Ixodida Metastigmata

Ticks are obligate hematophagous parasites of mammals, birds, reptiles, and amphibians. Their distinctmorphology and large size distinguish them from other Acari. They are among the largest of the Acari, with a range of 2 mm to 3 cm. In ticks the cephalothorax and abdomen are fused into an oval body, which is flattened dorsoventrally; the epistome is absent and the mouthparts are formed into a denticulate hypostome. This toothed organ anchors the tick to its host. The stigmata or spiracles are located posterior to coxae 4 in hard ticks (Ixodidae), or anterior in soft ticks (Argasidae). Hard ticks have a sclerotized dorsal plate (scutum), and their mouthparts project anteriorly; soft ticks lack a dorsal plate and their mouthparts are located ventrally.

Ixodidae typically have a three-host life cycle. Eggs are laid on the ground; after hatching the larva (seed tick) feeds upon the first host, then drops off and molts to the nymph stage. The nymph feeds on a second host, and drops off to molt; the adult feeds and mates on a third host, and drops off to lay eggs. Each stage remains on the hostfor 1-3 days and takes one blood meal, but leaves to molt. The feeding habits of these ticks make them disease vectors to domestic animals and humans in the agricultural and urban environment. Argasidae typically have multiple hosts during their life cycle. Adults and immatures remain in harborages during the day and emerge at night to find and feed on a host. Each stage of development may take several blood meals. The larva stage of the soft tick, Ornithodoros moubata, emerges from the egg with food in its gut and does not feed. The larval mouthparts in this species are only used to escape from the egg.

Tick-borne diseases include Rocky Mountain spotted fever, Colorado tick fever, Lyme disease, and relapsing fever. Certain ticks, especially engorging females feeding on the neck or near the base of the skull, inject venom that produces a paralysis. Several species of ticks occur in peridomestic habitats and utilize domestic and feral mammals and birds as hosts. Urban and suburban expansion has resulted in increased human exposure to two diseases transmitted by ticks: Rocky Mountain spotted fever and Lyme disease. Rocky Mountain spotted fever, also known as Tobia fever and Sao Paulo fever, is widely distributed in the Nearctic and Neotropical regions. In spite of its name, this disease is most prevalent in eastern USA. Urban and suburban expansion into shrubby fields and woodlands, with a resident small- and large-animal population and various species of ticks, has increased human exposure to tick vectors of the disease. Transstadial and transovarial passage of the rickettsiae in the ticks maintains this disease in the vector population. Relapsing fever is caused by species of Borrelia and is transmitted by several species of Ornithodoros ticks, which occur in huts, outbuildings, seasonal houses, and sometimes in caves. The disease is endemic across many regions of the world, and Ornithodoros ticks serve as the disease reservoir.

Ticks are often associated with domestic dogs in the urban and rural environment. In Japan, Haemaphysalis longicornis is the species most frequently found on dogs, followed by H.flava, Rhipicephalus sanguineus, and Ixodes ovatus. Small numbers of

H. hystriris, H. campanulata, H. japonica, H. ias, I. persulcatus,

I. nipponensis, and Amblyomma testudinarium also occur. Dogs in rural areas of Japan frequently carry H. longicornis, H.flava, and I. ovatus, while R. sanguineus is more associated with the dogs in urban/suburban areas. Exposure of a domestic dog to a garden is associated with infestations of R. sanguineus, and exposure to woodland is associated with infestations of H. flava and I. ovatus.

Lyme disease, which is caused by the spirochete Borrelia burgdorferi, is perhaps the most important tick-borne disease in North America, where several hundred cases are reported every year. It is now known from the British Isles, Europe and parts of Russia, northeastern China, Japan, South Africa, and perhaps Australia. The vectors include Ixodes species, which feed as immatures on a variety of small animals. Mouse and vole populations in urban environments maintain and spread this disease. Transmission of Lyme disease is by tick bite, and attachment and feeding for 1-3 days are necessary to transmit

Figure 18.5 Arthropoda: Ixodida. (a) Amblyomma americanum female; (b) Dermacentor variabilis female; (c) Rhipicephalus sanguineus male; (d) Ornithodoros moubata female.

the Borrelia pathogen. Transovarial transmission occurs at low rates in Ixodes ticks.

Boutonneuse fever produces button-like lesions on the skin at the tick attachment site. This rickettsial disease occurs in Africa, European and North African areas adjacent to the Mediterranean, the Middle East, and in Southeast Asia. Locally itis called Marseilles fever, South African or Kenya tick typhus, and Indian tick typhus. The primary tick vectors are Amblyomma hebraeum in the South African veldt, and the dog tick, Rhipicephalus sanguineus, in most other regions. Urban cases of this disease are associated with domestic dogs and the dog tick. Transmission may be directly through tick bite or by contact with skin and eyes after removing ticks from dogs. Transovar-ial passage of rickettsiae maintains the disease in the vector population.

