Ticks of domestic animals

Last updated

Ticks of domestic animals directly cause poor health and loss of production to their hosts. Ticks also transmit numerous kinds of viruses, bacteria, and protozoa between domestic animals. [1] These microbes cause diseases which can be severely debilitating or fatal to domestic animals, and may also affect humans. Ticks are especially important to domestic animals in tropical and subtropical countries, where the warm climate enables many species to flourish. Also, the large populations of wild animals in warm countries provide a reservoir of ticks and infective microbes that spread to domestic animals. Farmers of livestock animals use many methods to control ticks, and related treatments are used to reduce infestation of companion animals.

Contents

Adult male bont tick, Amblyomma variegatum Fabricius 1794. This species of tropical tick transmits the causative agent of heartwater disease and it alters the immune system of its livestock host such that dermatophilosis skin disease is greatly aggravated. Amblyomma-variegatum-male.jpg
Adult male bont tick, Amblyomma variegatum Fabricius 1794. This species of tropical tick transmits the causative agent of heartwater disease and it alters the immune system of its livestock host such that dermatophilosis skin disease is greatly aggravated.

Variety of ticks affecting domestic animals

Structure and internal anatomy of a hard tick, Ixodidae, showing the general positions and form of the major organs, legs, and feeding apparatus: Soft ticks, the Argasidae, have similar structures, but their mouthparts are smaller and project ventrally. Ixodid tick structure.jpg
Structure and internal anatomy of a hard tick, Ixodidae, showing the general positions and form of the major organs, legs, and feeding apparatus: Soft ticks, the Argasidae, have similar structures, but their mouthparts are smaller and project ventrally.

Ticks are invertebrate animals in the phylum Arthropoda, and are related to spiders. Ticks are in the subclass Acari, which consists of many orders of mites and one tick order, the Ixodida. Some mites are parasitic, but all ticks are parasitic feeders. Ticks pierce the skin of their hosts with specialized mouthparts to suck blood, and they survive exclusively by this obligate method of feeding. Some species of mites may be mistaken for larval ticks at infestations on animal hosts, but their feeding mechanisms are distinctive. All ticks have an incomplete metamorphosis: after hatching from the egg, a series of similar stages (instars) develops from a six-legged larva, to eight-legged nymph, and then a sexually developed, eight-legged adult. Between each stage is a molt (ecdysis), which enables the developing tick to expand within a new external skeleton. Ticks are grouped in three families, of which two have genera of importance to domestic animals, as follows. [2] The family Argasidae contains the important genera Argas, Ornithodoros, and Otobius. These genera are known as soft ticks because their outer body surfaces lack hard plates. The family Ixodidae contains 14 genera, [3] including Amblyomma, Dermacentor, Haemaphysalis, Hyalomma, Ixodes, Margaropus, and Rhipicephalus. Also, the important boophilid ticks, formerly of the genus Boophilus, are now classified as a subgenus within the genus Rhipicephalus. [4] [5] These genera are known as hard ticks because their outer surfaces have hard plates. Within these genera are, very roughly, 100 species of importance to domestic animals. [6] Some of these species are also important to humans. The only countries that do not have some kind of problem with ticks on domestic animals are those that are permanently cold. An outline classification of the Acari, including the two families of ticks of importance to domestic animals is in the article Mites of livestock.

Typical ticks of domestic animals

Amblyomma and Rhipicephalus ixodid ticks

Life-cycle of a typical three-host tick Three-host-life-cycle-hard-tick.png
Life-cycle of a typical three-host tick
Development stages of ixodid tick Rhipicephalus appendiculatus; E=eggs, L=larvae, N=nymphs, F=female, M=male; upper row unfed ticks, lower row fully engorged larvae, nymphs and a female; all same scale Life-cycle-of-ixodid-tick.jpg
Development stages of ixodid tick Rhipicephalus appendiculatus; E=eggs, L=larvae, N=nymphs, F=female, M=male; upper row unfed ticks, lower row fully engorged larvae, nymphs and a female; all same scale

Amblyomma species are widespread on domestic animals throughout tropical and subtropical regions. Typical Amblyomma species are: Amblyomma americanum , the lone star tick of the Southern and Eastern USA; Am. cajennense, the Cayenne tick of South America and Southern USA; Amblyomma variegatum , the bont tick of Africa and the Caribbean (see Gallery below for photograph of female and male). A typical Rhipicephalus species is Rhipicephalus sanguineus , the tropical dog tick, specialized to feed only on dogs. It is distributed globally throughout the warm countries, wherever humans with their dogs live. Typical Rhipicephalus species that feed on cattle in Africa are R. appendiculatus, the brown ear-tick, and R. evertsi, the red-legged tick. Rhipicephalus (Boophilus) microplus (or now simply Rhipicephalus microplus) is the most important tick of cattle in many tropical and subtropical countries to which it spread from Southeast Asia on transported cattle.

Boophilid ticks, a subgenus within Rhipicephalus

Rhipicephalus appendiculatus female and male dorsal at top, Rhipicephalus (Boophilus) microplus female and male dorsal at bottom (single photograph at one scale) Rhipicephalus species dorsal.jpg
Rhipicephalus appendiculatus female and male dorsal at top, Rhipicephalus (Boophilus) microplus female and male dorsal at bottom (single photograph at one scale)

These ticks, commonly known as cattle ticks or blue ticks, have a highly characteristic morphology and one-host lifecycle. They have high specificity for cattle as hosts and their morphological characteristics used for identification are less distinct than those of three-host rhipicephalids such as R. appendiculatus. They are economically important to the cattle-rearing industry by causing direct parasitic losses and by transmission of microbes. In addition to Rhipicephalus microplus , species of most importance to domestic animals are R. annulatus, which is widespread in tropical and subtropical countries, and R. decoloratus which occurs in Africa.[ citation needed ]

One-host lifecycle of R. microplus

Lifecycle of a typical one-host tick One-host-tick-lifecycle.png
Lifecycle of a typical one-host tick

These ticks are adapted to the advantages of specialising to feed on cattle and with all the feeding stages occurring on one individual host in a rapid sequence. They also can survive by feeding on deer or some wild bovid hosts. Infestation starts when larvae on vegetation attach to a new host. When a larva feeds, it molts at the site where it feeds and emerges as a nymph. The nymph feeds at the same site or close by and molts where it feeds. It emerges from molt as either an adult female or male. The female's single large blood meal is converted into a batch of 2000 eggs. The males take several small meals of blood to support their repeated attempts at mating. The molts are rapid and the next stage remains in the hair coat to start feeding again. The combined feeding and molting periods take about 21 days. The engorged female drops from the host, hides under leaf litter on soil surface, lays one batch of eggs, and then dies. When eggs hatch, the larvae crawl up grass stems and wait until they can attach to passing cattle.[ citation needed ]

Hyalomma ticks

Hyalomma rufipes female and male, dorsal Hyalomma-rufipes-female-male.jpg
Hyalomma rufipes female and male, dorsal

This genus contains many species of hard ticks important to domestic animals in hot, dry regions in Africa, the Mediterranean basin, the Middle East, Pakistan, India, [7] and through to China. Typical species are Hyalomma anatolicum, Hy. rufipes, Hy. truncatum, and Hy. detritum, which feed as adults on cattle, sheep, and goats. Hyalomma dromedarii is specialized to feed on dromedary camels. Hyalomma ticks are adapted to live in regions with large seasonal variation of temperature and low rainfall. Diapause is an important mechanism to adjust to these climates. Another adaptation is to have a lifecycle within one species that can be two-host or three-host. For example: Hy. anatolicum may feed on a hare, molt on the hare, and feed again on the same individual hare, detach and molt to an adult and then feed on a cow - that is a two-host lifecycle. Or it may feed as a larva on a gerbil, then as a nymph on a cow, and then as an adult on another cow in a three-host lifecycle. Furthermore, this tick commonly feeds as a three-host tick with larvae, nymphs, and adults feeding on separate individual dairy cows confined to cattle housing in zero-grazing systems.[ citation needed ]

Argas and Ornithodoros soft ticks

Ornithodoros savignyi argasid tick, dorsal. Ornithodoros-savignyi-dorsal.jpg
Ornithodoros savignyi argasid tick, dorsal.

