Suborder of Acarina
The monoecious ticks may reach up to 2 cm in length and are vectors of important pathogens (viruses, bacteria, rickettsiae, anaplasms, protozoa, and helminths; Table 2), since they feed on the blood of their hosts. Unlike vessel feeders (mosquitoes), tick mouth parts bring about more or less deep hollows in the host's skin, which become filled by blood of ruptured blood vessels (Fig. 1). Thus, the ticks are pool feeders engorging (in some species for minutes, in others for up to days) large amounts of blood (several times their body weights). During feeding salivary secretions prevent blood coagulation. In some species (e.g., Ixodes spp., Dermacentor spp.) these injected substances are toxic and cause paralysis (tick paralysis), which may lead to death in man and animals. In general, all stages of the tick's life cycle (larvae with six legs, nymphs and adults with eight legs) suck blood. The life cycle of ticks is characterized by periods of starvation which can be of long duration, and by relatively short periods involved with the uptake of enormous concentrated blood meals. The life cycle of an ixodid tick can often have a total duration of 6 years and host attachment may constitute less than 2% of this time. Starvation periods of more than 3 years are common, and starvation can be particularly extended in some argasid tick species which have been known to survive for up to about 14 years. This ability is very important and has to be considered when dealing with the acute transmission and epidemiology of certain pathogens.
The ticks are subdivided into three families, namely the Argasidae and the Ixodidae, to which most ticks belong, and the Nuttalliellidae, which is a monotypic family characterized by features mainly intermediate to those of the two major tick families. The two major families, the “soft” Argasidae and the “hard” Ixodidae, can be differentiated according to the following biological and behavioral criteria (Table 1).
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The more common genera of argasid ticks are Antricola (4 species), Argas (140 species), Otobius (2 species) and Ornithodoros (90 species). Ixodid ticks are further divided into two groups, the Prostriata and the Metastriata. Prostriata contains only the genus Ixodes which has about 250 species worldwide, while all other ixodid genera are classified as Metastriata. A distinctive difference between these two groups of ticks is the location of an anal groove anterior to the anus in Prostriata, and posterior to the anus in Metastriata. The more important metastriate genera are Amblyomma (100 species), Aponomma (26 species), Anocentor (monotypic), Boophilus (5 species), Dermacentor (31 species), Haemaphysalis (150 species), Hyalomma (21 species), Rhipicephalus (63 species) and Margaropus (3 species) (Table 2).
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Argas/Life Cycle, Ixodes Species/Life Cycle.
In ticks the sexes are separate but sexual dimorphism is less visible in the Argasidae than in the Ixodidae. In hard ticks, males and females have marked differences in the shape of the scutum, and females possess porose areas (with the exception of Ixodes kopsteini) which are not present in males. In the genus Ixodes, there is generally further dimorphism in the shape of the gnathosomal appendages. Superficially, soft tick males and females are distinguishable by the shape of the sexual aperture alone. There are principal differences in the reproduction of the two main tick families.
Reproduction in ticks is closely associated with feeding. This is of parasitological significance, since many pathogens of veterinary and medicial importance are transmitted transovarially to the progeny of female ticks which have taken up the pathogens with their blood meal. Because many tick species can lay very large numbers of eggs, this mode of transmission can become a most efficient means of multiplying the pathogens (viruses, bacteria, rickettsia, or protozoans). Reproduction in ticks is therefore not only of direct interest for the maintenance of tick populations, but also assumes a serious economic significance in relation to tick-transmitted diseases.
In argasid females, feeding and oviposition are cyclical activities which can be repeated several times (up to seven or Moore times). Mating can also be repeated in association with each female feeding. Mating can take place before or after feeding. Mated females digest the blood meal and oviposit, after which they are ready to repeat the process. Virgin argasid females, on the other hand, interrupt vitellogenesis until mating takes place, even if this does not occur for a long time. Unmated, engorged female Ornithodoros moubata can starve for up to 200 days before mating triggers off the completion of vitellogenesis and oviposition.
Autogenic development, i.e., the production of the next generation without the female feeding, has been reported in a number of argasid tick species. Facultative autogeny is usually exhibited during the first gonotrophic cycle when mated females lay eggs from which larvae hatch in the prolonged absence of a host, particularly in the case of ticks parasitizing seasonally migrant hosts. In the laboratory, autogeny can be induced in appropriate species under favorable conditions of temperature and humidity. Facultative autogeny has been observed in several species of Ornithodoros and Argas. The larvae of Ornithodoros moubata emerge from the egg and then remain quiescent until completing the molt to the nymph. In Ornithodoros savignyi some individuals complete the transformation from larvae to nymphs within the egg and emerge as nymphs. Obligatory autogeny is shown by two argasid genera with prolonged parasitic behavior, Otobius and Antricola. Antricola spp. females lack fully functional mouth parts. Otobius megnini has one parasitic larval and two parasitic nymphal instars which inhabit and do not leave the ungulate host's ear canals between blood meals, until the second nymphs leave the host and molt to the adult stages. Male and female adults both have vestigial mouth parts and do not take a blood meal. Mating takes place off the host and the female lays up to 1,500 eggs in small batches over a period of several months. Obligatory autogeny is similar in Antricola spp., where larvae and nymphs parasitize cave-dwelling bats, and females do not feed.
In ixodid ticks, larvae, nymphs and females all take a single complete meal after which they molt to the next instar, except when the female lays a single batch of eggs and then dies.
Thus, feeding and oviposition are each single events in the lifetime of a female. Autogeny has not been reported in ixodid ticks. Mating is only possible up to the completion of feeding, and is usually not possible prior to feeding. In most ixodid species mating takes place on the host only after attachment, but there are exceptions in the genus Ixodes, where in some species mating can take place prior to attachment to the host. In several species of Ixodes the male is as yet unknown, because mating apparently takes place off the host. The males appear either not to feed, or to feed parasitically on engorged females. Male Ixodes holocyclus and I. moreli have been shown to engage in homoparasitism, during which they feed on the hemolymph of partially or fully engorged females of the same species which appear to be unaffected. This may be an obligate form of male feeding in these and other ixodid species. Nymphs and males of Argas spp. and Ornithodoros spp. can also feed on the hemolymph and/or midgut contents of engorged individuals of their own species.