Lone star tick, Amblyomma americanum (Fig. 18.5a) Adult males are about 5 mm long (including the long mouthparts), uniformly light brown to brown and with white markings at the margin of the dorsal plate. Females are about 10 mm long when engorged, and have a white spot at the posterior end of the dorsal plate. Females lay a mass of more than 5000 eggs, and hatching occurs in about 30 days. Larvae attach to host animals from the tops of grass stems and other vegetation. Nymphs and adults crawl to host animals in the immediate area. Overwintering is as a fed larva, as an unfed nymph, or as an unfed adult. Some fed nymphs develop to adults during winter. This species has a variety of hosts, including wild and domestic animals, birds, and humans. It attacks humans in the larval, nymph, and adult stage. The lone star tick is a vector of Rocky Mountain spotted fever and tularemia. This species is distributed in Mexico and southern USA, particularly Oklahoma, Missouri, Arkansas, Texas, and Louisiana.

Other Amblyomma Species in this genus have white markings; the mouthparts are long and inflict painful bites on humans and deep wounds on animals. A. hebraeum, South African bonttick, occurs from South Africa northwards to Zimbabwe and Mozambique. Adult males have two spots medially on the dorsal plate, festoons pale; the female dorsal plate is pale white with brown markings. The immatures feed on small and large mammals while the adults feed on large animals. In the South African veldt larvae and nymphs actively crawl towards and feed on humans. The Cayenne tick, A. cajen-nense, is distributed from South America and the Caribbean to southern Texas. Adult males and females have extensive white markings on the dorsal plate. It is a vector of Rocky Mountain spotted fever in Central America, Columbia, and Brazil; immatures readily feed on humans and produce intense itching and lesions.

Pigeon tick, Argas reflexus Adult females are about 8.5 mm long and 5 mm wide, but taper anteriorly; males are about 6.5 mm long and 4.5 mm wide. The margin of the body is composed ofirregular striations. Palp segments are subequal, and segment 3 is the shortest. The capitulum has two long setae ventrally and directed forward. This species is associated with pigeons, although other avian and mammalian hosts, including humans, are known. This species is commonindoors and attacks people in Israel. It is abundant in the Middle East, Europe, southwestern Russia, and Asia. A closely related species in the A. reflexus group, A. latus, occurs inlarge numbers indoors, and is associated with pigeons.

American dog tick, Dermacentor variabilis (Fig. 18.5b) Adult males are about 4.5 mm long and 2.5 mm wide. The dorsal plate is dark brown, covers the abdomen, and is marked with a variable pattern of white marks. Engorged females are about 13 mm long and about 10 mm wide, and the dorsal plate is small. Females lay a mass of 4000-6500 yellowish-brown eggs on the ground; hatching occurs in 36-57 days, depending on temperature and humidity. Larvae feed almost exclusively on small rodents such as mice and voles; engorgement takes 3-12 days. Nymphs usually feed on mice or voles and become engorged in 3-11 days; molting takes 3 weeks to 1-3 months. Adults usually attack dogs and other large animals, including humans; females engorge in 6-13 days. Mating takes place on the host. Unfed adults live for about 2 years. This species is distributed east of the Rocky Mountains and in California, Mexico, and Canada. It is particularly abundant along the east coast of the USA. It is a vector of Rocky Mountain spotted fever in eastern USA, where infested domestic and feral dogs bring infected ticks to peridomestic habitats.

Other Dermacentor Ticks of this genus are widely distributed; they occur in North and South America, Europe, Eurasia, and Asia. D. andersoni, the RockyMountain wood tick, is distributed in western North America. It occurs in shrubby or open areas, and the primary hosts are large animals. D. albipictus is widely distributed in North America and hosts include horse, moose, elk, and deer. Eurasian species include D. marginatus, D. silvarum, and D. nuttalli. Lowland forests and shrubby areas from Kazakhstan to central Europe are the habitats for D. marginatus; D. silvarum ranges from Kazakhstan to western Siberia, and D. nuttalli ranges from central Siberia to Mongolia, and China south to Tibet. D. reticulatus has been introduced into southern UK.

Rabbit tick, Haemaphysalis leporipalustris Females are 11.3 mm long and 7.5 mm wide when engorged. The body is narrow anteriorly and broad posteriorly, and coarsely punctate. Hosts are rabbits, birds, and occasionally domestic mammals such as dogs and cats. It rarely feeds on humans but it is sometimes found in houses, and is important in the spread of Rocky Mountain spotted fever. This tick occurs in Central and South America, continental USA, and Canada.