Argas persicus, the fowl tick, is a major pest of poultry birds. The tampan ticks within the Ornithodoros moubata complex of species infest domestic pigs and also feed on humans. Ornithodoros savignyi is often found in large numbers at enclosures where camels and cattle are herded. Many species of argasid soft ticks are adapted to live in the nest or regular resting sites of their hosts, often waiting for months or even years for the host to return and enable the tick to feed. This nest-dwelling behavior is described as endophilic or nidicolous.[ citation needed ]

Multihost lifecycle of O. moubata

Lifecyle of Ornithodoros soft tick Multi-host-tick-lifecycle.png
Lifecyle of Ornithodoros soft tick

Argasidae soft ticks have different lifecycles from Ixodidae hard ticks, and these are very variable between species. [1] Typically, in Ornithodoros, a larva hatches from an egg laid in the nest or resting place of the host. The larva does not feed, but directly molts into the first nymph stage. This stage feeds, then molts into the next nymph stage. Feeding by soft ticks is generally completed within minutes rather than days, as with hard ticks. Depending on circumstances, four or five nymph stages occur, each progressively larger. Finally, a molt produces an adult female or male. The female takes repeated blood meals that are small compared to a female hard tick. Each blood meal is converted to a small batch of eggs. The male feeds sufficiently to support its mating. The lifecycle of Argas persicus is similar, but the larva feeds on blood of its bird host, remaining attached around 7 days.[ citation needed ]

Other groups of ticks

Other genera with species that are often of high local importance to domestic animals include the following examples, some of which are illustrated in the gallery below. Ixodes ( Ixodes ricinus , the deer tick of Europe; Ixodes scapularis , the black-legged tick of North America; Ixodes holocyclus , the paralysis tick of Australia). Haemaphysalis (Ha. leachii, the yellow dog tick of the tropics). Dermacentor ( Dermacentor andersoni , the Rocky Mountain wood tick; Dermacentor variabilis , the American dog tick; D. reticulatus , the ornate dog tick of Europe). D. nitens, the tropical horse tick of the Americas, has a one-host lifecycle similar to the boophilids. Margaropus winthemi, the beady-legged tick, infests horses and cattle in South Africa. The soft tick Otobius megnini, the spinose ear tick, has its nymphs feeding within the ear canal of many species of domestic animals. Adults of Ot. megnini do not feed. This tick occurs in the Americas and has spread to Africa and Asia.[ citation needed ]

Negative impacts to health

Biting stress and lost production

Rhipicephalus appendiculatus adults feeding at their favourite site on a calf: Each engorging female reduces gain of weight of calf by 4 g. Rhipicephalus-appendiculatus-calf-ear.jpg
Rhipicephalus appendiculatus adults feeding at their favourite site on a calf: Each engorging female reduces gain of weight of calf by 4 g.

When a hard tick pierces the skin of its host, initially little or no pain is caused. Later, during the prolonged feeding of ticks, inflammation is caused at the wound, followed by acquired immune reactions in the skin (dermal hypersensitivities types 1 and 4) to the foreign proteins in tick saliva. This defense by the host is generally effective, but at the cost of pruritus (itch) and pain at the feeding site. Infestations of ticks on certain individual animals of a herd of livestock animals can build up to very high levels. This occurs on a minor proportion of individuals in the herd, whilst most individual animals have low infestations. On a herd basis, the accumulated effect of this biting stress can cause loss of appetite and loss of blood. These two losses result in reduced feed intake and anemia; combined, they cause a lower rate of growth or of milk production compared to hosts without tick infestation. [8] [9] The feeding of soft ticks can cause severe biting stress because of the pain whilst they feed; Ornithodoros savignyi feeding on livestock that are herded in enclosures during nighttime is one notorious example.

Physical damage

Amlyomma variegatum adults feeding at udder of a heifer Amblyomma-variegatum-heifer-Ghana.jpg
Amlyomma variegatum adults feeding at udder of a heifer

At each feeding site of hard ticks, granuloma and wound healing produce a scar that remains for years after the tick has detached. When the skin of livestock animals is made into leather, these scars remain as blemishes that reduce the value of the leather. Larger ticks cause obstructive and painful damage, such as Amblyomma variegatum adults, which often feed on udders of cattle and reduce suckling by the calves. Hyalomma truncatum adults feed on the feet of sheep and goats, causing lameness. Wounds caused by dense clusters of adult ticks can make the host susceptible to infestation with larvae of flesh-eating myiasis flies, such as the screw-worm, Cochliomyia hominivorax . [10] [11]

Poisoning

Calf showing signs of sweating sickness Sweating-sickness-Zimbabwe.jpg
Calf showing signs of sweating sickness

When ticks feed, they secrete saliva containing powerful enzymes and substances with strong pharmacological properties to maintain flow of blood and reduce host immunity. Sometimes, this causes a poisoning of the host. This is not because of a functional toxin in the sense that snake poison is functional for the snake. However, the result can be various forms of toxaemia caused by a variety of ticks. A moist eczema, sometimes with hair loss (alopecia) known as sweating sickness in cattle is caused by Hyalomma truncatum. Tick paralysis can be life-threatening and is caused in sheep by feeding of Ixodes rubicundus of South Africa. In cattle, paralysis is caused by both Dermacentor andersoni in North America and the Australian paralysis tick, Ixodes holocyclus.I. holocyclus also causes paralysis in dogs and humans. [12] [13] [14]

Ticks as vectors of disease

Because ticks feed repeatedly and only on blood, and have long lives, they are suitable hosts for many types of microbes, which exploit the ticks for transmission between one domestic animal and another. Ticks are thus known as vectors (transmitters) of microbes. Most of these parasitic relationships are highly developed with a strict biological relationship between the microbe and the tick's gut and salivary glands. However, some microbes, such as Anaplasma marginale and A. centrale, can also be transmitted by biting flies, or by blood on injection needles (iatrogenic transmission). A characteristic of diseases caused by tick-transmitted microbes is that herds or flocks of livestock often acquire effective levels of immune resistance to both the vector ticks and the microbes, so outbreaks of acute disease tend to be rare. This stability is often due to immunity to the microbes developing as a result of survival through early infection from ticks carrying small infective doses of the microbe, the epidemiology of infections with Babesia species of protozoa is a well described example. [15] The ticks are often constantly present and long-lived. Acquisition of immunity may be aided by the protection of antibodies in the mother's colostrum (first milk).