In contrast to oogenesis, a large part of gametogenesis is not closely correlated with adult feeding. After the initial development, formation is discontinuous pending adulthood and the transfer of germinal cells to the female genital system. Argasid ticks (Argas, Antricola, Ornithodoros and Otobius) undergo spermatogenesis prior to feeding as adults.
The female genital systems of ixodid and argasid ticks are basically similar, consisting of a single ovary with paired oviducts which fuse to become an unpaired common oviduct or uterus (Argas vespertilionis, possessing a paired ovary, is an exception). The uterus opens into the vagina which is divided into cervical and vestibular regions (Fig. 2). The ovary of the tick is a hollow, tubular, thin-walled organ with a horseshoe-shaped cross-section due to a fold or longitudinal groove along the dorsal or anterodorsal surface. The unpaired ovary forms a garland-like continuous loop through most of the length of the unfed female, beginning anteriad at the level of the central nerve mass or genital aperture, and extending posteriad near the sides of the tick to curve forwards in front of the rectal sac. At the height of egg production it is the most prominent organ in the female ixodid tick. It is made up of thin layers of epithelial cells with interspersed germinal cells and a basement lamina or tunica propria which forms the external, hemocoelic surface of the organ. Germinal cells are least developed in the longitudinal groove where oogonia and early oocyte stages are found. Outside the groove, the oocytes are generally more advanced and give the ovary a granular appearance (Fig. 3). When the tick starts feeding, oocytes covered by the basement lamina protrude into the hemocoel. The ovary then has a characteristic grape-like surface structure. In members of the Argasidae the posterior part of the ovary is studded with oocytes while the anterior part is smooth, whereas in members of the Ixodidae ova develop along the whole length of the organ.
At both ends the ovary tapers and passes into long, coiled oviducts running in an anterior direction. The oviducts are elastic tubes capable of peristaltic movements which serve to transport eggs towards the uterus and vagina. The oviduct is capable of stretching in order to accommodate eggs. In argasid ticks, the distal oviduct forms a distinct ampulla, but this is less pronounced in ixodid ticks. Distally, the oviducts fuse into a single common oviduct or uterus; this is a large bilobed triangular sac in argasid ticks, smaller in the Prostriata, and inconspicuous in the Metastriata, where a separate receptaculum seminis takes over the function of storing the spermatophores and spermatids. In argasid ticks these are stored in the uterus. The uterus is connected by a short tube to the cervical region of the vagina. This is short in argasids, but is an enlarged saclike structure in prostriates, where it functions as a receptaculum seminis.
The receptaculum seminis of metastriates is above the uterus and opens directly into the cervical vagina which is the proximal portion of the vagina as opposed to the distal, vestibular portion of the vagina. In argasid ticks the cervical vagina is short. It is ensheathed with a thick layer of circular muscles. In all ticks the vestibular vagina connects the cervical vagina to the genital aperture, and is capable of prolapsing actively during oviposition when it plays a significant role as an ovipositing tube. Tubular accessory sexual glands are present in all ticks. They have openings between the two regions of the vagina and are presumed to coat eggs with secretory products as they pass prior to expulsion. The lobular accessory sexual gland, which is only found in ixodid ticks, is formed in the vestibular vagina from the hypodermis during feeding. Its secretion partially waterproofs eggs during their passage through the vagina.
Géné's organ is common to all female ticks. It is found just above where the capitulum is joined to the idiosoma, in the camerostomal fold of ixodid ticks, the camerostomal depression of argasid ticks, or anterodorsally ventrad of the pseudoscutum in nuttalliellids. During oviposition, Géné's organ emerges through an aperture to give each egg a waxy surface, as a final waterproofing. The porose areas of female ixodid ticks (Fig. 6), whose function was not known for a long time, appear to act in conjunction with Géné's organ by producing inhibitors of the autoxidation of the unsaturated egg wax lipids.
The morphology of the female reproductive organs of the single species in the family Nuttalliellidae, Nuttalliella namaqua, is basically intermediate between corresponding argasid and ixodid organs. The transverse position of the ovary, bilobed uterus, and vaginal divisions into cervical and vestibular parts are as in argasids; however, the connecting tube joining the uterus and cervical vagina and the valve between the vaginal divisions are ixodid in character. On the other hand, Géné's organ has a structure unique to this family.
The male reproductive system consists of paired tubular testes which extend from the level of the central nerve mass or genital aperture to about the level of the posterior margin of coxa IV (Fig. 2). Apically, the testes extend to become a pair of vasa efferentia which fuse to form a common vas deferens and ejaculatory duct.
Posteriorly, the testes may be fused (as in the Argasidae), broadly joined (as in many prostriate ticks), or connected only by a thin filament (as in the metastriate ticks). The testes in adults are covered by a thin connective tissue membrane similar to the tunica propria of the ovary. There are muscle fibers under the membrane. The wall of the testis consists of epithelial, interstitial and germinal cells. The germinal cells are arranged radially around the small lumen of the testis, forming cysts. The lumen of the testis is continuous with the lumen of the vas deferens. The appearance of the testes varies with the tick species and its nutritional and reproductive state. In particular, there are marked changes in the testes of ixodid males when they commence feeding.
The vasa efferentia are extensions at the end of the testes which fuse to become the common vas deferens whose connection to the external genital aperture is called the ejaculatory duct, a name sometimes also given to the common vas deferens as a whole.
Close to the fusion between the vasa deferentia, the accessory gland complex opens into the common vas deferens (Fig. 2). This is a large, multilobed gland system which varies in appearance between tick species. The accessory gland secretes mucoproteins, mucopolysaccharides and other compounds. The glands are involved in producing materials for spermatophore formation as well as for spermatid capacitation.
The testes in ticks are fully developed at the end of nymphal molting. In contrast to insects, male germinal cell maturation occurs gradually from the posterior end to the anterior end of the testes. In Hyalomma asiaticum nymphs, primary spermatogonia areas occupy the anterior end of the testes and secondary spermatogonia areas the posterior end. Primary spermatogonia undergo mitotic divisions to produce several generations of secondary spermatogonia, the last generation becoming primary spermatocytes during nymphal blood feeding. In H. asiaticum, as in most other metastriate ixodid ticks, further development only occurs when the adult males begin feeding. Autogenous spermatid production in unfed males has been reported in two metastriate ticks, Aponomma hydrosauri and A. concolor. A third species Amblyomma triguttatum transfers elongated spermatids to females without a prior blood meal.
