representing over 60% of cattle and 86% of the sheep production. An estimated 50% of beef cattle and 10% of lambs are fattened in feedlot systems. However, these animals originate from primaryproduction systems that are extensive in nature and would be at risk of T & TBD. The degree to which each of these livestock entities is subject to T & TBD depends on the distributions of specific tick species and the epidemiology of the disease concerned. Most cattle are raised in the eastern and northern provinces of the country, which are analogous to the distributional pattern of the major tick-borne diseases – heartwater, babesiosis, anaplasmosis and theileriosis. Sheep and goats in the central and eastern provinces are at risk of heartwater and some tick toxicoses. Sheep production dominates in the dry western provinces, which, with the exception of the Karoo paralysis tick, do not harbour many problematic tick species. The ostrich industry, another focus of impact, is localised in the Karoo, and is affected by export restrictions due to Crimean Congo Hemorrhagic Fever virus.

The cost of tick control, disease prevention, and treatment

In general, South African commercial farmers practice intensive tick control (up to 37 applications per annum), with the majority using the more modern of the available acaricides (pyrethroids, combination products, and injectable endectocides). The emerging sector probably uses less intensive control, but very little data are available, with the main expense being borne by some provincial governments in terms of subsidised dipping of communally-grazed cattle, and in the maintenance of facilities to provide the resource-poor with access to tick control. In the province of Mpumalanga, these services are also provided as a means of ensuring footand- mouth-disease surveillance of communallygrazed cattle. No published data are available on the cost of this infrastructure, but the input by Veterinary Services in the supply of acaricides and personnel alone, would be considerable for the maintenance of these measures.

The official sales figure for acaricides supplied by some 17 pharmaceutical companies serving the livestock industry in South Africa, was in excess of R185 million in 2003. More recent sales figures (see Table 4) for products used in the animal-health market indicate an escalation in the cost of tick control (R327 million for ectoparasiticides alone). These costs account for a substantial input into individual livestock enterprises – a large portion of which would eventually be recovered from the consumer.

Table 4. Sales figures of products relating to parasite, tick and tick-borne disease control in the South African animal-health market.

Segment Turnover (ZAR millions) % of Total
Industry total 1948 100
Parasiticide subtotal
  • Ectoparasiticides
609
327
31,2
16,7
  • Endectocides
136 7,0
  • Anthelmintics
146 7,5
Antimicrobials 479 24,5
Biologicals 595 30,5
Other 265 13,8

In addition, frozen, live blood ‘vaccines’ for heartwater, babesiosis and anaplasmosis – for use in the prevention of these TBD – are produced on a continuous basis by the ARC-OVI, and marketed by Onderstepoort Biological Products (OBP). Average annual sales of blood vaccines, mainly to veterinarians and commercial producers, indicate purchases in the region of: 140 000 doses of babesiosis, 100 000 doses of anaplasmosis, and some 60 000 doses of heartwater vaccine – which underscores the importance of these TBD.

A synopsis of the major tick-borne diseases

Heartwater

Heartwater is a rickettsial disease of cattle, sheep and goats, caused by Ehrlichia ruminantium, which is transmitted by the tick A. hebraeum in South Africa. Since the eradication of East Coast Fever, heartwater is considered to be one of the most important TBDs in South Africa, and is the only disease for which the economic impact has been documented in some detail (Draft Country Report, UF/USAID/SADC Heartwater Research Project, 2005). Using a spreadsheet model of a representative herd under disease risk, quantifying values of production losses and control costs, and then scaling up to a production-system level, provides estimates of the economic impact of the disease. Estimates based on the distribution of the vector projected the numbers of animals at risk to be more than 11 million, as summarised in Table 5. Proportionally, 35%, 54% and 12% of the total cattle, goat and sheep populations are at risk. The model concluded that total, annual losses from heartwater alone, in 2005, were estimated to be US$31.6 million (R189.6 million) – of which 66% were production losses and 34% control costs.

Babesiosis

Babesiosis or redwater, is a protozoal disease of cattle caused by both B. bigemina and B. bovis – both organisms transmitted by the vector tick, Rhipicephalus (Boophilus) microplus – while Rhipicephalus (Boophilus) decoloratus transmits only B. bigemina. Babesiosis is proposed as the second most economically important TBD in South Africa – affecting only cattle. It has basically the same distribution as heartwater and should therefore affect the same proportion of cattle, i.e. 35% of the cattle population is at risk of babesiosis. No conclusive data exist on economic effect, except that US$725,000 (R5.1 million) is spent annually in South Africa on specific babesicides.

Equine babesiosis, which is caused by Theileria (Babesia) equi and transmitted by R. e. evertsi, affects the health of horses and is of immense importance to the horse-racing industry, in that the European and Eastern countries and the Americas enforce restrictions on the export of infected race horses.

Table 5. Estimated number of livestock at risk of heartwater in South Africa (2012).

Production system Emergent Commercial Total
Beef
Dairy
Goats
Sheep
1 718 132

2 332 696
379 448
2 584 562
606 255
1 236 555
2 782 620
4 302 695
606 255
3 569 251
3 162 068

Anaplasmosis

Anaplasmosis is a rickettsial disease affecting cattle, which is caused by the organism A. marginale. The organism is transmitted biologically by five species of ticks, and mechanically by bloodfeeding flies. As with babesiosis, an estimated 35% of the cattle population would be at risk due to the distribution of its tick vectors. However, the distribution of the disease is markedly wider than that of heartwater and babesiosis, because it can be mechanically transmitted by blood-sucking flies. Thus more than 50% of the cattle population is at risk.

Theileriosis

Corridor disease (CD), caused by buffaloassociated T. parva, is transmitted by infected R. appendiculatus and R. zambeziensis. It is a controlled disease in South Africa – meaning that its prevention and control is regulated by the central Department of Agriculture and Fisheries. Infected African buffaloes are natural carriers of this parasite, which is found in the bloodstream – although they show no clinical signs of disease. The infection is transmitted to cattle by infected nymphs or adult ticks, resulting in clinical disease and high mortality rates. Cattle that survive such disease outbreaks may become carriers of the infection and could subsequently infect ticks. Elsewhere in Africa, East Coast Fever (ECF), caused by cattle-adapted strains of T. parva, is associated with large-scale deaths, whereas ‘January Disease’ (Zimbabwean theileriosis) causes sporadic deaths in cattle in mid-summer. ECF was introduced into South Africa in 1902 with infected cattle imported from East Africa, and was finally eradicated at great expense in 1955. The ‘cattle-adapted’ causative organism was eradicated, while the main vector, R. appendiculatus, remained present.

In South Africa, CD is still endemic in some buffalo populations, but infected buffaloes are confined to wildlife reserves bordered by control zones – one in the eastern lowveld (bordering the Kruger National Park) and another in northern KwaZulu-Natal (bordering the Hluhluwe- Umfolozi corridor – from whence the disease acquired its name). CD is controlled by state veterinary authorities through strict regulations aimed at preventing contact between cattle and infected buffaloes. The growth of game farming has led to the breeding and relocation of buffaloes country-wide, however, so increasing the potential risk of buffalo and cattle contact, which, in the presence of the tick vector, could lead to outbreaks of CD. A practical concern is the possible creation of a carrier state in cattle that recover from an infection. Of even greater concern is that the parasite could adapt to cattle, with resulting cattle-to-cattle transmission – causing ECF to re-emerge, with a devastating impact on the susceptible cattle population in the country. Since 1998 all buffalo destined for translocation have had to undergo a battery of diagnostic tests for CD, foot-and-mouth disease, tuberculosis and brucellosis, before they were legally permitted to be relocated. Such mandatory diagnostic tests – combined with quarantine restrictions of areas outside the CD endemic areas on which buffalo test CD positive attest to the indirect impact of TBDs.

Crimean Congo Haemorrhagic Fever virus

The virus survives transstadially and inter-seasonally in several tick species. Twenty-seven tick species have been reported to be reservoirs or vectors of the virus, with the two-host ticks of Hyalomma spp. being the main vectors in South Africa. The first confirmed human case was reported in 1981 and since then there have been sporadic cases (almost 200 in total) – mainly in rural areas. Approximately 70% of human infections result in clinical illness, with mortalities of up to 35%. Besides the zoonotic aspect, the economic importance of this disease was highlighted when several human cases occurred in an ostrich abattoir in Oudtshoorn, South Africa, in 1996. At the time US$213,900 (R1 069 500) of meat had to be immediately destroyed. This resulted in an instantaneous and extended embargo being placed on the export of all ostrich products from South Africa. South Africa exports US$12.6 million worth of ostrich meat per annum – mainly to Europe – and this represents some 85% of the world market. Ostrichleather exports exceed US$85 million each year. The ostrich industry generates some US$100 million in revenue and now operates under strict EU restrictions, which stipulate that no tickinfested birds or their products may be exported.

African Swine Fever virus

African swine fever is a highly contagious and fatal disease of domestic pigs, which causes no clinical disease in wild pigs. In domestic pigs the morbidity is 100%, and infection with a virulent strain is almost always fatal. It is transmitted by the argasid tick Ornithodoros porcinus. Transmission is via the mouthparts while feeding, and the virus is also excreted in the coxal fluid. Infected male ticks are able to transfer the virus to uninfected female ticks during copulation.

The disease is limited to the western, northern and eastern Limpopo Province – which has been designated as a Swine Fever Control area. In this area, there is strict control of the movement of pigs within, into, and from the area. The OIE classifies this disease amongst its List A diseases, which are of major importance in the international trade of animals and animal products. There would be serious economic implications should an outbreak occur in the domestic pig population.

Karoo tick paralysis

The females of Ixodes rubicundus cause a toxicosis known as ‘Karoo tick paralysis’, ranked as the third most important problem of sheep and goat farming within the distribution region of the vector tick. It is estimated to cause about 30 000 deaths per annum in livestock – mainly sheep. Timely removal of the ticks usually results in complete recovery of the affected animal.