At least one microbe causing disease associated with ticks is not transmitted by the ticks. The skin disease dermatophilosis of cattle, sheep, and goats is caused by the bacterium Dermatophilus congolensis , which is transmitted by simple contagion. When Amblyomma variegatum adult ticks are also feeding and causing a systemic suppression of immunity in the host, then dermatophilosis becomes severe or even fatal. [16]

Viral diseases

The virus of Nairobi sheep disease in East Africa is transmitted by Rhipicephalus ticks. African swine fever is naturally transmitted between wild species of the pig family by feeding of Ornithodoros moubata group ticks. This pattern of transmission can expand to include domestic pigs. However, within groups of domestic pigs, the virus can also be transmitted by contagion. Crimean-Congo hemorrhagic fever virus is transmitted between many mammal species by Hyalomma truncatum, Hyalomma rufipes, and Hyalomma turanicum over a wide area of Africa, Europe, and Asia. In cattle and sheep, it causes mild fever and its main importance is when it spreads to humans (zoonosis) by feeding of the larvae or nymphs of these ticks. [17] There are other viruses transmitted by ticks between wild animals and that have zoonotic importance when humans also become infected. The epidemiological pathways of these viruses can also involve domestic animals, if only by being hosts that add to the size of the tick population. Examples include the viruses that cause Tick-borne encephalitis, and Kyasanur Forest disease. [18]

Bacterial diseases

Anaplasma centrale in red blood cells of a cow (Giemsa stained) Anaplasma-centrale.jpg
Anaplasma centrale in red blood cells of a cow (Giemsa stained)

Borrelia bacteria are well described elsewhere in association with Ixodes ticks for causing Lyme disease in humans, but this disease also affects domestic dogs. Borrelia anserina is transmitted by Argas persicus to poultry, causing avian borreliosis in a wide spread of tropical and subtropical countries. [19] Anaplasma phagocytophilum (formerly Ehrlichia phagocytophila) is a bacterium of deer that spreads to sheep where it causes tick-borne fever in Europe, resulting in abortion by ewes and temporary sterility of rams. This bacterium invades and proliferates in neutrophil cells of the blood. This depletes these antibacterial cells and renders the host susceptible to opportunistic infections by Staphylococcus aureus bacteria which invade joints and cause the crippling disease of sheep called tick pyaemia. Anaplasma marginale infects marginal areas of red blood cells of cattle and causes anaplasmosis wherever boophilid ticks occur as transmitters. Anaplasma centrale tends to infect the central region of red blood cells, and is sufficiently closely related to An. marginale to have been used from long ago as a live vaccine to protect cattle against the more virulent An. marginale. Sheep and goats suffer disease from infection with Anaplasma ovis which is transmitted similarly to the anaplasmas described above. Ehrlichia ruminantium (formerly Cowdria ruminantium) is transmitted mainly by Amblyomma hebraeum and Am. variegatum in Africa, causing the severe disease heartwater in cattle, sheep, and goats. This disease is named after the prominent sign of pericardial edema. The bacteria infect the brain, causing prostration. Heartwater also occurs on the Caribbean islands, having spread there on shipments of cattle from Africa about 150 years ago, before anything was known of tick transmitted microbes. [11] [20]

Protozoal diseases

Blood film from dog infected with Ehrlichia arrowed above within a lymphocyte and Babesia arrowed below in erythrocyte (Giemsa stained) Ehrlichia-and-babesia-dog-South-Africa.jpg
Blood film from dog infected with Ehrlichia arrowed above within a lymphocyte and Babesia arrowed below in erythrocyte (Giemsa stained)

Babesia bovis protozoa are transmitted by R. microplus and cause babesiosis or redwater fever in cattle throughout the tropics and subtropics wherever this boophilid species occurs. The less pathogenic Ba. bigemina is transmitted by R. microplus and R. decoloratorus. Development of Babesia in the tick is complex and includes sexual reproduction. These Babesia are transmitted from adult female boophilid ticks to the next generation, as larvae, by infection of the eggs. This is known as transovarian transmission; it provides the only opportunity for transmission through one-host ticks. Other species of Babesia are transmitted by three-host ticks in ways similar to Theileria protozoa, as described below. In cattle, infection of the red blood cells may grow rapidly to create a potentially fatal inflammatory crisis of the blood. The name redwater (coloured urine) derives from the hemoglobinuria caused by the destruction of red blood cells infected with the merozoite stage of Babesia; anemia results from the same destruction. Horses suffer babesiosis or biliary fever when infected by Ba. equi or B. caballi. This occurs in many countries where vector ticks are found, such as R. e. evertsi, Hy. truncatum, and D. nitens. Dogs are at risk from severe infection with Ba. canis and its subspecies, transmitted by the dog ticks R. sanguineus, D. reticulatus , and Ha. leachi. Domestic cats become infected with Ba. felis and Ba. cati from feeding ticks. Cytauxzoon felis is a protozoan related to Babesia and Theileria. It is transmitted by the American dog tick, Dermacentor variabilis . This microbe circulates between wild bobcats in southern USA, causing little apparent disease. If it infects domestic cats, it causes a cytauxzoonosis that is eventually fatal.[ citation needed ]

Transmission of Babesia from cow to cow by feeding of one-host boophilid ticks Babesia-bovis-transmission.png
Transmission of Babesia from cow to cow by feeding of one-host boophilid ticks

Theileria annulata is a protozoan closely related to Babesia. In cattle, it causes the disease tropical theileriosis throughout a long arc of countries from Morocco across to China. [21] Theileria parva is the causative microbe of East Coast fever of cattle in Eastern, Central, and Southern Africa. Theileria species infect monocytic white blood cells of their hosts. The infected cells are induced to divide by the Theileria, which then proliferates within each daughter cell, in a rapidly expanding infection. This causes multiple inflammatory crises, of which pulmonary edema is a predominant cause of death. Theileria annulata is transmitted by Hy. anatolicum, Hy. detritum, and other hyalommas. Theileria parva is transmitted predominantly by Rhipicephalus appendiculatus. Because this is a three-host feeding tick, the opportunities for transmission are from infected cow to feeding larva then through the molt into the nymph which feeds and transmits. Similarly, transmission can also be from feeding nymphs to infected adult. This is known as transstadial transmission, and no transovarian transmission occurs in this case. The development of Theileria in ticks includes sexual reproduction which enables generation of new variants that can evade the immune mechanisms of cattle. [22]

Disease control methods

Treatment with chemical and botanical pesticides against ticks

Synthetic chemical acaricides

Dipping cattle to control Amblyomma variegatum ticks Dipbath-Nevis.jpg
Dipping cattle to control Amblyomma variegatum ticks

Ticks infesting sheep and cattle have been controlled with a wide variety of chemicals ranging from coal tar extracts, arsenic salts, and specific pesticidal chemicals such as DDT for many decades. These are now replaced by various synthetic chemicals of high specificity for acarines and ticks, and farmers frequently rely on treating their animals with these materials as their default method. [23] However, the expense of labour, equipment and acaricide can sometimes upset a good balance of cost : benefit with conventional treatment methods. [24] Synthetic chemical pesticides specific for ticks (acaricides) are suspended in water for application to the hair coat of domestic animals. Cattle can be immersed in dip-baths containing dipwash, or soaked using a pressurized spray-race made of metal tubing and nozzles. Sheep can be treated in smaller dips or showers. Acaricides can be applied to dogs in watery shampoo formulations. Acaricide active ingredients are usually soluble in oil. This makes them suitable for concentrated oily formulations which spread from a pour-on applicator over the hair coat. Alternatively, some acaricides are incorporated in polyvinylchoride plastic ear tags for cattle, or collars for dogs. [25] [26] Modern acaricides belong to the general classes of organophosphates (example chlorfenvinphos), formamidines (example amitraz), synthetic pyrethroids (example flumethrin), phenylpyrazoles (example fipronil), and benzylphenyl ureas (example fluazuron).[2] When correctly applied, they can be highly effective. Problems with acaricides are: danger of acute poisoning of treated animals and human staff; residues contaminating meat and milk; environmental contamination especially water sources; resistance that ticks acquire to acaricides; and cost of application. Cost and contamination can be reduced by seasonal timing of application (strategic treatment) based on ecological knowledge. Prediction of best times for treatment can be made using computerized models of the population dynamics of ticks. [27] [28] [29]