The timing of meiosis and spermiogenesis in the argasid and prostriate ticks is similar to that in most insects, occurring maximally during the final nymphal stage and the young adult period, i.e., prior to feeding as adults. Males of many prostriate ticks (genus Ixodes) do not feed at all. The same occurs in those species of argasid ticks which have vestigial mouth parts in the adult (Otobius spp.). A blood meal accelerates the germinal development.
Thus the male adult blood meal is the foremost stimulus for development of the primary spermatocyte stage in most metastriates. Other, earlier stimuli are active in the males of prostriate and argasid ticks. As a result of the stimuli which are effective, the spermatocyte undergoes a major growth stage, followed by two meiotic divisions to secondary spermatocytes. Newly formed spermatids are rounded and are found in the testes. Further development takes place as they move to the vasa deferentia and then to the common vas deferens, by which time they have an elongated form. Here they are stored until transfer to the female takes place through mating. Development is arrested at this point. Then the male transfers a spermatophore to the female. This is not preformed, but is produced during mating. The formation is a rapid process, requiring less than one minute to complete, and it occurs outside the male genital aperture. The spermatophore consists of two vessels, i.e., an outer (ectospermatophore) and an inner (endospermatophore) container between which the elongated spermatids are to be found.
When both sexes are prepared for copulation, the male tick positions himself with his venter in juxtaposition to the female venter, and inserts certain parts of the capitulum (varying between species) into the female sexual aperture. After this initial stimulation, which lasts some minutes, the spermatophore is formed and transferred to the female sexual aperture. Through evagination of the spermatophore only the endospermatophore is inserted into the female genital tract during copulation; the spermatids are contained only in the endospermatophore, while the ectospermatophore remains outside and soon drops off. The spermatophore is easily visible at the genital aperture of freshly mated Amblyomma variegatum females which are then no longer receptive for further stimuli from male ticks, which are themselves not attracted to these females. Mating triggers off an immediate feeding response in the females, regardless of the presence or absence of males. In this state female A. variegatum can then be induced to feed in an in vitro system.
In argasid ticks, endospermatophores and immature (uncapacitated) spermatids are stored in the uterus, while in ixodids they are transferred to and stored in other regions of the female genital tract: in the Prostriata this is the enlarged cervical vagina and in the Metastriata it is a separate receptaculum seminis which opens posterodorsally into the cervical vagina. The last stage of spermiogenesis, capacitation, then takes place within the female genital tract. The fully mature, or capacitated, spermatozoa are clavate or paddle-shaped at the anterior end, tapering into long posterior portions. Argasid sperm are longer than those of ixodids. The spermatozoon is 150–1000 μm long which is twice the length of uncapacitated spermatids. This is extremely large by comparison with the spermatozoa of other animals.
The surface of the tick ovary has a characteristic granular appearance which is caused by the partial protrusion into the hemocoel of the oocytes (Fig. 3). The oogonia and oocytes are less developed in the longitudinal groove along the ovary. As the female begins feeding, the oocytes protrude more into the hemocoel, above the surface of the ovary. They gradually project further until they are totally above the surface of the ovary, to which they remain attached by a thin stalk, the funicle, which is composed of elongated epithelial cells. Covering the oocytes and the ovary and separating them from the hemolymph is a basement lamina, which carries some muscle fibers on the outside. Balashov has divided the early, previtellogenic development into a phase of “small growth” followed by a phase of “large growth” with cytoplasmic growth, which is characterized by intense development of cytoplasmic organelles almost entirely lacking during the first phase. During cytoplasmic growth the surface area of the oocyte cellular membrane is greatly enlarged by the production of numerous microvilli below the basement lamina in preparation for further maturation of the egg. Vitellogenesis, the production of yolk as a nutrient for the developing larvae, is usually initiated by engorgement and mating, except in cases of autogeny or parthenogenesis as discussed above. The final product of vitellogenesis is represented by two kinds of yolk, protein and lipid. Lipid yolk is produced during the previtellogenic period but protein yolk is a characteristic of vitellogenesis, appearing as the membrane-limited granules shown in Omithodorus moubata to be composed of hemoglycolipoproteins which are immunologically identical to female hemolymph proteins. The yolk appears to have two different sources, intracellular from autosynthesis in the oocyte, and extracellular from synthesis in extraovarian tissues of precursors which are internalized by the developing oocytes. Protein yolk vesicles fuse to form large homogeneous yolk granules with a diameter of up to 80 μm in the egg of 0. moubata, which itself has a diameter of 1200 μm.
The source of the vitelline membrane has not been ascertained, but appears to be the oocyte. Eggshell synthesis begins during vitellogenesis when plaques of material appear between the microvilli of the cell membrane in the extracellular space under the basement lamina. As development advances, the microvilli become fewer and retract, while the eggshell plaques coalesce to form a complete vitelline envelope. From a certain point onwards, the vitelline membrane and the basement lamina appear to act as a barrier to the entry of pathogens which take the transovarian route of transmission. This has been shown for Babesia major kinetes in Haemaphysalis punctata, B. bigemina in Boophilus decoloratus, and in rickettsia. Although 28°C is a favorable temperature for the rapid development of B. bigemina kinetes in Boophilus decoloratus, only very few appear to be able to enter the oocytes which become impenetrable sooner at this temperature; at 24°C fewer kinetes are found in the hemolymph since a greater number are able to enter the oocytes before they become impenetrable (Fig. 3).
The success of transovarial transmission of parasites appears to be dependent on close synchronization with the development of the tick vector, and may be a reason for the more efficient transmission by some vectors. For example, Boophilus microplus appears to be a less efficient vector for Babesia bigemina, but a good vector for B. bovis.
The oocytes in the ovary of a tick do not develop synchronously, but can be found at different developmental stages at any time. As a result, vitellogenesis and oviposition are prolonged over several days or weeks in ixodid ticks.
Ovulation in ticks usually takes place within 1–2 weeks after the fertilized female has engorged. Following ovulation, peristaltic movements of the genital tract transport the eggs into the uterus where they can accumulate. The actual site of syngamy, i.e., the penetration of the oocyte by the sperm, has not been determined, and it may take place in the ovary or in the oviducts. During its passage the oocyte increases greatly in size, and the originally soft, extensible eggshell hardens progressively.
Generally, argasid females lay fewer eggs than ixodid females. Argas persicus can lay a total of 874 eggs in as many as seven batches, with a blood meal and mating preceding each batch. Ornithodoros coriaceus can lay over 2,000 eggs during a productive life of about 3 years.