Sweating sickness

Some strains of Hyalomma truncatum transmit a toxin during feeding. The toxin is epitheliotrophic and causes a moist eczemalike skin condition – but can lead to the death of the animal. Timeous removal of the ticks usually results in complete recovery of the affected animal. This condition was first described in South Africa in 1920, and was regarded to be of great economic importance at that time – with morbidity ranging from 2-100% (with a mortality rate of about 30%) within the distributional range of the tick. Even today, under the most stringent tick-control programmes, cases still occur sporadically, because with their preference to feed on the tail switch of cattle, these ticks are easily overlooked and may survive some control measures.

Production loss

The effects of ticks on livestock are often linked with those of tick-borne diseases. However, tick feeding – apart from causing direct damage resulting in abscesses, secondary infections, loss of teats, damage to genitalia and hides – especially in heavy infestations, also affects production through loss of condition, decreased weight gain, and a reduction in milk yield. A loss in live-weight gain of 10 g per female completing engorgement on cattle has been attributed to A. hebraeum, while R. appendiculatus accounted for a 4 g loss per engorged female in similar experiments. The growth-rate of cattle can decrease by 20 kg over a three-month period when heavily infested with 10 engorging A. hebraeum females, per animal, per day. A. hebraeum infestation has been shown to cause a reduction in milk yield, to the extent that a loss of 6 g live-weight gain was recorded in calves, per engorged female on the dams. The calves of Sanga-type cows – predominantly infested with R. (B.) decoloratus on a mixedbushveld farm – showed a loss of 8 g in weaning weight per engorged female tick. Heavy infestations of R. (B.) microplus damage hides by the formation of scar tissue at the feeding sites, while each female tick that completes engorgement results in a 0.6 g loss of potential growth in cattle.

Chemical control of ticks, and acaricide resistance in South Africa

Science never solves a problem without creating ten more

– George Bernard Shaw

The success of the livestock industry in South Africa is largely due to the adequate control of ticks by dipping since the first outbreak of East Coast Fever in 1902. Throughout most of the Twentieth Century, tick infestations on cattle were controlled mainly by chemicals administered by plunge-dipping, spraying in spray races, or by hand-spraying – and more recently in the form of pour-ons, spotons, and parenteral injections. Arsenic was first used for tick control in 1893 in South Africa, and this organic compound was followed by a range of organic acaricides which included the organochlorines, organophosphates, carbamates, formamidines and synthetic pyrethroids – complemented by combination products, the macrocyclic lactones, and the last to become available, a growth regulator. The development of environmentally safer acaricides has been due to marketing pressures and other factors, such as a growing environmental awareness of the harmful effects caused by a build-up of residues.

Historical perspective

Control measures against ticks and tick-borne diseases were applied on a large scale in southern Africa following the introduction and spread of East Coast Fever from East Africa. As a result of a 95%-mortality rate during the period 1901- 1902 in Southern Africa, considerable effort was devoted to the development of tick-control measures. Early attempts at vaccination by Robert Koch, and later by Sir Arnold Theiler, were largely unsuccessful. However, knowledge about the tick responsible for the transmission of the disease (Rhipicephalus appendiculatus) led to more successful control measures. These were based on tick control – quarantine procedures, pasture spelling, slaughter, and dipping in arsenic solutions (dipping at 5-5-4 day intervals, attuned to the feeding periods of the larval, nymphal and adult stages). Dipping proved to be the most practical and effective measure, and then became a compulsory mainstay of tick control until East Coast Fever was brought under control and eradicated in 1956. The disease was eradicated; however the vector is still present.

After the eradication of East Coast Fever, two options were essentially open to Southern African countries. They could either control the remaining major tick-borne diseases (babesiosis, anaplasmosis and heartwater) by vaccination (the frozen vaccines were available at that time) – progressing towards reduced tick control and endemic stability (which does not necessarily control the incidence of direct damage caused mainly by the multi-host ticks) – or they could continue to control the diseases by intensive dipping. It had been established at that time that the most efficient and economical manner to achieve a degree of national tick control was to target intervention at the parasitic stage, and short-interval dipping of livestock became the standard method of tick control. Compulsory dipping, however, was eventually abolished and the choice was left to individual farmers. This has increased the resistance problem – mainly by the high frequency usage of chemicals. The communal sector has traditionally been constrained by contract acquisition of acaricides that are subsidised by government, and a poor resource base – thus not being able to rotate or change acaricide groups, as and when necessary.

Current status

All acaricides in South Africa are required to be registered according to Act 36 of 1947. Currently, at the last count, the acaricide market provided some 92 products (trade names) for tick control, inclusive of 15 combination compounds. These products are based on only 18 active chemicals – representing five chemical groups or modes of action. These are the organophosphates, the synthetic pyrethroids, the formamidines, the macrocyclic lactones, and a chitin-synthesis inhibitor or growth regulator (see Table 6). The last two groups are systemic and are more effective against one-host ticks. Although some trade names or actives may be removed, or new ones added over time, the acaricide arsenal is a limited resource and judicious use is imperative.

Acaricide resistance

Resistance may be defined as the ability of the target pest (in this case the tick) to overcome the lethal effects of a chemical (i.e. acaricide) – and to survive and reproduce. Tick resistance to acaricides which are used for tick control is an international phenomenon, and has been an ever-increasing problem in South Africa. The first published report on the development of tick resistance was to arsenic in 1941 – in the one-host tick, R. (B.) decoloratus (then named Boophilus decoloratus). This was confirmed after controlled field trials and laboratory tests. Later, resistance to arsenic was also detected in R. evertsi evertsi, R. appendiculatus, A. hebraeum, and R. (B.) microplus (then named Boophilus microplus). This was followed by Benzene hexachloride (BHC) resistance in 1952, and DDT/pyrethrin resistance in 1956 (in R. (B.) decoloratus).

Subsequent widespread field use of the organophosphate acaricides, resulted in R. (B.) decoloratus becoming resistant to this group of acaricides – later followed by R. appendiculatus and R. evertsi evertsi. Similarly, resistance by the one-host species [Rhipicephalus (Boophilus)] ticks inevitably followed the prolonged use of the synthetic pyrethroids. More recently, formamidine (amitraz) resistance in A. hebraeum, R. (B.) decoloratus, and R. (B.) microplus, has been confirmed in South Africa (see Table 7). Acaricide resistance poses an ongoing economic threat to livestock production, novel actives are fewer and more expensive, and the cost of developing a novel acaricide compound is astronomical (one estimate, some 15 years ago, placed it at US$230 million per compound).

Table 6. Acaricidal actives currently registered for use in SA, according to chemical groups. (Sourced from mims - Index of Veterinary Specialities, 2010)

Chemical group Trade
names
Active chemical Formulation*
Organophosphates O
Synthetic pyrethroids P
Formamidines F
Macrocyclic lactones
Chitin-synthesis inhibitors
(Growth regulators)
Combination F-P
Combination O-O
Combination O-P
Combination P-P
Combination P-P-O
Combination F-P-O**
10
31
18
18
1
15
Chlorfenvinphos
Diazinon
Triazophos
Alphamethrin
Cyhalothrin
Cyfluthrin
Cypermethrin
Deltamethrin
Flumethrin
Amitraz
Doramectin
Ivermectin
Moxidectin
Eprinomectin
Abamectin
Fluazuron
Amitraz / Cypermethrin
Cymiazol / Cypermethrin
Amitraz / Deltamethrin
Chlorfenvinphos / Dichlorphos
D S
Chlorfenvinphos / Alphamethrin
Chlorfenvinphos / Cypermethrin
Chlorfenvinphos / Esfenvalerate
Flumethrin / Cyfluthrin
Alphamethrin / Cypermethrin
Tetrachlorvinphos
Cymiazole / Cypermethrin /
Chlorfenvinphos
D / D S / H
DD
D
D S
Po
Po / D S / S / H
Po / D S / H
Po / D S / H
D / D S / S
I
I / Po sys
II
I / Po sys
Po sys
Po
D S
Po
H S
D
Po
Po
DS

* D = Dip; D S = Dip or Spray race; H = Hand application or hand spray; I = Injectable (systemic action);

Po = Pour-on; Po sys = Pour-on with systemic action; S = Spray race

** Eraditick® Ultra: G No.: 3976 Act 36 of 1947: Patented

It is clear that it would be advantageous to prolong the use of available acaricides – by their effective use.

Genetic basis of resistance

As shown by Brown in 1976, resistance to chemical compounds by ticks and other arthropods is genetically determined, and operates primarily through the selective effect of chemicals on resistant mutants, which occur in field populations in low frequencies. It has been suggested that resistant mutants in a wild population occur in the order of 1 X 10-8, and in the order of 1 X 10-5 in a population under treatment. Thus, 1 in 1 000 billion to 1 in 10 billion individuals in the respective populations may have the ability to tolerate a lethal chemical. More simply put, if an acaricide is applied to a tick, it dies or it does not. If it dies it is susceptible, if not it has some biochemical adaptation (prior mutation) which circumvents the mode of action of the acaricide, and its survival contributes this ability to the population gene pool, where subsequent selection pressure (repeated dipping) favours and selects those with this resistance. The possibility that acaricides may induce resistance biochemically is discounted, as this would depend on the ability of each individual to adapt by suitable changes in its biochemical pathways. The resulting increased tolerance would not be heritable and maintained after inducer (the application of a particular acaricide) withdrawal. Early workers such as Stone and Nolan have shown that acaricide resistance persists in the absence of chemical pressure, and that considerably accelerated selection would take place on its reintroduction. Resistant alleles may therefore pre-exist in a population in a heterozygous state, even before an acaricide has been developed – the rest is selection by exposure to subsequent use.