Botanical acaricides

Farmers lacking access to, or sufficient cash for, manufactured synthetic acaricides often use various herbal treatments, locally available. Nicotine from treated tobacco leaf is an example, but such unregistered preparations require careful use to avoid poisoning or skin damage. Commercially formulated botanical acaricide may often be available in tropical regions, containing the active ingredient azadirachtin. This is extracted as neem oil from fruits and seeds from the need tree, Azadirachta indica . [30]

Eradication of ticks

Eradication of ticks, as total removal of all populations of a species over a wide geographical area defined by natural boundaries, has been attempted several times. [31] In the southern states of the USA the tick then known as Boophilus annulatus (Rhipicephalus annulatus) was eradicated for the purpose of control of babesiosis in cattle. The eradication was successful after more than 50 years of control with much emphasis on dipping in chemical acaricides. The tick was eradicated up to the border of USA with Mexico, and a control and quarantine zone remains in place there. [32] Similar efforts were made to eradicate the tick then known as Boophilus microplus (also a Rhipicephalus, Rhipicephalus microplus) from New South Wales, Australia. However, this failed, partly due to the difficulty of maintaining a barrier against invasions from the more favourable areas for the tick in sub-tropical Queensland. [33] Amblyomma variegatum was subject to a multi-country eradication program in the Caribbean area, but it failed for complex economic and political reasons. [34]

Biological and ecological based methods in control of ticks and transmitted microbes

Cattle breeding for disease resistance

Australian Friesian Sahiwal cow. AFS cow.jpg
Australian Friesian Sahiwal cow.

Breeding for resistant cattle has been successful for their ability to acquire strong immune resistance to Rhipicephalus microplus following natural exposure to these ticks. [35] Commercial breeds of cattle (examples: Australian Friesian Sahiwal and Australian Milking Zebu) are successful in the relevant environment. Only a few commercial breeds of tick-resistant cattle are available. These breeds were developed under laboratory conditions where bulls were selected for good ability to acquire immune resistance to ticks and cows were selected for heat tolerance and milk-yield. There is scope for selecting cattle under farm conditions by culling those animals persistently with heavy infestations of ticks.[ clarification needed ] This is due to a characteristic of many parasitic infestations where in a population of hosts a few individual hosts carry heavy infestations whilst the majority are lightly infested. This is called an overdispersed, or aggregated, distribution; it may be caused by individual variation in immune competence. [36]

Pasture management

Larvae of Rhipicephalus microplus questing on grass. Rhipicephalus-microplus-larvae-questing.jpg
Larvae of Rhipicephalus microplus questing on grass.

For farms infested with R. microplus in Australia and South America, rotation of pasture can kill the questing larvae. [37] Pasture management is feasible for control of these one-host ticks because the only stage on vegetation that quests for hosts is the larva stage. Because of their small size larvae are highly susceptible to dehydration and starvation so a period without access to hosts of approximately two months can be effective. The nymphs and adults of three-host ticks, such as Amblyomma and Rhipicephalus species, can live for many months to a year or more, respectively, whilst questing on the vegetation. Thus it is usually not practical to control them by pasture management. In addition, farmers find the priority to provide their stock with good feed often conflicts with the regimes for pasture rotation for tick control. [38] Ticks affecting dogs and other companion animals around private houses are reduced by clearing of vegetation and leaf litter, mowing grass short, and fencing out deer and other wild animals that bring in ticks.

Epidemiological factors

Compared to other arthropods of veterinary and medical importance most species of ticks are long-lived over their whole life-cycle. Ixodes species in cool temperate climates typically take one year to develop through each of the three feeding stages. Amblyomma species may also have a three-year life-cycle and the adults can live off-host, without feeding for up to two years. Ornithodoros and Argas ticks are particularly adapted to wait for their hosts to arrive by being able to survive for years between blood meals as adults, 18 years have been recorded for O. lahorensis. [2] [39] Food reserves for survival of off-host ticks include large membrane bound vesicles of lipid in the digestive cells of their gut. Further adaptations include a thick integument with waxy waterproofing combined with ability to secrete hygroscopic salts from specialized parts of their salivary glands (type 1 acini) out to the exterior of their mouthparts and then suck back in the watery solution that develops around the salty material. [40]

Engorged nymphs of Rhipicephalus appendiculatus showing effects of cattle immune resistance; top rows nymphs fed on non-immune host, bottom rows nymphs of reduced mass that fed on an immune host. Rhipicephalus-appendiculatus-nymphs-cattle-resistance.jpg
Engorged nymphs of Rhipicephalus appendiculatus showing effects of cattle immune resistance; top rows nymphs fed on non-immune host, bottom rows nymphs of reduced mass that fed on an immune host.

It has been shown that at least some species of ticks have fairly stable populations, with variations in population densities from year to year varying by approximately 10-fold to 100-fold. [41] The abiotic (environmental) factor that appears to have most influence on tick distribution and abundance is dehydration stress from the combination of high temperatures and low moisture (measured as relative humidity or low saturation deficit, usually resulting from a climate of low rainfall). Computer models to test hypotheses and to predict the distribution of ticks reflect these stresses, using meteorological information where available, or indices of vegetation type as an analogue of temperature and dehydration stress. [42] [43] Biotic (host related) factors that influence tick distribution and abundance include the obvious need for the hosts to which the ticks are adapted to be present, and also the defenses that the hosts have against the ticks. During the life-cycle of a three-host tick feeding on its natural host that has acquired immunological resistance to the feeding of the ticks there can be high tick mortality. [44] This mortality is highest for the larvae which are easily killed by the immune reactions in the host's skin. It is lowest in the feeding adults. However, even if the ticks do feed, detach and moult the size of newly moulted adults is less, and the reproductive capacity of the females is reduced. [45] These biotic factors are likely to produce a pattern of mortality of the ticks that is density-dependent. [43] A high density of ticks attempting to feed will induce strong immune resistance in their hosts but a low density of ticks will not induce such strong resistance.