Before oviposition can begin, the fully engorged females usually become positively geotropic and negatively phototactic, seeking sheltered places with a suitable microclimate. The female then becomes immobile. The preoviposition period of engorged female ticks lasts from 1 to 2 days up to several weeks depending on species and temperature. In Boophilus microplus this period is 2–4 days in the Australian summer and 5–9 days in winter, with a range of 2–12 days. On the periphery of the main area of distribution, in Southeast Queensland, oviposition is postponed indefinitely. Oviposition may be so far extended that many females die before ovipositing. The duration of oviposition is also dependent on the species of tick and the environmental temperatures, and can last from a few days up to several weeks.
Oviposition entails the individual treatment of each egg as it is laid. In ixodid ticks this requires a reorientation of the genital aperture to face the capitulum at an angle and to shorten the passage of eggs. In argasid ticks this does not take place, but otherwise oviposition is similar in both tick families. The next step is to bring the Géné's organ close to the sexual aperture. Géné's organ, the egg-waxing organ, is located in the camerostomal fold of ixodid ticks or the camerostomal depression of argasid ticks, dorsally behind or above the capitulum where it is joined to the idiosoma. It is an eversible two- or four-lobed sac with two anterolateral horns on each side. When eggs are about to be extruded from the vestibular vagina, the hypostome is depressed ventrally to such a degree that it rests against the venter of the tick, while the palpi diverge. As Géné's organ becomes fully everted, the vestibular vagina prolapses, forming an ovipositing tube through which the individual eggs are passed; they then pass between the horns of the Géné's organ. While the vagina retracts, the oocyte is thoroughly coated with waxy waterproofing secretions. In ixodid ticks, each oocyte is simultaneously exposed to a secretion from the porose areas during the period in which the Géné's organ covers this area of the capitulum. This additional secretion appears to inhibit the autoxidation of unsaturated egg-wax lipids. In argasid ticks waterproofing of the eggs is begun in the vestibular vagina. The eggs of argasid ticks are usually not sticky, while ixodid eggs adhere to the surfaces they rest upon. This can be upon the female tick's dorsum.
The ovipositing female of many ixodid species changes color, becoming yellowish or pale brown due to the masses of developing oocytes on the one hand, and the grossly distended Malpighian tubules on the other hand. Most of the metabolic waste is not eliminated by the female, and may be responsible, together with dehydration, for the death of the female ixodid tick soon after completion of oviposition.
The eggs of ixodid ticks are toxic to experimental animals, as are ovipositing female ticks. On the other hand, fully engorged female Amblyomma variegatum (which can have an engorged weight of up to 6 g) are consumed by herdsmen in parts of East and Central Africa, either raw or after roasting, and are considered a delicacy.
Contact between sexes and behavioral patterns leading up to copulation appear to be strongly influenced by pheromones. In ticks which mate off the host (i.e., argasid and some prostriate ticks) assembly pheromones, which are the least specific of the tick pheromones, appear to be responsible for bringing together males and females. These pheromones are also attractive to immature instars, e. g., in Argas persicus. The relationships between individuals of A. walkerae in the biotope are mainly induced by pheromones. Replete females determine the location of settlement, thereby sending the primary pheromonal stimulus attracting first males and then preimaginal stages to aggregate. Guanine excretions have a lesser pheromone effect. The assembly pheromone in guanine is less volatile than that emitted by the tick itself. In Ornithodoros porcinus porcinus, the guanine itself has been identified as an assembly pheromone which not only attracts conspecific ticks but is also attractive for larvae of Amblyomma cohaerens and adult Rhipicephalus appendiculatus.
A second type of pheromones, the aggregation-attachment pheromones, have been demonstrated in the metastriate genus Amblyomma, where they are produced by males during the course of feeding. They are more specific than assembly pheromones and attract conspecific unmated females, unfed males and nymphs. Hungry unmated females are reluctant to attach in the absence of this powerful stimulus. It is possible to induce mating in A. variegatum by removing males from the host after several days of feeding and placing them together with unfed females. Mating responses are immediate, culminating in copulation within a few minutes, after which the female is no longer receptive for males, but will commence feeding, frequently in the complete absence of a male. In this species, the primary stimulus leading to contact appears to be the male aggregation-attachment pheromone, followed by a response from the female (which may be recognized visually, or possibly chemically, by the male), whereupon the excited male agitates its striped legs, grasps the female, corrects her position if necessary, and then proceeds to insert his mouth parts into the genital opening and transfer the spermatophore.
The aggregation-attachment pheromones have been identified, the active substances being o-nitrophenol, methyl-salicylate and pelargonic acid. Pheromones are usually obtained for study by washing intact ticks in suitable solvents or by extraction from tick homogenates. They can also be collected from living ticks in small stainless-steel chambers when the effluent air is passed through solvents. The site of pheromone production in ticks has therefore remained difficult to determine. In a field trial synthetic pheromones were only partially successful in attracting ticks to an artificial target.
Ixodid or hard ticks are characterized by a dorsal shield or scutum of sclerotized cuticle in all stages which occupies about one-third of the anterior dorsal surface of females, nymphs and larvae, and the entire dorsal surface of males (Fig. 4, Fig. 5, Fig. 6). In female and immature ixodid ticks, the remaining, extensible dorsal surface is called the alloscutum. Argasid ticks are also called soft ticks, since they lack a scutum or dorsal shield in the adult stages and are covered by a leathery integument (Fig. 6).
In addition to exoskeletal functions of support and protection, the integument of ticks, particularly of ixodid ticks, is required to grow and expand in order to accomodate the large and concentrated blood meal. In ixodid ticks, the differences in size between larvae, nymphs, and adults are not as great as the differences between the flat, unfed instar and that same instar fully engorged. Larval, nymphal and female ticks of some species of ixodid ticks can increase in weight up to about 200-fold during feeding. As an example, Rhipicephalus appendiculatus larvae, nymphs and females can each increase their weight about 100-fold. During the blood meal the idiosoma of these stages is distended to give the typical enormously swollen appearance of the engorged tick. An additional important function of the integument of ticks is the regulation of water balance since it is highly impermeable to water.
The cuticle constitutes a limitation of the shape and maximum size of each tick stage. Further growth is only possible through molting of the pre-imaginal instars, i.e., by shedding the cuticle and replacing it with the larger form of the next stage.