Other Haemaphysalis Members of this genus are usually small and the sexes are similar; they parasitize wild and domestic animals and are distributed worldwide. H. parva (=H. otophila) occurs on dogs in Jerusalem, Israel. H. leachii, the yellow dog tick, is common in Asia and Africa and is a vector of malignant jaundice in dogs. In South Africa, urban cases ofboutonneuse fever caused by Rickettsia conori are associated with contamination of skin or eyes with infected ticks crushed while being removed by hand. H. spinigera is a vector of the arbovirus causing Kyasanur forest disease in monkey and humans in India. The immatures feed primarily on small forestrodents and monkeys. Humans are bitten during the dry pre-monsoon season when villagers enter the forest to gather firewood.

English dog tick, hedgehog tick, Ixodes hexagonus Males are 3.5-3.8 mm long; females are 3.5-4.0 mm long, and fed females are 13 mm long. Oviposition takes place at3-30 ° C, and about 1% of the eggs may develop parthenogenetically. Development from egg to adult in the laboratory at 22-23 °C takes about 60 days; under natural conditions development may last 2 years. This tick is a parasite of carnivores, such as foxes, dogs and cat, and the hedgehog (Erinaceus europaeus) in the urban environment. It is common in suburban locations in central Europe. As an endophilic tick, it spends most of its time inside the burrows or nests ofits hosts, and does not occur in buildings. It is a vector of tick-borne encephalitis (TBE) virus and Borrelia burgdorferi; the hedgehog is a reservoir host for both these diseases. This species is widely distributed in Europe, North Africa, and southern Asia.

Australian paralysis tick, Ixodes holocyclus Males are 1.92.7 mm long and 1.6-2.0 wide. The body is yellowish brown, the dorsal plate is glossy and with numerous fine punctuations. Unfed females from Queensland and New South Wales are 2.6-3.8 mm long; those from Victoria are 4.3-4.6 mm long. Engorged females are 12 mm long and grayish green or greenish black. The female dorsal plate is small and covers about one-third of the abdomen; the male has a large plate that covers the abdomen. Females lay a mass of about 3000 eggs in damp locations on the ground; hatching occurs in 40-60 days. Larvae are about 1 mm long and feed on small, native mammals such as a bandicoot (Parameles spp.), kangaroo, or opossum; larvae feed for 4-6 days. Nymphs are about2 mm long and feed on a variety of animals. They remain on the ground in moist vegetation for 14-40 days before finding a host; they feed for 4-7 days. Adultfemale ticks engorge for 6-20 days; males mate with females on the host but do not feed. This species is mainly distributed along the eastern coast ofAustralia, from Queensland to Victoria. It is also abundant on the central coastal plain, from Kempsey to Wollongong.

Symptoms of paralysis caused by I. holocyclus appear 3-7 days after the tick has attached and begun to feed. In humans the symptoms include severe headache, blurred vision, weakness in limbs, and increasing paralysis; after about4days, breathing becomes difficult. In domestic animals, the symptoms include loss of appetite, discharge from the eyes, difficulty walking, especially in the hind legs, vomiting, and dilated pupils. I. holocyclus is a vector of Queensland tick typhus, Rickettsia australis.

European sheep tick, Ixodes ricinus Adults are about 11 mm long. They are regularly oval, pale and reddish brown, with short, white hairs. It attacks a variety of vertebrate hosts. The free-living stages only survive in microclimates where the RH is high (80%), which includes leaf litter in temperate forested areas. In the urban environment, it occurs in naturally forested parts, gardens, and cemeteries. It occurs in some urban areas in Czech Republic, Germany, Austria, and the UK. Hedgehogs and foxes are the primary hosts for this tick in urban areas in central Europe. It is the most common vector tick in Europe and transmits a large number ofhuman pathogenic organisms, including several genospecies of Borrelia burgdorferi. This tick is cosmopolitan, and occurs in North America, from Ireland and the UK to western and central Europe, Russia, and from Algeria and Morocco east to northern Iran.

Black-legged tick, deer tick, bear tick, Ixodes scapularis (= I. dammini) Females are about 3.5 mm long and males are about 2 mm long. The body is uniformly orange brown and it has a dark brown to black spot anterodorsally. The mouth-parts are long and the dorsal plate of the male nearly covers the abdomen. This species is polyphagous and attacks a variety of hosts, including at least 27 species of birds, several small and large mammals, and humans. Immature stages commonly feed on the white-footed mouse (Peromyscus leucopus), and this mouse is the primary reservoir for Lyme disease in northeastern USA. Lyme disease is transmitted from mouse to mouse and mouse to human by larvae and nymphs of I. scapularis. White-tailed deer (Odocoileus virginianus) is the primary overwintering site and the main hostfor the adult tick. Adult ticks do notmove from host to host and are not responsible for transmission of Lyme disease. The distribution range of this tick is expanding to urban and suburban areas, and this may be linked to the proliferation of deer in urban environments. It is distributed in northeastern USA and adjacent regions of Canada, and it is the primary vector of Lyme disease in this region. Ixodes dammini was at one time considered a distinct species and the main vector ofLyme disease in northeastern and northcentral USA.