Ticks combine long life of the stages of that carry pathogenic microbes and long survival of these microbes in specialized niches within the tick, such as within cells of the salivary glands or the gut. In a population of Rhipicephalus or Hyalomma ticks feeding on cattle in which Theileria species of protozoa circulate and cause theileriosis, the ticks act as long term reservoirs of the protozoans. In addition, some species of protozoans (within the Theileria and Babesia genera), are able to infect ticks even when they exist in the blood of their hosts at such a low level that no signs of disease can be detected. This is known as a carrier state of infection. [46] [47] These pathogenic protozoa can be detected circulating in populations of the cattle hosts and tick vectors with only low levels of detectable disease in the cattle caused by the protozoa. Any situation like this - with prevalent infection or infestation but little disease - is called endemic stability. [48] It is possible that this can be exploited for better control of tick related diseases by use of breeds of cattle with good ability to acquire resistance to both the ticks and the protozoans. However, there are commonly situations where the potential benefits of endemic stability to disease are difficult for farmers to use effectively. The farmers may prefer to rely more on direct tick control, and drugs and vaccines against the protozoans. [49] [50]

Drug treatment against microbes

Antibiotics with efficacy against bacterial pathogens transmitted by ticks include: tetracycline, penicillin, and doxycycline. Against Babesia protozoa are imidocarb and diminazine, both of which can be used to treat patent clinical infections. [51] Against Theileria are parvaquone and halofuginone, both effective for clinical cases. [52] These drugs are usually administered to treat diagnosed cases, but the timing of treatment then becomes critical. Problems with drug treatment include the development of resistance by the microbes and cost. Also, treatment does not necessarily fully clear infections and this may lead to persistent subclinical infections which remain infective to more ticks (carrier infections); this may be considered unsafe in some situations.[ citation needed ]

Vaccination against microbes and ticks

Vaccination against An. marginale is done using live strains of the cross-reactive An. centrale. [53] Vaccines are available on a commercial basis to immunize cattle against Babesia bovis. [54] This is made by serial infection of calves to attenuate the virulence of the strain of Babesia, followed by splenectomy to produce many of the piroplasm stage in blood, which is then bottled for use. The vaccine is delivered containing the live protozoa to induce immunity without acute disease. [55] Theileria annulata can be grown and attenuated in virulence by means of infecting cell cultures with the schizont stage of the protozoan. This is delivered as a frozen vaccine from which live parasites are thawed out before injection. [56] [57] Cattle can be protected against East Coast fever by an infection-and-treatment procedure. Rhipicephalus appendiculatus ticks are infected with Theileria parva under laboratory conditions; theilerial sporozoites are extracted from the ticks and stored in liquid nitrogen; infective doses of the live vaccine are delivered to identified cattle and a few days later a protective dose of antibiotic is delivered to stop the infection from developing into clinical East Coast fever. [58] Vaccines are often highly effective, but the live parasite vaccines have problems of potential contamination with other microbes and induction of a carrier state which may be unwanted. Intensive attempts are made to develop vaccines to control these diseases using a recombinant DNA techniques to synthesize the relevant antigens, but as with vaccines against human malaria this is a difficult technological challenge. [59] [60]

A commercial vaccine was developed in Australia against Rh. microplus. [61] [62] It acts against a glycoprotein molecule that is exposed on the outer membrane of digestive cells of the gut of feeding ticks. This molecule is synthesized using recombinant DNA technique to make the antigen of the vaccine. Vaccinated cattle develop antibodies circulating in their blood. When the Rh. microplus female ticks engorge with blood, the antibody reacts with the natural antigen in their guts so strongly that digestion is disrupted and the reproductive rate of the ticks is reduced. This vaccine is manufactured in Australia and a closely similar vaccine is manufactured in Cuba. [63]

Related Research Articles

Ixodidae

The Ixodidae are the family of hard ticks or scale ticks, one of the three families of ticks, consisting of over 700 species. They are known as 'hard ticks' because they have a scutum or hard shield, which the other big family of ticks, the 'soft ticks' (Argasidae), lack. They are ectoparasites of a wide range of host species, and some are vectors of pathogens that can cause human disease.

Babesiosis Malaria-like parasitic disease caused by infection with the alveoate Babesia or Theileria

Babesiosis or piroplasmosis is a malaria-like parasitic disease caused by infection with a eukaryotic parasite in the order Piroplasmida, typically a Babesia or Theileria, in the phylum Apicomplexa. Human babesiosis transmission via tick bite is most common in the Northeastern and Midwestern United States and parts of Europe, and sporadic throughout the rest of the world. It occurs in warm weather. People can get infected with Babesia parasites by the bite of an infected tick, by getting a blood transfusion from an infected donor of blood products, or by congenital transmission . Ticks transmit the human strain of babesiosis, so it often presents with other tick-borne illnesses such as Lyme disease. After trypanosomes, Babesia is thought to be the second-most common blood parasite of mammals. They can have major adverse effects on the health of domestic animals in areas without severe winters. In cattle the disease is known as Texas cattle fever or redwater.

<i>Babesia</i> Genus of protozoan parasites

Babesia, also called Nuttallia, is an apicomplexan parasite that infects red blood cells and is transmitted by ticks. Originally discovered by the Romanian bacteriologist Victor Babeș, over 100 species of Babesia have since been identified.

Anaplasmosis

Anaplasmosis is a disease caused by a rickettsial parasite of ruminants, Anaplasma spp and is therefore related to rickettsial disease. The microorganisms are Gram-negative, and infect red blood cells. They are transmitted by natural means through a number of haematophagous species of ticks. The Ixodes tick that commonly transmits Lyme disease also spreads anaplasmosis.

<i>Theileria</i>

Theileria is a genus of parasites that belongs to the phylum Apicomplexa, and is closely related to Plasmodium. Two Theileria species, T. annulata and T. parva, are important cattle parasites. T. annulata causes tropical theileriosis and T. parva causes East Coast fever. Theileria species are transmitted by ticks. The genomes of T. orientalis Shintoku, Theileria equi WA, Theileria annulata Ankara and Theileria parva Muguga have been sequenced and published.

<i>Babesia microti</i> Species of parasitic protist in the Apicomplexa phylum

Babesia microti is a parasitic blood-borne piroplasm transmitted by deer ticks. B. microti is responsible for the disease babesiosis, a malaria-like disease which also causes fever and hemolysis.

Heartwater is a tick-borne rickettsial disease of domestic and wild ruminants. It is caused by Ehrlichia ruminantium - an intracellular Gram-negative coccal bacterium. The disease is spread by bont ticks, which are members of the genus Amblyomma. Affected mammals include cattle, sheep, goats, antelope, and buffalo, but the disease has the biggest economic impact on cattle production in affected areas. The disease's name is derived from the fact that fluid can collect around the heart or in the lungs of infected animals.

<i>Rhipicephalus sanguineus</i> Species of species of tick found worldwide

Rhipicephalus sanguineus, commonly called the brown dog tick, kennel tick, or pantropical dog tick, is a species of tick found worldwide, but more commonly in warmer climates. This species is unusual among ticks in that its entire lifecycle can be completed indoors. The brown dog tick is easily recognized by its reddish-brown color, elongated body shape, and hexagonal basis capituli. Adults are 2.28 to 3.18 mm in length and 1.11 to 1.68 mm in width. They do not have ornamentation on their backs.

<i>Ixodes pacificus</i> Species of arachnid

Ixodes pacificus, the western black-legged tick, is a species of parasitic tick found on the western coast of North America. I. pacificus is a member of the Ixodidae (hard-bodied) family. It is the principal vector of Lyme disease in that region. I. pacificus typically feeds on lizards and small mammals therefore its rate of transmission of Lyme disease to humans is around 1% of adults. It is an ectoparasite that attaches itself to the outside of its host and feeds on the hosts blood meal. It can have a heteroxenous lifestyle or monoxenous life cycle depending on how many hosts it feeds on in each cycle. I. pacificus has a four stage life cycle that takes around 3 years to complete. These stages include egg, larva, nymph, and adult. They prefer dense woodland habitats or areas of brush and tall grass.

<i>Rhipicephalus microplus</i>

The Asian blue tick is an economically important tick that parasitises a variety of livestock species especially cattle, on which it is the most economically significant ectoparasite in the world. It is known as the Australian cattle tick, southern cattle tick, Cuban tick, Madagascar blue tick, and Porto Rican Texas fever tick.