Development of resistance within populations

The development of resistance against acaricides which are used for tick control occurs in three phases. Firstly, the initial establishment of resistant alleles in a population must occur to establish the potential. This happens by a process of random mutation which is proportional to population size. Once heterozygous, resistant individuals are established, the second phase of propagation of resistant alleles – by the preferential survival of heterozygotes – occurs. This phase is accompanied by the dispersal of resistant alleles to susceptible sub-populations, although resistance is usually not noticeable during this phase. The final phase, which is the establishment and selection by acaricides of homozygous, resistant individuals in the population is usually depending on the degree of dominance of the resistant alleles – very rapid. Stringent dipping programmes – leaving a low residual population number – reduce intraspecific competition, which further enhances density-dependent survival of parasitic offspring on the host. Dependent on the prior existence of resistant alleles, selection pressure with different acaricides, and the introduction of resistant sub-populations from elsewhere – multiple acaricide-resistant tick populations may well develop.

Table 7. Acaricide use and resistance in South Africa.

Compound First Used Resistance 1st reported
Arsenic 1893 1941 (du Toit)
DDT 1948 1956 (Whitehead)
BHC & Toxaphene 1950 1952 (Whitnall et al.)
Carbamates 1960 1966 (Shaw et al.)
Organophosphates 1960 1966 (Shaw et al.)
Formamidines 1974 1995 (Taylor & Oberem)
Synthetic Pyrethroids 1981 1987 (Coetzee et al.)
Macrocyclic Lactones 1990
Growth Regulators 2000

Acaricide resistance is more widespread and diverse in one-host ticks. The main reasons for the more rapid selection for resistance in these ticks is their short generation time, combined with the high probability of all three feeding stages (feeding on the same host) being exposed to selection pressure by an acaricide. Inversely, resistance to acaricides develops more slowly in the two- and three-host ticks: there are longer generation times, with less exposure of the immature tick stages (many feeding on alternate hosts) to acaricides. The use of high concentrations of active ingredient, as in pour-on formulations, has led to the acceleration of resistance – particularly with pyrethroids. This is a major problem with ‘home made’ formulations mixed by farmers.

Rate of development of acaricide resistance

The rate at which resistance against acaricides develops depends on a number of different factors. These are: the degree of dominance of the resistant alleles, the strength of the acaricide used, and the frequency of dipping. Stone – working with R. (B.) microplus (recently reassigned and described as Rhipicephalus australis) in Australia – showed resistance to DDT to be incompletely recessive, while BHC-dieldrin resistance was found to be completely dominant. Organophosphate resistance, on the whole, is dependent on incompletely dominant alleles. The degrees of dominance are reflected in the manifestation of field resistance to these three acaricide groups in Australia and South Africa (South Africa in parentheses): DDT after 5 (8) years; BHC-dieldrin after 5 (18) months; and organophosphates after 5-15 (6-20) years. The first field resistance to a synthetic pyrethroid in South Africa was reported 8 years after registration for general use, and in that particular case it was interpreted as occurring after 18 months of field use. Resistance to amitraz took a lot longer to appear in the field.

The strength of acaricide used is limited by toxic effects on host animals and is dictated in practice more by economic considerations – in that the concentration registered for use is that which gives satisfactory control (95+%). Observations in the field indicate that the rate of AR development can be accelerated by products containing high concentrations of active ingredient, such as pour-ons, and, in particular, home-made pour-on formulations.

Resistance mechanisms

According to Stone, resistance by arthropods to chemicals may be due to one or more different mechanisms:

  1. reduced penetration
  2. excretion or increased storage of the toxicant
  3. reducing the toxicity of the applied chemical
  4. increased detoxification by metabolic breakdown of the chemical
  5. reduced sensitivity of the target system to the chemical.

Mechanisms (i) and (ii) have not been identified in ticks, although (iii) is regarded to be of potential importance in organophosphate resistance. Mechanisms (iv) and (v) have been shown to be responsible for tick resistance to arsenicals and pyrethroids, and to organophosphates, respectively. Non-essential sulphahydrals in resistant ticks are thought to reduce the toxicity of arsenic compounds. Breakdown of the isomers of the pyrethroid, flumethrin, has been reported for R. (B.) microplus (now Rhipicephalus australis).

Mechanism (v) – reduced sensitivity of the target system – is responsible for the major portion of resistance in tick strains, to organophosphates. These acaricides act by inhibition of acetylcholinesterase which is essential for correct nerve function. Resistance is effected by the modification of actylcholinesterases, which render the ticks insensitive to organophosphate action. In many pyrethroid-resistant strains, a single target-site mutation on the Na(+) channel confers very high resistance to both DDT and all synthetic pyrethroid acaricides.

A further factor influencing resistance to acaricides is that of a complex cross-resistance pattern. This is probably due to individual acaricides within the group having the same mode of action and therefore being sensitive to the same resistance mechanism.

Acaricide resistance testing methods

Various laboratory methods have been developed to test for acaricide resistance. The laboratory methods usually involve either larval or adult ticks and include the Shaw Larval Immersion Test (SLIT) or the Larval Packet Test (LPT) – both of which are based on the testing of larvae. The Adult Immersion Test (AIT), however, uses field-collected adult ticks. The SLIT and the Food and Agriculture Organization (FAO)-adapted LPT, are the most important larval acaricide-resistance testing methods currently being used worldwide. The SLIT is a timed immersion of unfed larvae in an aqueous test wash, followed by a holding period in a clean environment, and, finally, larval mortality counts. The principle of the FAO-adapted LPT involves exposing unfed larvae to pre-prepared filter papers impregnated with the active chemical in an oil solvent for the whole period of the test, usually 24 hours, and followed by mortality counts. This method was initially developed in Australia and later adapted for use on African ticks. The main disadvantage of these specific tests (SLIT and LPT) is that they require at least 6 weeks for the LPT, and more than 60 days for the SLIT – to obtain results. Both tests also require trained technical personnel, as well as a range of expensive equipment, and the upkeep of susceptible – and preferably also resistant – reference strains.

The AIT uses engorged adult female ticks, and tick resistance may be detected within 42 days using a reproductive estimate based on larval hatch from treated females. The test can be performed by less-experienced personnel, using less expensive equipment. An in vivo stall test is, however, still the most conclusive indicator of acaricide efficacy – its disadvantage being its expense. Ongoing research employing molecular techniques has developed DNA-based molecular tests and ELISA-based assays for acaricide resistance. Researchers aim to determine the genotype of individual ticks with these tests in order to obtain a comprehensive profile of their susceptibility (and resistance) to various pesticides.

The detection of resistance at an early stage is important in order to introduce timeous resistance-management strategies. These could include: ensuring the correct concentration and application, as directed, strategic change (alternating) from one acaricide group to another (being mindful of cross resistance within groups), adjunctive treatment with systemic acaricides, vaccination, and avoidance of introducing resistant ticks to the farm or pasture by the movement of tick-infested stock. Alternating between acaricide groups remains a moot point. Some argue for short-term alternation (every year or two) with the aim of timeously preventing the development of resistance within the tick population, while others argue that a specific acaricide should be used until resistance by the tick population becomes problematic, before changing to another chemical group. Presently, only five chemical groups are available – one of which, the organophosphates, has been in use for over 50 years and there is uncertainty about its continued efficacy and toxicity in the environment.

Future prospects

New technologies offer the potential of vaccines both against the ticks themselves and against the diseases they transmit. Australian researchers have developed ‘Bm86’ – a vaccine that stimulates an immune response against the tissues of the tick’s gut – thereby preventing effective feeding and so killing the tick. So far they have done this for their resident blue tick, Rhipicephalus australis (previously R. (B.) microplus). This vaccine is, however, not effective against its South African counterpart, R. (B.) microplus. Other suitable antigens for use in tick vaccines may be uncovered with future research.

Novel chemical groups developed by pharmaceutical companies in future, will likely be expensive due to the cost of research and development. The livestock producer will therefore be forced to use integrated tick control to limit tick damage below economically acceptable thresholds. This control method involves using tick-resistant cattle, vaccination, stocking and density manipulation – along with strategic and/or opportunistic chemical treatment to reduce tick effects. Its application is specific to a host of factors, including conditions of management, breed, prevalent tick species, diseases, and intensity of challenge. However, its utilisation does not preclude intensive chemical control.

Host factors

“It is not the strongest of the species that survives, nor the most intelligent that survives. It is the one that is the most adaptable to change.”

– Charles Darwin

“A host is like a general: calamities often reveal his genius”

– Horace

Animals have the ability to develop an immune response against ticks. When ticks attach to an animal and start to feed, a hypersensitivity reaction involving the release of histamine in the skin, triggers a grooming response, which is followed by cellular and humoral immune reactions as tick feeding progresses. These immune responses interfere with tick feeding, and the parasite mounts a counterattack by secreting immune-modulating substances in its saliva during feeding. Depending on the innate and adaptive ability of the host and the tick, these processes determine the eventual success of the feeding ticks. Although all cattle breeds display this ability to some extent, certain breeds have a better developed innate ‘resistance’ to ticks, and are better adapted to acquire resistance to repeated tick challenge. This ability to restrict tick-feeding success is more pronounced in the so-called Sanga or zebu type (indigenous) cattle and Bos indicus breeds – apparently as a result of their longer evolutionary association with ticks, as opposed to Bos taurus breeds. Thus the principles associated with so-called ‘tick resistance’ can be summarised as follows:

  1. The degree of innate host resistance of a bovine is proportional to its zebu/indicus gene content.
  2. Tick exposure (or challenge) is required for increasing acquired resistance.
  3. Resistance is an immunogenic response – phenotypic characters such as hair length and colour or skin thickness, could not be correlated with resistance status in detailed field trials.
  4. Resistance is stress dependent – e.g. nutritional stress will detrimentally affect the immune response, as do hormonal stressors such as pregnancy.
  5. Resistance is heritable – depending of course on breed; some authors have indicated a heritability index of 0.4.