As in other arthropods, the integument of ticks consists primarily of the cuticle and a single epidermal cell layer which secretes the cuticle. The cuticle is similar to that of insects (Fig. 7, Fig. 8, Insects), but differences exist, particularly in the alloscutum of female ixodid ticks. The cuticle is a heterogeneous, noncellular layer which forms an external covering but also extends into the fore- and hindguts and lines the ducts of dermal glands and the tracheal system. The degree of sclerotization of the cuticle varies from hard sclerotized plates to soft, extensible membranes. Ixodid ticks have relatively large areas of sclerotized cuticle, while in argasid ticks sclerotization is limited to fairly small areas.
The cuticle is composed of two primary layers, a thin outer epicuticle and the thicker inner procuticle. The epicuticle has considerable flexibility but is nonextensible in ixodid ticks. Stretching during feeding is possible through the unfolding of deep folds in nonsclerotized areas of the idiosoma of the ixodid tick. The epicuticle is nonchitinous and consists of wax, cuticulin and polyphenol layers. Argasid ticks also have a further outermost protective layer, the cement, a general arthropod characteristic which is absent in ixodid ticks. The cement is produced by dermal gland secretion. The wax layer confers impermeability on the cuticle. In ixodid ticks this is the outermost layer. Beneath it, the polyphenol layer is composed of minute droplets rich in polyphenols which penetrate into the underlying cuticulin layer. A thin protein or lipoprotein membrane carries large numbers of micropores connected to pore canals which themselves originate in the epidermal cell layer and pass through the procuticle, anastomosing terminally before reaching the cuticulin. In Ixodes ricinus it has been estimated that more than 1.4 million pore canals can be found per square millimeter (Fig. 7). Dermal glands become active soon after feeding begins, remain so until molting is complete, and are thought to participate in cuticular transformation.
The procuticle is composed mainly of chitin bound to protein and can show differing degrees of sclerotization. When the outer part of the procuticle is completely sclerotized, it is called exocuticle, and the nonsclerotized portions are then called endocuticle. The mesocuticle is defined as a partly sclerotized layer of the procuticle. Both the endo- and the mesocuticle, which form the alloscutum cuticle, are extensible and enable the accomodation of the large blood meal in larval, nymphal and female ixodid ticks, through their capacity for expansion and stretching. The increase in the volume of the tick is particularly rapid during the final feeding period and is achieved by considerable stretching of the alloscutum. This is made possible during the initial feeding period through preparatory growth of the cuticle, enabling the phase of rapid feeding. During the first phase of feeding, growth of the cuticle dominates over expansion, while at the end of feeding, when ingestion reaches a peak, idiosomal distension occurs as a result of cuticular extension.
During the growth period, procuticle with a complex lamellate structure is deposited. At the same time, epidermal cells enlarge 3 to 4 times, with rapid development of organelles involved in synthesis. In argasid tick larvae, which feed for several days, there is also cuticle thickening during the growth phase. During the final phase of ixodid female feeding, the cuticle of the alloscutum stretches and is reduced to about half the thickness reached at the end of the growth phase.
During molting (ecdysis), a phase of cuticle separation (apolysis) is followed by formation of new cuticle and shedding of the previous cuticle. Separation results from lysis of the procuticular lamellae closest to the epidermis. In the new cuticle epicuticle is formed first and then procuticle.
Hemocyte participation in the molting process is peculiar to ticks. During the premolting period, apolysis and the early stages of new cuticle formation, numerous hemocytes lie under the epidermal cell layer, sometimes penetrating into the epidermis.
Ticks are typically acarine in having hexapod larvae and octapod nymphs and adults. The legs are jointed and divided into seven segments (coxa, trochanter, femur, genu, tibia, tarsus and pretarsus). The terminal pretarsus consists of a basal stalk, paired claws and a membraneous pulvillus (Fig. 4, Fig. 6). The pulvillus is absent in argasid ticks. Each true segment is flexed by an individual flexor muscle, while coxal protractor and retractor muscles provide backward and forward leg movement. Leg extension is brought about by hydrostatic pressure. All legs are ambulatory, but the first pair of legs also aids in sensory orientation.
Powerful muscle groups are also present in the alloscutum of female, nymphal and larval ixodid ticks, through which the tick is able to redistribute the centre of gravity and regain an upright position when it falls into an upside-down position. The dorsoventral muscles are arranged roughly in longitudinal rows. The point of insertion is characterized only by shallow furrows or grooves.
The major organ systems and the chelicerae are equipped with muscles, most of which only play a role during the short periods of host-orientated activity and the following digestive and/or ovipositing periods.
The structure of muscle attachment in ticks must make allowance for the periods of molting from one stage to the next, particularly when the muscle is attached to the cuticle. By means of the electron microscope, muscle attachment has been shown to be through a structure characteristic of other arthropods. Tendons, or tonofibrillae, by which the muscles are attached, consist of two sets of tonofibrillae which are not continuous from the muscle to the epidermal cells of the cuticle. One set of tonofibrillae is anchored to the internal faces of muscle cells, while the second set is attached to the epidermal cells. The intercellular spaces between tonofibrillae are filled with a cement-like substance. The anchorage at both the proximal muscle cells and distally the epidermal cells is through structures known as hemidesmosomes, which are adhesions between the basal lamina through the plasma membrane to the cytoskeleton. Similar arrangements are found in mites (Fig. 7B, Mites/Fig. 1).
The entrance to the alimentary canal, the tubular buccal canal, is formed dorsally by the chelicerae and ventrally by the hypostome (Fig. 4, Fig. 9). These two parts of the gnathosoma form the anchorage of the tick to the host skin during feeding. The chelicerae are paired, sheathed, rigid, sclerotized tubes with two segments (other acarians have three segments) ending in cutting digits with recurved teeth with which the tick penetrates the host skin (Fig. 9, Fig. 10). The unpaired hypostome is an extended, toothed anterior process of the basis capituli with retrograde denticles on the ventral surface. In ixodid ticks with the exception of some Ixodes spp., the feeding channel is further sealed during host attachment by attachment cement, a salivary gland product which solidifies almost immediately, making the tick alimentary canal continuous with the lesion in the host skin. The cement seals off and firmly embeds the mouth parts (Food Uptake and Digestion). If some tick species are removed manually from the host, the cement often remains attached to the mouth parts.