<i>Babesia bovis</i>

Babesia bovis is a single-celled parasite of cattle which occasionally infects humans. It is a member of the phylum Apicomplexa, which also includes the malaria parasite. The disease it and other members of the genus Babesia cause is a hemolytic anemia known as babesiosis and colloquially called Texas cattle fever, redwater or piroplasmosis. It is transmitted by bites from infected larval ticks of the order Ixodida. It was eradicated from the United States by 1943, but is still present in Mexico and much of the world's tropics. The chief vector of Babesia species is the southern cattle fever tick Rhipicephalus microplus.

<i>Theileria parva</i>

Theileria parva is a species of parasites, named in honour of Arnold Theiler, that causes East Coast fever (theileriosis) in cattle, a costly disease in Africa. The main vector for T. parva is the tick Rhipicephalus appendiculatus. Theiler found that East Coast fever was not the same as redwater, but caused by a different protozoan.

Anaplasma bovis is gram negative, obligate intracellular organism, which can be found in wild and domestic ruminants, and potentially a wide variety of other species. It is one of the last species of the Family Anaplasmaceae to be formally described. It preferentially infects host monocytes, and is often diagnosed via blood smears, PCR, and ELISA. A. bovis is not currently considered zoonotic, and does not frequently cause serious clinical disease in its host. This organism is transmitted by tick vectors, so tick bite prevention is the mainstay of A. bovis control, although clinical infections can be treated with tetracyclines. This organism has a global distribution, with infections noted in many areas, including Korea, Japan, Europe, Brazil, Africa, and North America.

Mites of domestic animals

Mites that infest and parasitize domestic animals cause disease and loss of production. Mites are small invertebrates, most of which are free living but some are parasitic. Mites are similar to ticks and both comprise the order Acari in the phylum Arthropoda. Mites are highly varied and their classification is complex; a simple grouping is used in this introductory article. Vernacular terms to describe diseases caused by mites include scab, mange, and scabies. Mites and ticks have substantially different biology from, and are classed separately from, insects. Mites of domestic animals cause important types of skin disease, and some mites infest other organs. Diagnosis of mite infestations can be difficult because of the small size of most mites, but understanding how mites are adapted to feed within the structure of the skin is useful.

Mites of livestock

Mites are small crawling animals related to ticks and spiders. Most mites are free-living and harmless. Other mites are parasitic, and those that infest livestock animals cause many diseases that are widespread, reduce production and profit for farmers, and are expensive to control.

Haemaphysalis bispinosa is a hard-bodied tick of the genus Haemaphysalis. It is found in India, Sri Lanka, Myanmar, Pakistan, Nepal, Australia, and Indonesia. It is an obligate ectoparasite of mammals. It is a potential vector of Kyasanur Forest disease virus. These ticks was found parasitized by a chalcid Hunterellus sagarensis in these diseased areas.

<i>Rhipicephalus annulatus</i>

The Cattle tick,, is a hard-bodied tick of the genus Rhipicephalus. It is also known as North American cattle tick, North American Texas fever tick, and Texas fever tick.

<i>Rhipicephalus pulchellus</i>

The zebra tick or yellow back tick is a species of hard tick. It is common in the Horn of Africa, with a habitat of the Rift Valley and eastward. It feeds upon a wide variety of species, including livestock, wild mammals, and humans, and can be a vector for various pathogens. The adult male has a distinctive black and ivory ornamentation on its scutum.