Extensive field trials over four years – using Nguni (representing zebu), Bonsmara (representing a composite cross-breed) and Hereford (representing a Bos taurus breed) cattle – took place in a high tick challenge area without acaricide intervention, and involving counts of engorged ticks as an indicator for tick feeding success. Herefords displayed the highest tick counts, Bonsmaras intermediate tick counts, while Nguni cattle had the lowest counts of the one-host blue tick (R. (B.) decoloratus) and the three-host bont tick, A. hebraeum. Overall, tick counts declined each year on all breeds – which incidentally maintained their respective resistance status. The number of ruptured abscesses caused by the long-mouthed A. hebraeum and Hyalomma ticks were predominant on the Herefords, intermediate on the Bonsmaras, and negligible (<2) on the Nguni cattle. Although the Hereford cattle acquired resistance to ticks under these circumstances, this was insufficient to prevent production loss. Thus the breed is not adapted to these high tick challenge situations, and was in need of acaricide intervention. Subsequent research established that counts of all ticks under the tail on the perineum of an animal correlate exceedingly well with counts of engorged females as a means of determining the relative resistance status of individual animals. Selection of cattle for the ability to mount resistance against ticks is therefore feasible.

Other strategies would be ranching appropriate cross-breeds. It is interesting to note that some wild herbivores – notably buffalo and eland which can have heavy tick burdens – appear to have developed a tolerance over time, since they apparently do not mount an immune response which discourages feeding (Horak et al., 2007). Other herbivores, such as impala rams, show the effect of stress on host immunity by having exceptionally high tick burdens during the rutting season, when grazing (nutrition) and grooming become secondary activities.

Only a few tick species are host specific: this ability of ticks to be able to feed on a variety of wild and domestic hosts, contributes to their survival in the ecosystem.

Bionomic factors

“The first law of ecology is that everything is related to everything else.”

– Barry Commoner

Most African ticks are not considered to be host-limited (i.e. their ranges are not limited by host availability). In the main, those of major economic importance in South Africa are affected by bionomic factors – mainly temperature and rainfall, vegetation type, and elevation. These affect the survival and propagation of particular tick species. Regions or zones are thus moulded by the interplay of long-term biotic and abiotic factors that determine their vegetative character and potential, and these – modified by land-use – determine the habitat suitability for particular tick species. For example, in the broader context of South Africa, most of the major tick vectors occur in the more humid eastern and coastal regions (e.g. A. hebraeum, Rhipicephalus (Boophilus) species, and R. appendiculatus), with the central regions being a transitional or barrier zone to their distribution patterns. The more arid western regions also contain those species with lower humidity requirements (e.g. Hyalomma species and R. evertsi evertsi). In a more limited context, R. appendiculatus requires grassland interspersed with trees or bush as a suitable habitat. The practice of brush removal within its distribution – in order to establish grass pastures – has, however, curtailed its survival on such properties.

As an example of the temperature effect, the developmental life cycle of R. (B.) decoloratus is highly dependent on temperature and humidity; the eggs require an effective temperature of 1 000 to 1 800 day-degrees to hatch. Those laid in the summer months (high ambient temperature) during the rainy season develop rapidly and hatch within c. 1 month – while those laid just before winter require a lengthy period to reach their effective temperature requirement. They remain dormant and protected against low winter humidity levels, and hatch only with the advent of higher temperatures in the following spring: humidity determines the quality of hatch and longevity of larvae on the vegetation (see Figure 9).

Climatic effects – in conjunction with other factors such as photoperiod, vegetation type and structure, and host factors – therefore influence the occurrence, abundance and seasonality of tick species according to their adaptive requirements, both at a macroclimatic (seasonality) and microclimatic (circadian rhythms) level. Each tick species therefore occurs within specific ranges of environmental variables which enable it to survive and reproduce.

Figure 9 The pre-hatch period and larval survival of Rhipicephalus (Boophilus) decoloratus – illustrating the effect of temperature.

 
potential spatial distribution of species may be determined by computer models that can relate presence or abundance data of a specific species to environmental factors which determine habitat suitability for, or preference of, the species. Habitat suitability models – which are generated by combining species occurrence data with environmental GIS data – aim to predict those areas within a region that satisfy the requirements of the ecological niche of the species concerned, and thus represent its potential distribution. As a result, distribution modelling has become a valuable tool towards exploring and understanding the distribution of species. The availability of a wide range of climatic data, including precipitation, temperature, relative humidity and potential evaporation (Schultz 2007), are all relevant to tick survival – combining with physical environmental variables such as altitude and terrain morphology and vegetation types (see Figure 10).

Figure 10 The major biomes of South Africa: according to Mucina & Rutherford (eds), 2006, The vegetation of South Africa, Lesotho and Swaziland, Strelitzia 19. South African National Biodiversity Institute, Pretoria.

 

Biological control of ticks

“All have their worth and each contributes to the worth of the others.”

– J.R.R. Tolkien, The Silmarillion

Besides host factors, which have already been discussed at length, predators, parasites, pathogens and the disruption of tick viability through biological interventions (e.g. vegetation manipulation and microhabitat disturbance), are all factors that have been researched in an attempt to exploit their influence on tick populations. Predation of ticks by various animals, birds, reptiles and insects is known to occur as a constant and natural process. Probably the best known and only predation of any significance for tick control is that of the oxpecker birds in Africa: Buphagus eythrorhynchus, the red-billed oxpecker; and Buphagus africanus africanus, the yellow-billed oxpecker. With their habit of ‘grooming’ the coats of their hosts, with scissoring movement, these birds indiscriminately remove larvae and smaller nymphal stages. However, some reluctance has been shown by the red-billed oxpecker in terms of feeding on larger engorging ticks, although the scarcer yellow-bill has the ability to utilise these. Although their actual effect on tick numbers is almost impossible to evaluate, these birds no doubt play a role in tick control on free-living animals, and may also have a role on livestock in integrated control programmes. It must also be borne in mind, however, that these birds are free-living and may move to other areas should their food source diminish through intensive acaricide use on their hosts. Farmers, who want to encourage the birds as part of a sustainable tick control effect on livestock, will need to practice an extensive regional cooperation using birdfriendly acaricides. Hymenopteran parasites and pathogenic fungi have also been found to affect ticks but have as yet not been successfully employed in tick control. Their numbers appear to be too low to have significant impacts on tick numbers. The sterile-male control method which is used for insect control – is deemed to be impractical due to the logistics involved: a ratio of some 10:1 would be required to have any effect. The introduction of tick-resistant plants which form a barrier to tick-questing behaviour by possessing hooked trichomes (e.g. Desmodium spp.) and chemical deterrents (e.g. Melinis minutiflora, Pennisetum cynodon and Stylothanthes spp.) have received attention, but their pragmatic utilisation as tick control agents has not materialised. Habitat modification in the form of bush clearing may hold some promise in localised settings where the preferred habitat of a tick species is disrupted by the planting of artificial grass pastures (e.g. A. hebraeum and R. appendiculatus that are ecologically dependent on tall grass and tree shade) – but this practice may increase the prevalence of other species (e.g. R. (B.) decoloratus) that actually prefer such habitats. Pasture spelling or resting until questing ticks have died off presents the problem of pasture availability, in that most larvae (and nymphs for that matter) may take a long time to die [e.g. R. (B.) decoloratus larvae may be viable for 5 to 8 months on the vegetation depending on season]. Furthermore, small numbers of all stages of most tick species are bound to encounter an alternative, non-livestock host that would ensure their survival.

Figure 11 Relative numbers (Log10) of R. (B.) decoloratus and R. appendiculatus larvae collected by vegetation drags in adjacent burned and unburned sections, after a controlled veld burn in August.

 

Abiotic intervention, such as veld burning – as traditionally practiced in late winter – may remove questing ticks on the vegetation, but usually does not coincide with the seasonalactivity periods of most ticks. An additional disadvantage of veld burning is that the protective layer of vegetation is removed, the effective temperature for the developing stages is increased, and their development is more rapid – resulting in an overcompensation of tick numbers. As illustrated in Figure 11, an extensive veld burn in August succeeded in only a temporary, negligible reduction in the numbers of R. (B.) decoloratus larvae collected directly after the burn – with a subsequent overcompensation of larvae taking place during the months of February to March. Furthermore, R. appendiculatus larvae are most active in June, and the same intervention had very little effect on the numbers collected relative to the unburned section. However, some producers have reported a significant reduction in brown ear tick (R. appendiculatu) numbers by controlled burning of selected sections on their properties during June and July.

In general, therefore, factors that constitute the concept of biological control remain mostly as adjuncts to chemical control – localised in effect and useful (extremely beneficial and practical in the case of host immunity) as measures to be incorporated in integrated tick control as a whole.

Accounts of tick species

“Behold the tortoise: he makes progress only when he sticks his neck out.”

– James Bryant Conant

The following section is intended as an overview of the most important ixodid tick species affecting livestock in South Africa. Although the main morphological features are described, and some species are illustrated, this handbook is not intended as an identification manual. Rather, it furnishes details of each species with regards to biology, host and disease relationships – with emphasis on their distribution and habitat suitabilities, and particularly those that portray potential range expansion.

Amblyomma hebraeum – the South African bont tick

General

Known as the ‘bont’ tick because of the characteristic colour pattern on the scutum and its banded legs – A. hebraeum is common on livestock within its distributional range, and is the transmitter of heartwater to ruminants and a cause of direct damage to its hosts as a result of its long mouthparts.

Salient features

Large conspicuous ticks (Figures 12 and 13).

  • Hypostome and palps long (as with all Amblyomma species – Table 1)
  • Eyes large and flat
  • Colour pattern characteristic: dark brown ground colour, with pale yellow ornamentation tinged coppery-green at the edges
  • Festoons present: pale yellow in the male
  • Anal plates absent in the male

Hosts

Adults infest sheep and goats, but prefer larger domestic animals (cattle) and wild ruminants such as giraffes, buffalo, eland and rhinoceros – to which they attach in clusters in the hairless areas of the groin and axillae and on the dewlap, belly, perineum and peri-anal region. The immature stages feed on the same hosts as the adults, as well as on smaller antelope species, scrub hares, ground-frequenting birds (especially guineafowls), and tortoises. However, they are extremely rare on rodent hosts. On mammals, nymphs attach on the feet, legs, groin and neck, and larvae on the feet, legs and muzzle, and on the head and neck of ground-frequenting birds.