The buccal canal is a common duct for the intake of host tissues and for the outflow of saliva. It passes into the pharynx, a powerful suction organ with several sets of constrictor and dilator muscles, which, in conjunction with the pharyngeal valve, moves host tissues into the esophagus. The esophagus, a narrow tube adjoining the pharynx, passes through the synganglion or “brain” (as in other acarians) before leading to the midgut or ventriculus. This consists of a large central chamber from which several pairs of blind-ending diverticula or ceca lead off, providing additional surface area on which digestive processes can take place. Some are branched or form numerous loops. The midgut fills most of the body cavity of the tick. It is well equipped with muscle fibers situated externally and arranged both longitudinally and transversely, and is capable of peristaltic and other movements. When the leg of a tick is cut off, as in investigations for hemolymph stages of Babesia spp. or Theileria spp., the hemolymph is frequently mixed with gut contents because ceca protruding into the leg are also damaged.
The midgut has a fairly uniform structure throughout, the wall consisting of a single epithelial cell layer resting on a thin basal lamina, with muscle fibers on the hemocoelic side. According to Balashov and Sonenshine, three types of cells are present in the epithelium: reserve or stem (undifferentiated) cells, secretory cells and digestive cells. Agdebe and Kemp described intermediate digestive cells (digestive cell series) and two different secretory cells in Boophilus microplus. There are indications that each cell can differentiate successively to serve both secretory and digestive functions, particularly in argasid ticks. In ixodid ticks it appears more likely that each cell differentiates irreversibly to take either a secretory or a digestive role. The apical or luminal surface of epithelial cells is covered with microvilli, while the distal plasma membrane is folded until the time when the tick begins ingesting blood. Because of projecting epithelial cells, the midgut lumen is small.
A short intestine (sometimes called the small intestine) joins the midgut to the rectal sac. It is a tube narrowing towards the rectal sac which it enters anteroventrally. In the rectal sac, the fecal discharge accumulates, together with the products of the Malpighian tubules, to be expelled through the anus.
In ixodid ticks the salivary gland plays a major role during feeding, and it is also of importance for the development of a variety of pathogens, many of which conclude their development there before being transmitted to the host. The role of the salivary gland in argasid ticks is different, the excretion of fluid into the host during feeding being minimal. In ixodid ticks salivary excretion into the host animal body is responsible, to a large extent, for preventing the excess dilution of the tick body fluids by eliminating the major part of the blood meal's liquid content (Food Uptake and Digestion). It has been the subject of extensive studies, both by light and electron microscopy.
The salivary gland is a paired organ with a similar appearance in both sexes (Fig. 9). It consists of grapelike clusters of acini extending from the level of the peritremes along the sides to the gnathosoma, where the paired main ducts open into the salivarium, which opens dorsally into the buccal canal.
In argasid ticks two types of acini are present, while in ixodid ticks there are three in females and four in males of some species. Type I acini are agranular and are confined to the anterior region of the gland, where they open directly into the main or secondary ducts (Fig. 9). In Hyalomma asiaticum, type I acini contain several nuclei, one of which is considerably larger than the others. In Rhipicephalus appendiculatus four types of cells are found. The peripheral cells show densely compact foldings of their plasma membranes to and from the basal lamina, forming a basal labyrinth, and interdigitate with the peripheral plasma membranes of the central cell with its large nucleus. A ring-shaped constrictor cell surrounds the acinar duct which is also formed by the neck cell. The structure is thought to be responsible for secreting hygroscopic salts required for the active uptake of atmospheric moisture by nonparasitic stages. The acinus type I shows little change during feeding. Type II acini in argasids show two or three cell types in different species. In ixodid ticks, the granular types II–IV acini show marked changes during feeding. Up to 10 different granular cell types are found. The granules are sometimes complex in structure. Type II acini increase in size and secretory activity during feeding, and can dominate in late feeding. As in type III and IV acini, cells are arranged in radial segment fashion around the lumen which leads to the duct, passing a valve (argasids do not have a valve). There is no clearly proven association between structure and function of cells in granular acini, some of which pass through a rapid sequence of synthesis, secretion and hypertrophy. This sequence is asynchronous between cells. The type IV acinus of R. appendiculatus males continues development after the first mating and may reach its maximum size several days after the female has dropped. All acini types include a variety of secretory cells, the products of which fulfill different tasks such as lytic, anesthetic, anticoagulant functions.
All ticks are obligate ectoparasites of mammals, reptiles or birds. Depending on their host relationships, ixodid ticks can be referred to as one-, two- or three-host ticks, while most argasid ticks can be referred to as multihost ticks. These feeding habits are of ecological interest as well as of significance in disease transmission and control of ticks. The larvae, nymphs and adults of one-host ticks all feed and molt on the same host. Ticks of the genus Boophilus are such examples where larvae attach to bovines and engorged females drop off the host 3–4 weeks later. Except for the engorged female, all stages are very small. The genus Margaropus also includes one-host ticks. Acaricide resistance in ticks is particularly prevalent among one-host ticks (Boophilus) where selection pressure is directed against all stages and heritably resistant mutant individuals have a greater chance of survival and of becoming the progenitors of resistant populations. In the two-host ticks larvae feed and molt without leaving the host, the replete nymph dropping and molting on the ground. The adults then seek a second host to complete development. Rhipicephalus evertsi, with two subspecies, is a two-host tick found throughout sub-Sahelian Africa. Some species of Hyalomma are also two-host ticks and among them are ticks which can use two or three hosts in different generations. The majority of hard ticks require three hosts to complete development, each stage becoming replete on a host and then dropping to the ground to molt. Larvae, nymphs and adults each seek a different host, the engorged female dropping from the third host to lay eggs on the ground. Seasonal and regional variations in the prevailing microclimate conditions of three-host ticks can result in life-cycle spans of 2 or 3 years in Dermacentor andersoni, or even up to 6 years in Ixodes ricinus, in cool climates.
In two- and three-host ticks the different stages may prefer completely different host species. In many three-host ticks larvae and nymphs prefer small rodents and lagomorphs as hosts while adults attack larger mammals. In some cases the larvae and nymphs of a species are unable to survive on the host species of the adults.
The argasid ticks have different feeding habits from hard ticks, with usually much shorter feeding periods and up to seven nymphal feedings (Ornithodoros coriaceus) as well as up to seven meals in the adult stage (Argas persicus), with a different host each time. Ticks with these feeding habits can be termed multihost ticks. Otobius spp. are exceptions, showing a modified one-host pattern of feeding.