References

  1. 1 2 Walker, Mark David (2 November 2017). "Ticks on dogs and cats". The Veterinary Nurse. 8 (9): 486–492. doi:10.12968/vetn.2017.8.9.486.
  2. 1 2 Sonenshine, D.E. (1993), Biology of ticks (vol 1). Oxford University Press, New York. ISBN   0-19-505910-7
  3. Guglielmone, Alberto A.; Robbins, Richard G.; Apanaskevich, Dmitry A.; Petney, Trevor N.; Estrada-Peña, Agustín; Horak, Ivan G.; Shao, Renfu; Barker, Stephen C. (6 July 2010). "The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida) of the world: a list of valid species names" (PDF). Zootaxa. 2528 (1): 1–28. doi:10.11646/zootaxa.2528.1.1.
  4. Beati, Lorenza; Keirans, James E. (February 2001). "Analysis of the systematic relationships among ticks of the genera Rhipicephalus and Boophilus (Acari: Ixodidae) based on mitochondrial 12s ribosomal DNA gene sequences and morphological characters". Journal of Parasitology. 87 (1): 32–48. doi:10.1645/0022-3395(2001)087[0032:AOTSRA]2.0.CO;2. PMID   11227901.
  5. Barker, S. C.; Murrell, A. (October 2004). "Systematics and evolution of ticks with a list of valid genus and species names" (PDF). Parasitology. 129 (S1): S15–S36. doi:10.1017/s0031182004005207. PMID   15938503.
  6. Taylor, M.A. (2007). Veterinary parasitology. Oxford: Blackwell Publishing. ISBN   978-1-4051-1964-1.
  7. Geevarghese, G; Dhanda, V (1987). The Indian Hyalomma ticks (Ixodoidea: Ixodidae). Publications and Information Division, India Council of Agricultural Research. OCLC   19554336.[ page needed ]
  8. Jonsson, N.N. (April 2006). "The productivity effects of cattle tick (Boophilus microplus) infestation on cattle, with particular reference to Bos indicus cattle and their crosses". Veterinary Parasitology. 137 (1–2): 1–10. doi:10.1016/j.vetpar.2006.01.010. PMID   16472920.
  9. Pegram, R. G.; James, A. D.; Oosterwijk, G. P. M.; Killorn, K. J.; Lemche, J.; Ghirotti, M.; Tekle, Z.; Chizyuka, H. G. B.; Mwase, E. T.; Chizhuka, F. (September 1991). "Studies on the economics of ticks in Zambia". Experimental & Applied Acarology. 12 (1–2): 9–26. doi:10.1007/BF01204396. PMID   1748032. S2CID   24594154.
  10. Stachurski, F. (December 2000). "Invasion of West African cattle by the tick Amblyomma variegatum". Medical and Veterinary Entomology. 14 (4): 391–399. doi:10.1046/j.1365-2915.2000.00246.x. PMID   11129703. S2CID   12470638.
  11. 1 2 Lancaster, J.L. (1986). Arthropods in livestock and poultry production. Chichester: Ellis Horwood Ltd. ISBN   978-0-85312-790-1.[ page needed ]
  12. Gothe, Rainer; Kunze, Klaus; Hoogstraal, Harry (23 November 1979). "The Mechanisms of Pathogenicity in the Tick Paralyses". Journal of Medical Entomology. 16 (5): 357–369. doi:10.1093/jmedent/16.5.357. PMID   232161.
  13. Stone, Bernard F.; Binnington, Keith C.; Gauci, Maryann; Aylward, James H. (June 1989). "Tick/host interactions forIxodes holocyclus: Role, effects, biosynthesis and nature of its toxic and allergenic oral secretions". Experimental & Applied Acarology. 7 (1): 59–69. doi:10.1007/BF01200453. PMID   2667920. S2CID   23861588.
  14. Barker, Stephen C.; Walker, Alan R. (18 June 2014). "Ticks of Australia. The species that infest domestic animals and humans". Zootaxa. 3816 (1): 1–144. doi:10.11646/zootaxa.3816.1.1. PMID   24943801.
  15. Bock, R.; Jackson, L.; De Vos, A.; Jorgensen, W. (October 2004). "Babesiosis of cattle". Parasitology. 129 (S1): S247–S269. doi:10.1017/s0031182004005190. PMID   15938514.
  16. Martinez, Dominique; Aumont, Gilles; Moutoussamy, M.; Gabriel, D.; Tatareau, A. H.; Barré, Nicolas; Vallée, F.; Mari, Bernard (1993). "Epidemiological studies on dermatophilosis in the Caribbean". Revue d'Elevage et de Médecine Vétérinaire des Pays Tropicaux. 46 (1–2): 323–7. PMID   8161379.
  17. Coetzer, J.A.W. (1994). Infectious diseases of livestock with special reference to southern Africa. Cape Town: Oxford University Press. ISBN   978-0-19-570506-5.[ page needed ]
  18. Gould, EA; Solomon, T (February 2008). "Pathogenic flaviviruses". The Lancet. 371 (9611): 500–509. doi:10.1016/S0140-6736(08)60238-X. PMID   18262042. S2CID   205949828.
  19. Hoogstraal, H (June 1979). "Ticks and spirochetes". Acta Tropica. 36 (2): 133–136. doi:10.5169/seals-312515. PMID   41420.
  20. Uilenberg, G.; Barre, N.; Camus, E.; Burridge, M.J.; Garris, G.I. (March 1984). "Heartwater in the Caribbean". Preventive Veterinary Medicine. 2 (1–4): 255–267. doi:10.1016/0167-5877(84)90068-0.
  21. Norval, R.A.I. (1992). The epidemiology of theileriosis in Africa. London: Academic Press. ISBN   978-0-12-521740-8.[ page needed ]
  22. Katzer, F.; Ngugi, D.; Walker, A.R.; McKeever, D.J. (February 2010). "Genotypic diversity, a survival strategy for the apicomplexan parasite Theileria parva". Veterinary Parasitology. 167 (2–4): 236–243. doi:10.1016/j.vetpar.2009.09.025. PMC   2817781 . PMID   19837514.
  23. George, J. E.; Pound, J. M.; Davey, R. B. (October 2004). "Chemical control of ticks on cattle and the resistance of these parasites to acaricides". Parasitology. 129 (S1): S353–S366. doi:10.1017/s0031182003004682. PMID   15938518. S2CID   11953803.
  24. Okello-Onen, J; Mukhebi, A.W; Tukahirwa, E.M; Musisi, G; Bode, E; Heinonen, R; Perry, B.D; Opuda-Asibo, J (January 1998). "Financial analysis of dipping strategies for indigenous cattle under ranch conditions in Uganda". Preventive Veterinary Medicine. 33 (1–4): 241–250. doi:10.1016/s0167-5877(97)00035-4. PMID   9500178.
  25. George, J. E.; Pound, J. M.; Davey, R. B. (2008). "Acaricides for controlling ticks on cattle and the problem of acaricide resistance". In Bowman, Alan S; Nuttall, Patricia A (eds.). Ticks. pp. 408–423. doi:10.1017/CBO9780511551802.019. ISBN   978-0-511-55180-2.
  26. Willadsen, Peter (May 2006). "Tick control: Thoughts on a research agenda". Veterinary Parasitology. 138 (1–2): 161–168. doi:10.1016/j.vetpar.2006.01.050. PMID   16497440.
  27. Mount, G. A.; Haile, D. G.; Davey, R. B.; Cooksey, L. M. (1 March 1991). "Computer Simulation of Boophilus Cattle Tick (Acari: Ixodidae) Population Dynamics". Journal of Medical Entomology. 28 (2): 223–240. doi:10.1093/jmedent/28.2.223. PMID   2056504.
  28. Randolph, S. E.; Rogers, D. J. (September 1997). "A generic population model for the African tick Rhipicephalus appendiculatus". Parasitology. 115 (3): 265–279. doi:10.1017/s0031182097001315. PMID   9300464. S2CID   7624515.
  29. Schmidtmann, Edward T. (1994). "Ecologically based strategies for controlling ticks". In Sonenshine, Daniel E.; Mather, Thomas N. (eds.). Ecological Dynamics of Tick-borne Zoonoses. Oxford University Press. pp. 240–280. ISBN   978-0-19-507313-3.
  30. Handule, Ismail Mohamed; Ketavan, Chitapa; Gebre, Solomon (31 March 2002). "Toxic Effect of Ethiopian Neem Oil on Larvae of Cattle Tick, Rhipicephalus pulchellus Gerstaeker". Agriculture and Natural Resources. 36 (1): 18–22.
  31. Walker, Alan R. (July 2011). "Eradication and control of livestock ticks: biological, economic and social perspectives". Parasitology. 138 (8): 945–959. doi:10.1017/S0031182011000709. PMID   21733257. S2CID   206246539.
  32. Strom, C. (2009). Making catfish bait out of government boys: the fight against cattle ticks and transformation of the yeoman south. The University of Georgia Press, Athens, GA, USA and London UK. ISBN   978-0-8203-2749-5.[ page needed ]
  33. Angus, Beverley M. (December 1996). "The history of the cattle tick Boophilus microptus in Australia and achievements in its control". International Journal for Parasitology. 26 (12): 1341–1355. doi:10.1016/s0020-7519(96)00112-9. PMID   9024884.
  34. Pegram, R. 2010. Thirteen years of hell in paradise: an account of the Caribbean Amblyomma program. Trafford Publishing, Bloomington, Indiana, USA. ISBN   978-1-4269-4453-6.[ page needed ]