Life cycle and seasonal occurrence

This is a three-host tick; adults and nymphs will actively seek a host and climb onto them from the ground when their presence is detected. Replete females lay c. 18 000 eggs. The larval hatch is dependent on environmental conditions, and may take up to 5 months; larval feeding takes 7–14 days. Nymphs may remain inactive for some months after moulting and feed for 7–14 days; the males feed for 5–6 days before sexual maturity, and then secrete a pheromone that attracts other males, females and nymphs which attach in their vicinity. Mating takes place and females feed for 7–9 days. The life cycle is usually completed in 1 year, but prevailing conditions may extend it for some time. Adults are generally more numerous in the warm, humid summer months; larvae during the colder, drier late autumn and early winter months; and nymphs during winter and spring. All stages may be present on hosts throughout the year in most regions. There are minimal definite seasonal patterns of abundance of the different stages in the warm, humid, lowveld regions of South Africa.

 

 

Disease

Amblyomma hebraeum is most important as the vector of the causative organism of heartwater– E. ruminantium – for cattle, sheep and goats in South Africa. Transmission is transstadially or stage to stage. Infection is picked up by the larvae or nymphs when feeding on an infected animal, and this is transmitted to a susceptible host by the next stage. Helmeted guineafowls and scrub hares – which are the preferred hosts of the immature stages – may act as sub-clinical reservoirs of infection. A. hebraeum also transmits the protozoan, T. mutans, which is the cause of benign theileriosis in cattle, and Rickettsia conori and Rickettsia africae, the cause of tick-bite fever in man. Heavy infestations of this tick species may cause a reduction in growth rate and its long mouthparts cause wounds that may develop secondary bacterial infection or lead to myiasis by maggots of the cattle blowfly, Chrysomya bezziana.

Habitat and distribution

Amblyomma hebraeum is associated with warm, humid, wooded habitats, and does not occur in open grassland or treeless areas. The geographic distribution based on plotted locality records in South Africa, and its modelled habitat suitability, are illustrated in Figure 14. The mesic eastern region of South Africa, in close association with the Savanna and Albany Thicket biomes of Mucina & Rutherford (Figure 10), display a high habitat suitability index for A. hebraeum. High habitat suitability, in conjunction with confirmed presence data, are indicated in the south-central coastal region of the Eastern Cape Province - especially in the Albany Thicket biome. Habitat suitability extends in close association with the Savanna biome into KwaZulu-Natal, with highest suitability evident in its north-eastern region. The Savanna biome of the north-eastern region of Mpumalanga and of most of Limpopo also display high suitability – extending westward to the north-eastern region of North West Province. A median suitability index predicted for the southern coastal region of the Western Cape Province, infers suitable niches for the occurrence of A. hebraeum as evidenced by a small number of positive locality records in this region. The potential spread of this species into the central-southern region of the North West Province, and extending westwards into its more arid, shrub areas, as well as into similar xeric savanna habitats in the north-eastern Northern Cape Province, is also indicated. Such range extensions may be facilitated by changing land-use patterns: many cattle farms in these areas have reverted to wildlife farming, which changes the vegetation in favour of this species. A. hebraeum is absent in the Free State Province, which is a predominantly Grassland biome with an unsuitable habitat index – with low suitability being evident only in the north-eastern and south-eastern regions of this province.

Figure 12 Amblyomma hebraeum adults: illustration of the male (left) and female (reproduced by kind permission of the Onderstepoort Journal of Veterinary Research).

Figure 13 A fully engorged (fed) Amblyomma hebraeum female.

Figure 14 The geographic distribution of Amblyomma hebraeum in South Africa and its modelled habitat suitability. Dots represent 1 147 confirmed localities.

 

Amblyomma marmoreum – the South African tortoise tick

General

Amblyomma marmoreum (Figure 15) became more important when it was shown that it could acquire and transmit E. ruminantium – the causative organism of heartwater in ruminants. It was also demonstrated that the leopard tortoise, Geochelone pardalis, which is a preferred host of all stages of development of the tick, could be infected with E. ruminantium, and that A. marmoreum could acquire infection from an infected tortoise. In addition, it was found that helmeted guineafowls and scrub hares – which are the preferred hosts of its immature stages – may act as sub-clinical reservoirs of infection. Despite this, A. marmoreum is not considered to be of economic importance, because the adults, and probably the immature stages, do not feed on livestock and its contribution to the status of heartwater as a disease is considered to have no practical impact.

Salient features

  • Hypostome and palps long (as with all Amblyomma species – Table 1)
  • Eyes relatively small and flat
  • Colour pattern characteristic: ground colour brown, with a pattern of characteristic pale yellow, buff markings
  • Scutum with several large deep punctations (the scutum may be scuffed from rubbing against the tortoise’s shell during feeding)
  • Festoons present: partly coloured in the male

Hosts

The leopard tortoise is almost exclusively the preferred host of the adults, which attach on the soft body parts around the head, the front and back legs, and the tail. The immature stages feed on tortoises, ground-frequenting birds (especially guineafowls), scrub hares and on cattle – the cattle being preferred more by larvae than by nymphs.

Life cycle and seasonal occurrence

This is a three-host tick. Fully-fed females are extremely large (c. 3 cm long) and when replete they may lay up to 25 000 eggs. Larvae and nymphs may feed for up to 30 and 50 days respectively, depending on the host species. The period from larval attachment to adult engorgement in laboratory experiments, varied from 69 to 172 days. If warm-blooded hosts are utilised by the immature stages, the life cycle may take 1 year, and should the immatures feed on tortoises, it may take up to 2 years to complete. Adults are more numerous in summer, larvae in late summer, and nymphs in late summer and again in early spring.

Figure 15 Amblyomma marmoreum adults: illustration of the male (left) and female (reproduced here by kind permission of the Onderstepoort Journal of Veterinary Research).

 

Disease

Amblyomma marmoreum may act as a carrier of E. ruminantium, but it is not known as a vector of any other organisms which are pathogenic to livestock.

Habitat and distribution

The south-eastern Eastern Cape Province, associated with the Albany Thicket biome, extending westwards along the southern coastal regions into the Fynbos biome of the Western Cape Province, with a central inland incursion into the Succulent Karoo – displays high habitat suitability for A. marmoreum (see Figure 16). High suitability indices are evident northwards of the Albany Thicket biome into the south-eastern and central Free State (Grassland biome), as well as portions of the Nama Karoo and Savanna biomes of the north-eastern Northern Cape, into the southwestern regions of the North West Province. The Indian Ocean Coastal Belt and Savanna biomes of KwaZulu-Natal and Mpumalanga, and the north-eastern Savanna regions of the Limpopo and North West Provinces, also display high suitability indices for this species. High suitability generally coincides with presence data, but with a wider predicted distribution around these foci (Figure 16). The small number of locality records for this species and its presence across a large number of vegetation biomes, suggest that its distribution in South Africa could be more widespread than indicated, as has previously been suggested by Horak and co-workers.

Figure 16 The geographic distribution of Amblyomma marmoreum in South Africa, and its modelled habitat suitability. Dots represent 154 confirmed localities.

 

Hyalomma rufipes - the large or coarse bont-legged tick

General

A large robust tick with long mouthparts, beady eyes, and long banded legs. Actively hunts for hosts along the ground. Of the three Hyalomma species in South Africa, this species is the main vector for Crimean Congo Haemorrhagic Fever virus (CCHF).

Salient features

  • Hypostome and palps (mouthparts) are long
  • Eyes present and hemispherical
  • Ornate: legs are banded at articulations (see Figure 17)
  • Scutum shiny and dark with dense, uniformlyspaced punctations
  • Marginal groove well defined and long in the male
  • Dense setae on the integument surrounding the spiracle
  • Festoons present
  • Three sets of anal plates present in the males

Hosts

The main hosts of the adults are cattle, wild ungulates, sheep, goats and horses. The immature stages feed on hares and birds: the latter contributing to it being the most widespread Hyalomma species in Africa. Adults attach to the hairless areas on the animal: the lower perineum, peri-anal region, udder, and genitalia. Immature stages are invariably found on the head and neck of birds.

 

 

Life cycle and seasonal occurrence

Hyalomma rufipes has a two-host life cycle, that, depending on environmental conditions, may be completed in 1 year. Females lay c. 10 000 to 15 000 eggs, which hatch in 3 months; larvae feed for 5–7 days and nymphs for 7 days; it normally takes 4–5 months for nymphs to moult to adults; and adults feed for 5–7 days. Adults are most numerous in summer, and larvae and nymphs in the drier autumn, winter and early spring months. The engorged nymphs overwinter (undergo diapause) – enabling adult emergence in warmer, moister climes during late spring – and hence their long period of inactivity.

Disease

In addition to CCHF and the transmission of Rickettsia conori to humans, H. rufipes has also been implicated in the transmission of anaplasmosis (A. marginale) to cattle. The long mouthparts cause lesions at the attachment sites, that may lead to severe abscesses.

Figure 17 Hyalomma rufipes, male, dorsal view, illustrating the banded legs and dark scutum of this species. (Photo: A.A. Latif )

 

Habitat and distribution

Hyalomma rufipes is the most widely distributed of the three species in this genus in South Africa. With the exception of the eastern and southern coastal belts, it is present throughout the country. This is corroborated by the locality records and the modelled habitat suitability for this species (see Figure 18). High habitat suitability for H. rufipes – indicative of adaptation to dry climates – is evident over the more xeric west of South Africa, including the North West, almost the entire Northern Cape, and most of the Free State provinces. The low number of locality records in the central and northern regions of the Northern Cape Province, can be ascribed to a low sampling effort in this rather inhospitable region of the country. Except for a narrow strip along the south-eastern seaboard of KwaZulu-Natal and the Eastern Cape provinces – comprising the Indian Ocean Coastal Belt biome of Mucina & Rutherford (Figure 10) – where the tick is absent, there are confirmed locality records and medium to low habitat suitability in the remainder of South Africa.