Ticks show a varying degree of host specificity. This varies from the very wide range in ticks such as Ixodes ricinus (mammals, birds, reptiles) to preferences for smaller groups such as in the Haemaphysalis leachi group which prefers carnivores, and finally to very high specificity, sometimes involving a single host such as is found with Rhipicephalus simpsoni on the cane rat. On the host, many tick species choose more or less specific sites, usually for strategic rather than other purposes. In East Africa, ticks with long mouth parts and very painful bites (Amblyomma spp.) prefer the perianal and inguinal regions where the host cannot reach them and where they are safer from predating birds of the genus Buphagus (oxpeckers). Specific sites in adult ticks are also likely to improve the chances of finding a mating partner.
Ticks are reluctant to feed on an unusual host. lf they do feed, they take up smaller quantities and concentrate the components to a lesser degree. Out of five mated rhinoceros tick (Amblyomma rhinocerotis) females engorged on a bovine, only three laid eggs, of which only one batch hatched. The resultant larvae refused a variety of laboratory hosts.
In ticks, reproduction and feeding are often closely related . However, there are many cases of larval and adult ticks not requiring a blood meal for further development (Reproduction and Feeding). In many prostriate species the male does not feed.
As a rule, the period of feeding is short in argasids and long in ixodids. In most species of Argas and Ornithodoros adults and nymphs do not require more than 15–60 min to engorge, the range being approximately 2 min to 2 h. Larvae of argasid ticks require longer feeding times than the corresponding nymphs and adults. Argas persicus and A. reflexus larvae require 5–10 days and A. boueti 16–25 days. During engorgement soft ticks ingest quantities of blood corresponding to 3 or 4 times their original body weight. In hard ticks this quantity can be 50–200 times the weight of the unfed female. They remain attached to the host and engorge in 5–12 days, unless they do not mate, in which case they may remain for several weeks. Larvae and nymphs of Rhipicephalus appendiculatus increase their body weight to the same degree as the female, i.e., about 100 times. Male ixodid ticks feed for 3–5 days, during which time their weight more or less doubles and after which they will ingest further blood only if the nutrients are exhausted while they are searching for or waiting for a female. They may remain on the host, sometimes seeking a fresh host, for several weeks or months.
The attachment of ticks to the host is interesting both from the point of view of the physiological adaptations to this role and from its significance for the health of the host which is of extreme economic importance, the cost of tick and tick-borne disease control being measured in thousands of millions of dollars per year.
The initial lesion is formed by the cutting digits of the chelicerae which in some species may be aided by lytic components of saliva. The hypostome enters the wound and becomes embedded by the recurved teeth which are mainly found on the ventral surface (Fig. 1).
In most ixodid ticks, insertion is accompanied by a flow of attachment cement which enters the wound and bathes the hypostome and chelicerae, apparently hardening almost instantaneously, and which results in a formation characteristic of the tick species or genus involved. The cement casting usually consists of a core wedged into the skin lesion and a spread cone encasing the hypostome and chelicerae which provides a seal on the skin of the host. The cement appears to be basically proteinaceous, and, interestingly, contains several immunogenic proteins also found in salivary gland extracts. The physical nature of the cement prevents these proteins from having antigenic activity. When ticks are forcibly removed cement is still often found on the mouth parts. Argasidae and some prostriate ticks do not form cement.
While the mechanical action of host penetration is confined to minor damage to adjacent tissues, tick salivary components are responsible for a wide range of tissue changes and local or systemic host reactions. It is not always possible to distinguish direct salivary activities from immune or pathological reactions of the host. The saliva has been shown to have a variety of pharmacological effects. The anticoagulant activity was shown as early as 1898 –1899 in Ixodes ricinus by Sabbatini and has since been found in other ixodid tick species. In argasid ticks, the excretion of fluid into the host during feeding is minimal. The anticoagulant of Rhipicephalus appendiculatus has been isolated and purified from the salivary glands of adults. It is a protein with a relative molecular weight of approximately 65,000 that inhibits blood clotting factor Xa and is mainly produced during the period of rapid engorgement from day 4 to day 7 of feeding and is not immunogenic. Small quantities are effective anticoagulants for large volumes of blood at 10°C and at room temperature, but at 37°C the anticoagulant activity is removed in less than 1 h possibly due to metabolizing activities of bovine or rabbit blood. This may be an indication that the anticoagulant is only active directly at the tick bite site and is possibly a precaution to prevent continuing activities within the tick itself. Tick salivary gland extracts also have effects on vasodilation, vascular permeability, and cytolytic activities.
In both ixodid and argasid ticks the elimination of excess water and ions is a vital function during the uptake of the more or less exclusively fluid nutrients (Excretory System). Two different strategies are involved in extracting these from the hemolymph. In argasid ticks coxal fluid secretion starts near the end of or immediately after engorgement. In ixodid ticks the salivary glands remove the excess fluid from the hemolymph while the tick is still attached to the host, thereby concentrating the blood meal immediately and allowing a larger volume of blood to be taken up. When this process has been completed it is a major endeavor of all ticks to prevent any further loss of fluid until the next blood meal.
Some tick species do not form clearly distinguishable hemorrhagic feeding pools at the tick bite site, although there is a distinct area of affected tissue surrounding the tick mouth parts. The fast-feeding argasid adults cause a hemorrhagic pool to develop soon after attachment. The cavity formed beneath the mouth parts of some ixodid ticks may to some extent be a result of host reactions and may not be essential to tick feeding.
Whole blood forms an essential part of the tick diet. Ixodid ticks can also successfully ingest other tissues practically devoid of red blood cells. Amblyomma variegatum nymphs feeding in an in vitro system achieved 24% higher engorged weights when they fed on heparinized whole blood than when they fed on defibrinated blood from the same bovine donor.
Feeding stimuli are better known from argasid ticks than from ixodids due to the possibility of in vitro feeding which is less successful in ixodids. Argas spp. and Ornithodoros spp. respond to reduced glutathione, nucleotides and amino acids, but in most cases only if at least 1 mg glucose/ml is also present in the medium. There appear to be separate chemoreceptors on the mouth parts, one specific for glutathione and nucleotides and the other for amino acids.