  35. Hewetson, R. W. (May 1972). "The inheritance of resistance by cattle to cattle tick". Australian Veterinary Journal. 48 (5): 299–303. doi:10.1111/j.1751-0813.1972.tb05161.x. PMID   5068812.
  36. Shaw, D. J.; Grenfell, B. T.; Dobson, A. P. (December 1998). "Patterns of macroparasite aggregation in wildlife host populations". Parasitology. 117 (6): 597–610. doi:10.1017/s0031182098003448. PMID   9881385.
  37. Harley, K.L.S.; Wilkinson, P.R. (1971). "A modification of pasture spelling to reduce acaricide treatments for cattle tick control". Australian Veterinary Journal. 47 (3): 108–111. doi:10.1111/j.1751-0813.1971.tb14750.x. PMID   5103591.
  38. Elder, J.K. (1980). "A survey concerning cattle tick control in Queensland, 4. Use of resistant cattle and pasture spelling". Australian Veterinary Journal. 56 (5): 219–223. doi:10.1111/j.1751-0813.1980.tb15976.x. PMID   7436925.
  39. Hoogstraal, Harry (1985). "Argasid and Nuttalliellid Ticks as Parasites and Vectors". Advances in Parasitology Volume 24. Advances in Parasitology. 24. pp. 135–238. doi:10.1016/S0065-308X(08)60563-1. ISBN   978-0-12-031724-0. PMID   3904345.
  40. Bowman, A. S.; Ball, A.; Sauer, J. R. (2008). "Tick salivary glands: The physiology of tick water balance and their role in pathogen trafficking and transmission". In Bowman, Alan S; Nuttall, Patricia A (eds.). Ticks. pp. 73–91. doi:10.1017/CBO9780511551802.004. ISBN   978-0-511-55180-2.
  41. Horak, Ivan G.; Gallivan, Gordon J.; Spickett, Arthur M. (24 February 2011). "The dynamics of questing ticks collected for 164 consecutive months off the vegetation of two landscape zones in the Kruger National Park (1988–2002). Part I. Total ticks, Amblyomma hebraeum and Rhipicephalus decoloratus". Onderstepoort Journal of Veterinary Research. 78 (1): 32. doi: 10.4102/ojvr.v78i1.32 . PMID   23327204.
  42. Randolph, S. E. (May 1994). "Density-dependent acquired resistance to ticks in natural hosts, independent of concurrent infection with Babesia microti". Parasitology. 108 (4): 413–419. doi:10.1017/s003118200007596x. PMID   8008455.
  43. 1 2 Randolph, S. E. (2008). "The impact of tick ecology on pathogen transmission dynamics". In Bowman, Alan S; Nuttall, Patricia A (eds.). Ticks. pp. 40–72. doi:10.1017/CBO9780511551802.003. ISBN   978-0-511-55180-2.
  44. Utech, KBW; Wharton, RH; Kerr, JD (1978). "Resistance to Boophilus microplus (Canestrini) in different breeds of cattle". Australian Journal of Agricultural Research. 29 (4): 885. doi:10.1071/ar9780885.
  45. Chiera, J. W.; Newson, R. M.; Cunningham, M. P. (April 1985). "Cumulative effects of host resistance on Rhipicephalus appendiculatus Neumann (Acarina: Ixodidae) in the laboratory". Parasitology. 90 (2): 401–409. doi:10.1017/s003118200005109x.
  46. Latif, AA; Hove, T; Kanhai, GK; Masaka, S (September 2001). "Laboratory and field investigations into the Theileria parva carrier-state in cattle in Zimbabwe". The Onderstepoort Journal of Veterinary Research. 68 (3): 203–208. hdl:2263/18951. PMID   11769352. S2CID   20471003.
  47. Bock, R.; Jackson, L.; De Vos, A.; Jorgensen, W. (October 2004). "Babesiosis of cattle". Parasitology. 129 (S1): S247–S269. doi:10.1017/s0031182004005190. PMID   15938514. ProQuest   750568336.
  48. Hay, Simon I. (July 2001). "The paradox of endemic stability". Trends in Parasitology. 17 (7): 310. doi:10.1016/s1471-4922(01)02008-6. PMC   3173862 . PMID   11423357.
  49. Jonsson, Nicholas N.; Bock, Russell E.; Jorgensen, Wayne K.; Morton, John M.; Stear, Michael J. (March 2012). "Is endemic stability of tick-borne disease in cattle a useful concept?". Trends in Parasitology. 28 (3): 85–89. doi:10.1016/j.pt.2011.12.002. PMID   22277132.
  50. Rubaire-Akiiki, Christopher M.; Okello-Onen, Joseph; Musunga, David; Kabagambe, Edmond K.; Vaarst, Mettee; Okello, David; Opolot, Charles; Bisagaya, A.; Okori, C.; Bisagati, C.; Ongyera, S.; Mwayi, M.T. (August 2006). "Effect of agro-ecological zone and grazing system on incidence of East Coast Fever in calves in Mbale and Sironko Districts of Eastern Uganda". Preventive Veterinary Medicine. 75 (3–4): 251–266. doi:10.1016/j.prevetmed.2006.04.015. PMID   16797092.
  51. Todorovic, RA; Vizcaino, OG; Gonzalez, EF; Adams, LG (September 1973). "Chemoprophylaxis (Imidocarb) against Babesia bigemina and Babesia argentina infections". American Journal of Veterinary Research. 34 (9): 1153–61. PMID   4747036.
  52. Singh, D.K.; Thakur, M.; Raghav, P.R.S.; Varshney, B.C. (January 1993). "Chemotherapeutic trials with four drugs in crossbred calves experimentally infected with Theileria annulata". Research in Veterinary Science. 54 (1): 68–71. doi:10.1016/0034-5288(93)90013-6. PMID   8434151.
  53. Dalgliesh, R. J.; Jorgensen, W. K.; de Vos, A. J. (March 1990). "Australian frozen vaccines for the control of babesiosis and anaplasmosis in cattle—A review". Tropical Animal Health and Production. 22 (1): 44–52. doi:10.1007/BF02243499. PMID   2181745. S2CID   25721150.
  54. de Vos, A.J. (1 December 1979). "Epidemiology and control of bovine babesiosis in South Africa". Journal of the South African Veterinary Association. 50 (4): 357–362. hdl:10520/AJA00382809_3606. PMID   576018.
  55. Timms, P.; Dalgliesh, R. J.; Barry, D. N.; Dimmock, C. K.; Rodwell, B. J. (March 1983). "Babesia bovis: comparison of culture-derived parasites, non-living antigen and conventional vaccine in the protection of cattle against heterologous challenge". Australian Veterinary Journal. 60 (3): 75–77. doi:10.1111/j.1751-0813.1983.tb05874.x. PMID   6347164.
  56. Pipano, E. (March 1995). "Live vaccine against hemoparasitic disease in livestock". Veterinary Parasitology. 57 (1–3): 213–231. doi:10.1016/0304-4017(94)03122-d. PMID   7597786.
  57. Hashemi-Fesharki, R. (February 1988). "Control of Theileria annulata in Iran". Parasitology Today. 4 (2): 36–40. doi:10.1016/0169-4758(88)90062-2. PMID   15463034.
  58. Di Giulio, Giuseppe; Lynen, Godelieve; Morzaria, Subhash; Oura, Chris; Bishop, Richard (February 2009). "Live immunization against East Coast fever – current status". Trends in Parasitology. 25 (2): 85–92. doi:10.1016/j.pt.2008.11.007. PMID   19135416.
  59. McKeever, D.J; Taracha, E.L.N; Morrison, W.I; Musoke, A.J; Morzaria, S.P (July 1999). "Protective Immune Mechanisms against Theileria parva: Evolution of Vaccine Development Strategies". Parasitology Today. 15 (7): 263–267. doi:10.1016/s0169-4758(99)01465-9. PMID   10377527.
  60. Musoke, A.; Morzaria, S.; Nkonge, C.; Jones, E.; Nene, V. (15 January 1992). "A recombinant sporozoite surface antigen of Theileria parva induces protection in cattle". Proceedings of the National Academy of Sciences. 89 (2): 514–518. Bibcode:1992PNAS...89..514M. doi:10.1073/pnas.89.2.514. PMC   48269 . PMID   1731322.
  61. Willadsen, Peter; Smith, Don; Cobon, Gary; McKENNA, Robert V. (May 1996). "Comparative vaccination of cattle against Boophilus microplus with recombinant antigen Bm86 alone or in combination with recombinant Bm91". Parasite Immunology. 18 (5): 241–246. doi:10.1046/j.1365-3024.1996.d01-90.x. PMID   9229376. S2CID   8405011.
  62. Willadsen, P. (2008). "Anti-tick vaccines". In Bowman, Alan S; Nuttall, Patricia A (eds.). Ticks. pp. 424–446. doi:10.1017/CBO9780511551802.020. ISBN   9780511551802.
  63. Delafuente, J; Rodríguez, M; Redondo, M; Montero, C; García-García, JC; Méndez, L; Serrano, E; Valdés, M; Enriquez, A; Canales, M; Ramos, E; Boué, O; Machado, H; Lleonart, R; de Armas, CA; Rey, S; Rodríguez, JL; Artiles, M; García, L (February 1998). "Field studies and cost-effectiveness analysis of vaccination with Gavac? against the cattle tick Boophilus microplus". Vaccine. 16 (4): 366–373. doi:10.1016/s0264-410x(97)00208-9. PMID   9607057.

Further reading