Figure 18 The geographic distribution of Hyalomma rufipes in South Africa, and its modelled habitat suitability. Dots represent 1 109 confirmed localities.

 

Hyalomma truncatum – the small, smooth bont-legged tick

General

Hyalomma truncatum is a medium-sized tick, which is dark brown in colour with long mouthparts, beady eyes, and long banded legs. The posterior portion of the male scutum is sunken with numerous large punctations – giving it a rough appearance in contrast to the otherwise smooth scutum which is uniformly covered with small punctations.

Salient features

  • Hypostome and palps long (see Figure 19)
  • Eyes present and hemispherical
  • Ornate: legs have pale bands at articulations
  • Scutum dark brown and appearing smooth and shiny (small punctations) – except for the contrasting posterior depression with larger punctations
  • Areas around the spiracles with sparse setae
  • Marginal groove well defined and long in the male
  • Festoons present
  • Three sets of anal plates present in the males

Hosts

Adults prefer large domestic herbivores (cattle, sheep, goats, horses), as well as large, wild herbivores (giraffe in particular may become very heavily infested). Adults often attach to domestic dogs – causing large wounds at the attachment sites. Immature stages feed on hares and murid rodents. Adults may be found in the tail switch, around the anus, and on the lower perineum, legs and feet of the herbivores that they infest.

Life cycle and seasonal occurrence

Hyalomma truncatum has a two-host life cycle that may take up to a year to complete. Adults are most numerous in late summer, and immatures in the drier autumn, and in winter and early spring.

Disease

Hyalomma truncatum transmits Babesia caballi to horses, causing equine piroplasmosis, and Rickettsia conori to humans, causing tick-bite fever. The adults of some H. truncatum strains secrete an epitheliotrophic toxin in their saliva during feeding, which causes a disease called sweating sickness in cattle – particularly calves. The long mouthparts cause lesions which may become secondarily infected with bacteria, leading to abscesses; these wounds may also attract cattle blowflies, resulting in myiasis. Dogs may develop severe necrotic wounds at the attachment sites. Attachment of adults to the interdigital clefts and fetlocks of lambs may lead to lameness.

Figure 19 Unfed Hyalomma truncatum females, illustrating the dark scutum, long mouthparts and banded legs.

 

Habitat and distribution

Hyalomma truncatum is adapted to dry habitats, but is also prevalent in more temperate climates, and is present through much of South Africa. The locality records for H. truncatum and its modelled habitat suitability in South Africa, are illustrated in Figure 20. Except for the eastern region of the Eastern Cape, and a broad band around the Lesotho border including the south-eastern region of the Free State, central KwaZulu-Natal, and southwestern Mpumalanga and Gauteng – this tick occurs throughout South Africa. However, it appears to be only sparsely distributed in most of the Northern Cape Province. Areas of high habitat suitability are present in the North West Province, spilling over northwards and eastwards into the bordering provinces of Limpopo and Gauteng, and southwards around the junction between the North West, Free State and Northern Cape provincial borders. The basal area of the Cape Peninsula and the southern coastal area around Port Elizabeth in the Eastern Cape Province, also display high habit suitability.

Figure 20 The geographic distribution of Hyalomma truncatum in South Africa, and its modelled habitat suitability. Dots represent 807 confirmed localities.

 

Rhipicephalus (Boophilus) decoloratus – the blue tick

General

The common name ‘blue tick’ relates to the colour of the engorged females. This name leads to considerable confusion amongst lay persons in that the engorged females of several tick species are blue in colour. R. (B.) decoloratus (see Figure 21) is the commonest, most widespread and prevalent of the one-host ticks in Africa – to which it is indigenous.

Salient features

  • Scutum pale yellow and transparent, with the dark caeca of the gut evident from above
  • Hypostome and palps (mouthparts) short
  • Teeth on hypostome arranged in rows of 3+3 (only in this species of the subgenus)
  • Protuberance on the internal margin of the first (proximal) palpal segment bearing setae
  • Eyes present, small and often difficult to distinguish in the males
  • Legs slender, and pale yellow
  • Festoons absent
  • Anal plates present in the males – their tips visible in dorsal view
  • Small, tail-like caudal appendage present in the males

Hosts

Cattle are the main hosts, but R. (B.) decoloratus also feeds on horses, donkeys, sheep, goats and many wild ungulates. This is a one-host tick which feeds preferentially on the back, upper legs, neck, shoulders, dewlap and belly of cattle.

 

 

Life cycle and seasonal occurrence

Rhipicephalus (B.) decoloratus is a one-host tick. Females may lay 2 000 to 2 500 eggs, about 7 days after detaching from the host. Eggs hatch in 3–6 weeks under ideal conditions (see Figure 9) and larvae quest for a host on vegetation. Larvae feed and moult to the nymphal stage on the same host after 7 days; nymphs feed and moult to adults, still on the same host, within 7 days, with mating taking place on the host and females engorged within 7 days. The whole life cycle may be completed in c. 2 months, under ideal conditions, which may result in 4 generations per year being completed in areas of high suitability. Overwintering eggs hatch synchronously with the spring temperature rise – resulting in large numbers of larvae on the vegetation around October, and progressing to an even higher number in the summer months because of the tick’s short generation time.

Disease

Rhipicephalus (B.) decoloratus transmits the protozoan Babesia bigemina – a cause of bovine babesiosis (redwater) in cattle. The organism is transmitted only by the nymph and adult stages, but passes transovarially to the next generation and may be transmitted by many successive generations without individuals having to feed on another infected host. The species also transmits Anaplasma marginale – which causes anaplasmosis or gallsickness in cattle, and Borrelia theileri (spirochaetosis) in cattle, sheep, goats and horses. Heavy infestations may result in a reduction in the rate of growth of cattle.

Figure 21 Rhipicephalus (Boophilus) decoloratus adults: male (left) and female. (Photos: Heloise Heyne)

 

Habitat and distribution

Rhipicephalus (B.) decoloratus occurs typically in grassland and wooded areas with temperate climates, and tends to be absent in drier climes. The modelled habitat suitability for R. (B.) decoloratus in South Africa is illustrated in Figure 22. High habitat suitability for R. (B.) decoloratus is indicated over a large area of the mesic eastern region of South Africa, encompassing the Grassland and Indian Ocean Coastal Belt biomes of Mucina & Rutherford, the eastern and north-eastern portions of the Savanna biome, as well as the Fynbos biome of the Western Cape Province. Highly suitable habitats, in agreement with locality records, are evident in KwaZulu-Natal, Gauteng, Mpumalanga and Limpopo provinces – with lower suitability indicated in the western strip of Limpopo, the coastal region of the Western Cape, central and north-eastern Eastern Cape, the central and eastern region of the Free State, and the central and north-eastern region of the North West Province. Possible range expansion is indicated towards the west in the Free State and North West provinces. Habitat suitability for this species declines in the Succulent Karoo biome of the Western Cape Province, while the drier Nama-Karoo and the Savanna biomes of the Northern Cape and western regions of the North West provinces appear to be unsuitable habitats; the last mentioned shows an especially high degree of unsuitability.

Figure 22 The geographic distribution of Rhipicephalus (Boophilus) decoloratus in South Africa, and its modelled habitat suitability. Dots represent 2 308 confirmed localities.

 

Rhipicephalus (Boophilus) microplus – the Asiatic blue tick

General

Rhipicephalus (Boophilus) microplus is regarded as an exotic species and was introduced by accidental transportation on cattle – into East and South Africa from southern Asia via Madagascar – after the 1896 rinderpest outbreak. The species has since become very well established in southern and eastern Africa and is widespread in Madagascar. Over the last two to three decades, it has increased its range considerably, and has displaced the indigenous R. (B.) decoloratus in the Limpopo, Eastern Cape, Mpumalanga and North West provinces of South Africa. Although R. (B.) microplus is reputedly a cattle tick, goats have also been implicated as possible alternate hosts – although the maintenance of viable populations depends on the availability of cattle as major hosts. The ability of R. (B.) microplus to transmit to cattle B. bigemina, as well as the more pathogenic Babesia bovis, combined with its invasive potential – makes it the more dangerous of the two onehost ticks in this subgenus in South Africa.

Salient features

  • Scutum reddish-brown
  • Hypostome and palps (mouthparts) short
  • Teeth on hypostome arranged in rows of 4+4
  • Internal margin of the first (proximal) palpal segment concave (no protuberance as in R. (B.) decoloratus)
  • Eyes present, small, and often difficult to distinguish in the males
  • Legs slender, and pale yellow
  • Festoons absent
  • Anal plates present in the males
  • Small tail-like caudal appendage present in the males

Hosts

Rhipicephalus (B.) microplus probably propagates effectively only on cattle. In the presence of cattle, however, goats have also been implicated as alternate hosts. This species normally attaches to the belly, the surface above the udder or testes, the dewlap, shoulders, and flanks.

 

 

Life cycle and seasonal occurrence

Rhipicephalus (B.) microplus is a one-host tick – its life cycle being similar to that of R. (B.) decoloratus. However, R. (B.) microplus females lay c. 2 500 to 3 000 eggs, about 500 more than R. (B.) decoloratus; while it completes its feeding phase marginally faster than R. (B.) decoloratus and egg hatch occurs sooner (within 4 weeks). These characters combine to give it a reproductive edge over R. (B.) decoloratus in areas where they occur sympatrically. Males of both species will copulate with females of either species, and in concurrent infestations the marginally faster feeding rate and earlier emergence of R. (B.) microplus males, results in R. (B.) decoloratus females mated by R. (B.) microplus males producing sterile progeny – thus placing R. (B.) decoloratus at a further reproductive disadvantage. This higher reproductive potential has helped R. (B.) microplus to outcompete R. (B.) decoloratus in areas where they occur together, and has probably augmented its range extension (and displacement of R. (B.) decoloratus) over time.

The majority of larvae quest for hosts from the vegetation in spring, with successive generations accumulating through summer into autumn.