Other Ixodes This genus is distributed worldwide, and several species occur in the urban and suburban environment along with their hosts. The Pacific coast black-legged tick, I. pacificus, is the primary vector of Lyme disease in western USA. The groundhog tick, I. cookei, is common in eastern USA, where it occurs from New England states south to Virginia. Nymphs and adults bite humans, and they occur in outbuildings or other structures frequented by rodents, such as groundhogs. I. persulcatus vectors Lyme disease in Russia. I. redikorzevi occurs in villages and small towns in Israel, and bites people.

Relapsing fever tick, ornithodoros hermsi Adult females are 5-6 mmlongand3-4mmwideandlight brown. The engorged female is about 11 mm long and reddish brown to grayish blue. The integument of adult male and female is strongly tuber-culated. Larvae survive 3 months and adults survive 7 months without food. Development from egg to adult is 202-314 days at 30 °C and 364-602 days at 21 °C. This species occurs in the mountains (1500 m) of California northward to British Columbia. It is a vector ofrelapsing fever in the mountainous area of California and in some other western states.

Eyeless tampan, ornithodoros moubata (Fig. I8.5d) Adults are about 8 mm long and 6-7 mm wide; engorged females are 11 mm long. The integument of nymphs and adults is densely tuberculated and without spines. Mouthparts are small, and eyes are lacking. Females lay more than 400 eggs in six or seven batches; hatching occurs in about 8 days at30 °C. Larvae emerge from the egg with food in their gut and probably do not feed. Nymphs feed four or five times. Adults feed six or seven times on differenthosts. After each meal females deposit eggs; the preoviposition period is 5-25 days. This soft tick is active at night and it occurs as two forms. O. moubata moubata is found indoors, and feeds on humans and chickens; O. moubata porcinus occurs outdoors in warthog (Phacohoerus spp.) burrows and generally does not attack humans. O. moubata moubata is common in rest-houses on travel routes, and can be carried in household materials, such as mats and bed-rolls. Both subspecies have wild and domestic populations, and the domestic populations are linked to disease transmission to humans. This species is widely distributed in East, Central, and southern Africa; it is a vector of relapsing fever.

Other ornithodoros This large genus is distributed in Africa, theMiddle East, North and Central America. O. coniceps occurs in Israel where ithas infested buildings and bitten people. O. talaje occurs in Central and South America and feeds on wild rodents, swine, cattle, and humans. It is a vector of relapsing fever. O. rudis occurs in Central and South America. It feeds primarily on humans, and regularly occurs indoors. The pajaroello,

O. coriaceus, is a large tick (engorged females are about 20 mm long) that normally feeds on deer and cattle, but delivers a painful bite to humans. It occurs in the coastal areas of California, Mexico, and South America.

Brown dog tick, kennel tick, Rhipicephalus sanguineus (Fig. 18.5c) Males are about 3 mm long, flattened, uniformly reddish brown, and the body surface is punctate. Engorged females are about 12 mm long and the body is grayish blue to light green. Females lay a mass of 1000-3000 eggs in cracks and crevices above ground. Hatching occurs in 19-60 days, but cool and dry weather prolongs hatching. Larvae are about2 mm wide (engorged) and light brown. They crawl on walls indoors, and attach themselves to domestic animals and people; they can survive about 8 months without food. Nymphs are about 3 mm diameter and dark gray. They feed for 4-9 days, and then drop off the host and molt to adults in 12-29 days. Adults attach to dogs or other animals, and engorge for 6-50 days; they live for 18 months before attachment and feeding. Development from egg to adult can be completed in about 63 days at 29 °C. This tick prefers warm and dry situations and seldom develops outdoors in continental USA. It is native to Africa, but it has successfully spread to much of the world. It survives in heated buildings in urban environments in countries between 50 °N and 35 °S. Populations of this tick have increased in urban areas in many parts of the world, along with increases in ownership of pet dogs and increases in feral dogs. R sanguineus can complete its life cycle on dogs; it is well adapted to urban environments. It requires high temperatures for development, and in temperate regions it is successful indoors. This tick is a vector of Rocky Mountain spotted fever in southern USA, and with boutonneuse fever in the Mediterranean region ofEurope.

Other Rhipicephalus Species of this genus occur in Eurasia and Africa, and from its homeland, R sanguineus has spread to other parts of the world. R turanicus occurs in shrub and tree habitats in some towns in Israel, along the coastal plain.

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