Disease

Rhipicephalus (B.) microplus transmits the protozoan parasites Babesia bigemina and Babesia bovis – which cause bovine babesiosis or redwater in cattle. B. bovis infection is acquired by adults feeding on infected hosts, and is then passed on transovarially to be transmitted by larvae in the next generation. The tick also transmits A. marginale, which causes bovine anaplasmosis (tick-transmitted gallsickness) and Borrelia theileri (the cause of spirochaetosis in cattle).

Figure 23 The geographic distribution of Rhipicephalus (Boophilus) microplus in South Africa, and its modelled habitat suitability. Dots represent 307 confirmed localities.

 

Habitat and distribution

This species occurs in grassland pastures – requiring more humid habitats than R. (B.) decoloratus. The modelled habitat suitability for R. (B.) microplus in South Africa is depicted in Figure 23. Well-defined areas of high habitat suitability for R. (B.) microplus within the Grassland biome are evident in the north-eastern region of the Eastern Cape Province. Indeed, the harbour city of East London, in this province, has been suggested as the initial port of entry for R. (B.) microplus into South Africa. Areas of high habitat suitability also extend into the southern regions of KwaZulu-Natal, and within the Savanna biome into the north-eastern region of Limpopo Province (Venda). Adjacent areas show median suitability – also evident in the northeastern region of the North West Province and a narrow belt adjoining the Kruger National Park in eastern Mpumalanga and Limpopo. In contrast to R. (B.) decoloratus, this species is absent in the Kruger National Park, which is not surprising as R. (B.) microplus is almost exclusively a cattle tick.

The number of locality records in areas of modelled low suitability in central Mpumalanga, northern Gauteng, the south-western Eastern Cape, and the Western Cape provinces, bear testimony to its invasive nature and apparent ability to utilise suitable environmental niches. The presence of R. (B.) microplus in these isolated pockets of apparent low suitability, indicates probable non-equilibrium distribution status in these areas, which is suggestive of continuing active dispersion. This is presently a cause of major concern to livestock owners because of the ability of the species to transmit B. bovis. The potential range expansion of R. (B.) microplus, within the areas of suitable habitat described here, thus warrants close monitoring in the future.

It has been postulated that R. (B.) microplus may well have reached equilibrium status in foci that are more suitable for it than for R. (B.) decoloratus (Figure 24), and that its dispersion and displacement may subside in areas more suitable for the latter species – i.e. the north-eastern region of the North West Province, the belt adjacent to the Kruger National Park, and the south-central part of the Eastern Cape Province.

Figure 24 Comparison of relative habitat suitability for R. (B.) microplus and R. (B.) decoloratus in South Africa.

 

Rhipicephalus appendiculatus – the brown ear tick

General

Known as the ‘brown ear tick’ because of the colour of the males and engorged females ( see Figures 25 and 26), and its preference for feeding on the ears of cattle. This species transmits East Coast Fever, caused by cattleadapted Theileria parva in east Africa, and is the vector of buffalo-associated T. parva, which causes Corridor disease in cattle in South Africa.

Salient features

  • Hypostome and palps of medium length
  • Basis capituli hexagonal
  • Eyes present, slightly convex
  • Festoons present
  • Anal plates present in the male
  • Legs increase in size from I–IV
  • Anterior process of coxa I, visible from above
  • Cervical fields large, curved, with scalpelshaped depressions
  • Narrow caudal appendage present in fed males
  • Medium to fine punctations on scutum

Hosts

This tick has an extremely wide distribution. All stages feed on cattle, while goats, nyala, greater kudu, eland, waterbuck and buffalo are all important main hosts. Immatures feed on the same hosts as the adults, as well as on smaller antelopes and scrub hares. The adults prefer to feed externally on the ear pinnae, spreading to the eyelids, horn base and upper neck – and even around the anus in heavy infestations. Immatures more commonly feed on the ears, muzzle, neck, dewlap and cheeks of cattle.

 

 

Life cycle and seasonal occurrence

Rhipicephalus appendiculatus is a three-host tick and all stages engorge within 4–7 days. Replete females lay c. 5 000 eggs, which hatch after 3 weeks to 3 months, depending on environmental conditions. The life cycle of R. appendiculatus is regulated by photoperiod, and in South African latitudes this species enters facultative diapause whereby adults that moult from nymphs in autumn are delayed in hostquesting behaviour induced by day-length conditions. Adults therefore engage in their quest for hosts only when day length is optimal – in higher latitudes synchronised with the rainy season in spring, resulting in a strictly seasonal single generation per year in South Africa. This phenomenon may well underpin the success of the East Coast Fever eradication campaign in the 1950s in South Africa, because successful stageto- stage transmission of the causative organism is reliant on only one generation per year. Adults are prevalent in summer, larvae in autumn to winter, and nymphs in late winter and early spring. Closer to the equator, day-night length is virtually the same over all seasons and rainfall is more evenly spread, so enabling a 3-month life cycle for this species and the completion of some 4 generations per year.

Disease

Rhipicephalus appendiculatus transmits buffaloassociated T. parva, which is the cause of Corridor disease in cattle in South Africa. Infection is acquired by larvae and nymphs feeding on an infected animal, and it is transmitted to the next susceptible host by the succeeding stage; the infection is not transmitted transovarially to the next generation. The tick also transmits T. taurotragi, which causes benign bovine theileriosis, and also Rickettsia conori, which is the cause of tick-bite fever in humans. Heavy infestations may result in immune suppression due to tick toxicosis that may lead to re-emergence of tick-borne diseases in infected animals, as well as tissue damage with resultant abscesses, or deformed or lost ear pinnae and wounds on udders and tails.

Figure 25 An unfed questing Rhipicephalus appendiculatus male.

Figure 26 A fully engorged (fed) Rhipicephalus appendiculatus female.

Habitat and distribution

This species requires good vegetation cover and thrives in woodland and savanna habitats, and does not survive in open grassland plains. The modelled habitat suitability for R. appendiculatus in South Africa is shown in Figure 27. The locality records indicate a predilection for the Savanna biome in the mesic east of South Africa. The species is absent in this biome as well as in the Namaand Succulent Karoo in the xeric west of the Northern Cape and North West provinces, and in the Fynbos biome of the Western Cape Province – indicative of a reliance on adequate rainfall. The south-eastern coastal area of the Western Cape Province displays some degree of habitat suitability for this species, but there are no confirmed locality records in this area. The morphologically similar Rhipicephalus nitens, which may be misidentified as R. appendiculatus, is prevalent in this area. The southern-most locality record is just south of Port Elizabeth in the Eastern Cape Province. With the exception of consistent confirmed collections in the northern region of the Free State Province bordering the North West Province in a relatively distinctive crater remnant zone (the Vredefort Dome area, categorised as Savanna by Mucina & Rutherford), R. appendiculatus is absent from the Grassland biome encompassing most of the Free State province. The remainder of the north-eastern region of the Free State Province displays low habitat suitability for this species. This is in agreement with reports that it does not occur in open grassland, but rather requires grass interspersed with trees or bush as a suitable habitat. Correspondingly, the Savanna biome in the mesic east of South Africa contains areas of high habitat suitability for this species. These extend from the southerncentral region of the Eastern Cape towards the north-eastern region of this province, and throughout most of KwaZulu-Natal, eastern Mpumalanga, Limpopo Province, northern Gauteng, and the north-eastern regions of the North West Province. The distribution of R. appendiculatus mirrors that of A. hebraeum in large parts of its preferred habitat.

Figure 27 The geographic distribution of Rhipicephalus appendiculatus in South Africa, and its modelled habitat suitability. Dots represent 1 556 confirmed localities.

 

Rhipicephalus evertsi evertsi – the red-legged tick

General

Rhipicephalus evertsi evertsi is quite easily distinguished from other ticks in the genus by its uniform reddish-orange legs, dark scutum, and convex beady eyes (see Figure 28). A subspecies, Rhipicephalus evertsi mimeticus – which has banded legs and may be mistaken for a Hyalomma spp. – occurs in the arid areas of Namibia and western Botswana, and viable populations occur in the north-western parts of the North West Province. R. e. evertsi is common on livestock, zebra and eland, and is the most widespread species of the genus Rhipicephalus in the Afrotropical Region.

Salient features

  • Hypostome and palps of medium length
  • Basis capituli hexagonal
  • Eyes present, convex, beady, orbited
  • Festoons present
  • Anal plates present in the male
  • Scutum dark, densely punctate, contrasting with reddish-orange body wall

Hosts

Adults prefer wild and domestic equids, but cattle, sheep, goats and a wide range of antelope species, especially eland, are readily utilised. Immatures feed on the same host range as the adults, as well as on scrub hares. Adults feed mainly under the tail around the anus, and sometimes in the groin and axillae and sternum of sheep and goats. Immatures feed, usually deep down, on the inner surface of the external ear canal.

 

 

Life cycle and seasonal occurrence

Rhipicephalus e. evertsi is a two-host tick. Replete females lay c. 7 000 eggs, which may hatch within 1 month. Larvae attach in the ear canal of a host, feed for 5–7 days, and moult in situ to nymphs that also feed for 5–7 days; engorged nymphs detach, overwinter in the moulting stage, and adults emerge in spring; adults attach to a new host and replete females detach after 5–7 days. Under ideal conditions more than one life cycle may be completed in one year. Adults are most active from spring to late summer, and immatures from mid-summer to early winter, but R. e. evertsi may be present throughout the year in warmer regions.

Figure 28 Rhipicephalus evertsi evertsi adults; male (left), and female (right). (Photos: Heloise Heyne)

 

Disease

Rhipicephalus e. evertsi is an important vector of Babesia caballi and Theileria (Babesia) equi – both causative organisms of piroplasmosis in domestic equids. Its adults are implicated in the intrastadial transmission of A. marginale to cattle. Adults emerging synchronously infest spring-born lambs in high numbers, and the animals become paralysed by a toxin secreted by engorging females – hence the name ‘springlamb paralysis’. The degree of paralysis induced is proportional to the number of engorging female ticks per kg body mass of the animal, and symptoms can be reversed by removal of the ticks.

Habitat and distribution

Increasing aridity appears to be the main factor restricting the distribution of this species. Locality records (Figure 29) indicate that R. e. evertsi occurs extensively in the Grassland and Savanna biomes in the mesic east of South Africa to the east of longitude 24° E, and in the Fynbos biome of the Western Cape Province, south of latitude 33° S. In addition, there are several confirmed locality records, in association with a median habitat suitability index, in the eastern region of the Northern Cape Province bordering the North West and Free State provinces. Excluding these records and an isolated pocket on the west coast, there are no locality records in the remainder of the Northern Cape Province, which is in agreement with the low habitat suitability for this species in this province.

Figure 29 The geographic distribution of Rhipicephalus evertsi evertsi in South Africa, and its modelled habitat suitability. Dots represent 2 787 confirmed localities.

 

Rhipicephalus simus – the glossy brown tick

General

Adults are large, dark ticks, which are characterised by the glossy appearance of their large, dark and smooth scutum – with that of the male characteristically having 4 longitudinal rows of large punctations (see Figure 30).

Salient features

  • Hypostome and palps of medium length
  • Basis capituli hexagonal, with blunt lateral angles
  • Eyes present, flat
  • Festoons present
  • Anal plates present in the male
  • Cervical fields large, curved
  • Scutum dark, smooth, glossy in appearance: 4 longitudinal rows of large punctations in the male; large punctations delineate the cervical groove of the female.

Hosts

Adults prefer cattle, horses and dogs, and monogastric wild animals such as large carnivores, rhinoceros, warthog, bushpig and zebra. Immatures parasitise murid rodents, and the availability of rodent hosts determines adult abundance. Adults attach in the tail switch and around the feet of cattle and horses, and around the head and neck of dogs.

Figure 30 Rhipicephalus simus adult male, dorsal view.

 

Life cycle and seasonal occurrence

Rhipicephalus simus is a three-host tick: replete females lay c. 5 000 eggs, and further detail on its reproductive biology is unclear. Adults are most abundant in the warm, wet summer on large hosts, larvae on rodents in spring, and nymphs on rodents during winter and spring.

Disease

Although R. simus can transmit A. marginale to cattle experimentally, it is an unlikely natural vector, as its immature stages feed almost exclusively on rodents which do not become infected with the bacterium. It also transmits Rickettsia conori (tick-bite fever) to humans. Adults produce a paralysis-inducing toxin that affects calves and lambs.

Habitat and distribution

The modelled habitat suitability for R. simus in South Africa is depicted in Figure 31. This species is established in regions with a savanna habitat and is never encountered in large numbers. Because the preferred sites of attachment of adult ticks on livestock are in the tail switch of cattle and around the feet of sheep, this may account for the dearth of recorded locality data. R. simus has been recorded most frequently in southern, eastern and northeastern South Africa. This distribution pattern is supported by the high habitat suitability evident for this species in the coastal region of the Eastern Cape, foci in KwaZulu-Natal, eastern and north-western Mpumalanga, eastern and western Limpopo, north-eastern North West, and in north-central Gauteng. Its distribution is predominantly within the Savanna biome, and it is most commonly encountered in vegetation types of undifferentiated woodland or scrub woodland. A number of locality records in areas of low habitat suitability may be due to the species being able to utilise suitable niches within these areas. This would especially be so, provided the preferred murid rodent hosts of the immature stages are abundant, as well as those of the adult stage.

Figure 31 The geographic distribution of Rhipicephalus simus in South Africa, and its modelled habitat suitability. Dots represent 177 confirmed localities.

 

Rhipicephalus zambeziensis

General

Rhipicephalus zambeziensisis is a dark-brown and heavily punctate tick. Its distribution is restricted to the north-eastern regions of South Africa. It is considered as important because of its similarity to R. appendiculatus – with both species transmitting buffalo-associated T. parva, which causes Corridor disease in cattle. Interspecific hybridisation with R. appendiculatus may occur and the two species may be difficult to distinguish where they occur together.

Salient features

Rhipicephalus zambeziensis is morphologically very similar to R. appendiculatus, but is more punctate.

  • Hypostome and palps of medium length
  • Basis capituli hexagonal, with blunt lateral angles
  • Eyes present, flat
  • Scutum dark
  • Coxa I anterior spurs visible dorsally in the male
  • Festoons present
  • Anal plates present in the male
  • Narrow caudal appendage present in fed males
  • Cervical fields large and curved with a noticeable wrinkled texture, conspicuously delineated by rows of distinct setiferous punctations along external cervical grooves

Hosts

The main hosts are cattle, greater kudu and impala, and adults have been found in relatively large numbers on lions. Adults attach on the head and ears on cattle and kudu, and predominantly on the muzzle of impala. Immatures are common on scrub hares and attach to the feet and legs of larger hosts.

Figure 32 The geographic distribution of Rhipicephalus zambeziensis in South Africa, and its modelled habitat suitability. Dots represent 29 confirmed localities.

 

Life cycle and seasonal occurrence

Rhipicephalus zambeziensis is a three-host tick and its seasonality mirrors that of R. appendiculatus – i.e. adults in late summer, larvae in autumn and winter, and nymphs in winter and early spring.

Disease

In South Africa R. zambeziensis is an important vector of the protozoan parasite T. parva, which causes buffalo-associated Corridor disease in cattle and Theileria taurotragi, which causes benign bovine theileriosis.

Habitat and distribution

Rhipicephalus zambeziensis is adapted to hot, dry conditions – tolerating relatively low humidity levels of 55% in the dry months, and less than 70% in wet months. The modelled habitat suitability for this species in South Africa is shown in Figure 32. R. zambeziensis is present in the great river valleys and adjacent low-lying areas of southern African countries – from Angola in the west to Tanzania in the east. A small number of locality records for this species in South Africa (29) represent its southernmost distributional range. In South Africa, R. zambeziensis replaces R. appendiculatus in the hot, dry Sabi and Limpopo river valley systems, with areas of overlap in wet to dry transitional zones. Its distributional range is in north-eastern Mpumalanga, north-eastern, western and the far northern border region of Limpopo Province, and the northern region of North West Province bordering Limpopo Province. High habitat suitability for this species is in agreement with locality records. However, high habitat suitability is also indicated in the south-central region of Limpopo Province where no locality data exist, and invasion in this area is thus highly probable. Areas of low habitat suitability – without evidence of occurrence and therefore indicative of a low possibility of range expansion – are flagged for north-eastern KwaZulu-Natal and the far northern border region of the Northern Cape and North West provinces.

Because of the similarities between Rhipicephalus appendiculatus and Rhipicephalus zambeziensis – especially in their morphology and function as vectors – the relative habitat suitability for the two species is compared in Figure 33.

Figure 33 Comparison of relative habitat suitability for R. zambeziensis and R. appendiculatus in South Africa.

 

How climate change could affect tick distribution

“He who loves practice without theory is like the sailor who boards ship without a rudder and compass and never knows where he may cast.”

– Leonardo da Vinci

Tick distribution data in this publication are based on existing climatic, vegetation and terrain variables for South Africa. It may, however, be prudent to take heed of general climate-change predictions for South Africa in the context of how this could affect future tick distributions according to their generalised environmental adaptations. With regard to climate change, evidence suggests that significant warming has occurred over western and central southern Africa, but more moderately in the coastal areas, over the last five decades. Furthermore, indications are that while global temperatures have increased by c. 1°C, those of southern Africa are increasing at twice the global trend. Thus, the temperature over this region may increase at an even faster rate over the coming decades, while the region generally becomes drier. Except for the possible direct effects of temperature and precipitation predictions on the tick species, their impact on hosts in particular – but also on land-cover, wildlife and agricultural practices – have to be considered. Extreme increases in temperature would probably damage the habitat structure of most of the economically important tick species in areas of marginal habitat suitability. However, a warmer central interior (i.e. Free State Province) – especially if associated with vegetation change in combination with discernible bush encroachment and land-use patterns for wildlife ranching – could create more suitable habitats for species that require a wooded savanna ecology. This would suit such tick species as: A. hebraeum, a species already encroaching in the north-western areas of the Northern Cape Province; and R. appendiculatus and most of the other economically important Rhipicephalus spp. (especially the onehost species, R. (B.) decoloratus and R. (B.) microplus). However, overall drier conditions would restrict their range expansion, whilst favouring the Hyalomma species. Over eastern South Africa, despite a projected general decrease in precipitation due to intensification of subtropical high-pressure systems in the troposphere, it is likely that summers will become wetter with more extreme rainfall events – especially over central South Africa. Wetter, moister summers in the eastern region of South Africa signal increased suitability, due to higher humidity levels for all tick species already prevalent in this region – especially the one-host species. However, a general decrease in precipitation may place restrictions on the three-host tick species. Higher seasonal precipitation in the central regions could open up suitable niches for A. hebraeum and R. appendiculatus. Although precipitation predictions are more uncertain, there are strong indications of regional increases in annual dry spells (indicative of more extreme dry seasons), increases in the annual wet spells (indicative of more extreme wet seasons), and increases in daily amounts of precipitation. Tick species such as A. hebraeum and R. evertsi evertsi may be forced into more definite seasonality patterns (i.e. the adults may be more restricted to summer prevalence). Climatic suitability for . (B.) microplus may even increase in areas currently unsuitable for this species.

To illustrate the possible effect of predicted climate change, the probability of the occurrence of R. appendiculatus for the period 2046–2065 – based on modelled future scenarios of temperature and rainfall – is shown in Figure 34. Compared with current modelled habitat suitability (Figure 27), the model predicts that habitat suitability for R. appendiculatus will decrease in the northern and eastern border regions of Limpopo and Mpumalanga provinces, and in the northeastern corner of KwaZulu-Natal. Increased habitat suitability is evident westward through central Mpumalanga into the eastern Free State and north-central North West provinces.

Figure 34 The probability of occurrence of R. appendiculatus for the period 2046–2065, based on modelled future scenarios of temperature and rainfall.

 

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