In ixodid ticks the addition of ATP or glutathione to the medium enhanced the attachment process of ticks partially fed in vitro. Recently, carbon dioxide which is known to be an attractant for ticks (Host Finding) and to have a strong effect on the water balance has also been shown to be a phagostimulant for Rhipicephalus appendiculatus and Amblyomma variegatum. Using a 5% CO2 atmosphere, the larvae and nymphs of A. variegatum can be induced to fully engorge in an in vitro system in the total absence of a host animal, achieving engorged weights comparable to those achieved on mammalian hosts and with a high molting rate. Rhipicephalus appendiculatus larvae, nymphs and females can be fed in an artificial system when the CO2 concentration is 7%. In this system female A. variegatum feed more successfully if ATP is added to the whole blood medium upon which they feed.
Host tissues, mainly in fluid form, are sucked in by a pharyngeal pump mechanism and pass through the esophagus into the midgut where digestion takes place. In ticks this is a slow intracellular process, in contrast to hematophagous insects where protein digestion basically takes place in the lumen of the intestine. As blood enters the midgut it passes into the large central chamber, from where it is further distributed into the diverticulae by peristaltic movement.
During the first phase of feeding in ixodid ticks, the growth phase, the tick ingests only small quantities of blood, while organs undergo growth and development. This period lasts for about 4–6 days in most species, with almost no blood uptake during the first 12–24 h of preparatory feeding behavior. During the growth phase blood is taken up by phago- and pinocytosis into the type 1 digestive cells which are predominant at this time; this is followed by a rapid breakdown of their components. The mobilized nutrients are used to build the cuticle for the enormous expansion during the following phase, as well as for the preparation of intense metabolism during and after feeding. During the second or expansion phase the major part of the blood meal is ingested by the tick within a period of usually not more than 1–2 days. At this stage the main component appears to be whole blood, while in the earlier stage a large proportion of inflammatory cellular components is contained in the ingested tissues. As the first large part of hemolysed blood enters the midgut, type II digestive cells become abundant. These cells take up hemoglobin and other proteins by pinocytosis. No signs of phagocytosis have been observed in this cell type. During the expansion phase the idiosoma of larval, nymphal and female ixodids shows the characteristic enormous distension which is due to cuticular extension.
Whereas feeding and digestion in ixodid ticks are not separated but merge, digestion in argasid ticks starts after the tick has dropped off its host. During the first phase the blood meal is concentrated in the gut lumen with little digestion, while hemolysis of red blood cells begins. This is followed by a second phase of intensive intracellular digestion by the digestive cells. The third phase is characterized by a slow rate of digestion and low metabolic activity of the starving tick while it is waiting for its next blood meal which, in extreme cases, can be delayed for many years.
Hemolysis, i.e., the rupturing of the red blood cell membranes and the release of hemoglobin, has been investigated in Ornithodoros savignyi and has been shown to take place gradually as the red blood cell membranes became increasingly fragile. In this tick species, hemolysis was more rapid in males than in females. In ixodid ticks hemolysis appears to be a more abrupt process, taking place soon after ingestion of blood and leaving no trace of cell membranes in the midgut blood mass. The saliva of Rhipicephalus appendiculatus females fed for 4 days was found not to have any hemolytic effect.
The engorged weight of an ixodid tick can correspond to 50–200 times the unfed weight, while there is less weight increase in feeding argasid ticks. The blood is concentrated 2–3 times during uptake and the volume of the blood in the engorged tick may be only 20% of the total volume of blood imbibed. Some ticks, particularly members of the genus Dermacentor, excrete large amounts of undigested blood through the anus during feeding, i.e., while they are still on the host animal.
In all ticks, the task of removing excess hyposmotic fluid rapidly during or immediately following the blood meal is vital for osmoregulation and is a major excretory effort. In the two main tick families, fluid excretion is achieved by two entirely different mechanisms.
Argasid ticks remove fluid during the final period of engorgement and/or after they have left the host. They can be observed to exude large volumes of a clear fluid from a pore on the first coxal joint. The fluid is secreted from the coxal organ, a tubular osmoregulatory apparatus ending distally in a filtration membrane. This is assumed to form an ultrafiltrate of hemolymph, which itself receives fluids and ions from the midgut while the blood meal is being concentrated. Further regulation of the fluid balance is carried out in the coxal tubule which leads the final excretory product to the coxal orifice by which it leaves the tick; this mechanism is suited to the fast feeding habits of most argasid ticks which remain attached for a few minutes to two hours. Argasid ticks appear to inject negligible saliva into the host.
In ixodid ticks, which usually feed for several days or even weeks, removal of hyposmotic fluids is achieved by means of the salivary glands. The salivary gland is a paired acinar organ with a complex of various cells, of which a major portion is granular. Of the three acinus types found in female ixodid ticks, type I and type III acini have been suggested as sites of water secretion (Fig. 9A). There is more evidence available that cells in type III acini are mainly responsible. These cells undergo striking morphological changes during the course of feeding, including the appearance of a cell type designated the “water cell”. Type II and III acini play a significant role as the sites of proliferation of the infective stages of Theileria spp. and Babesia spp. which are transmitted with the saliva. This may be a further indication of the major excretory function of these two types of acini.
None of the cells found in the acini have been conclusively attributed with specific functions related to the known activities of the salivary gland or the saliva. These include the production of attachment cement and various pharmacologically active components, some of which are shown in Table 3.
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In ixodid ticks, the final phase of feeding involves in particular a rapid concentration of blood nutrients, during which the hemolymph is loaded with the resulting excess fluid; this excess is then removed by the salivary gland and injected into the host. Feeding is a rhythmic succession of salivation and food uptake. Interfering with salivary gland function or control and hence osmoregulation, such as by applying organophosphate acaricides, results in an inability to remove excess fluid, leading to a disruptive increase in hemolymph volume. During feeding, some ixodid tick species excrete large amounts of undigested or partially digested blood. Particularly profuse excretion occurs in the genus Dermacentor where fecal water loss can be up to 25% of the total elimination of water. In other species fecal loss may be negligible, but the volume of saliva injected into the host can be as great as or greater than the total volume of the engorged larva, nymph or female.
As in other arachnids, ticks conclude nitrogen metabolism with the production of guanine rather than uric acid. In ticks, nitrogenous excretion is largely separate from ion and water regulation. The guanine content of excreta is very high and it is eliminated in almost solid form, thus preserving water reserves in the starving tick. Excretion takes place in the Malpighian tubules, a pair of blind-ending slender tubules which form several loops in the body cavity and open into the rectal sac where there may be mixing of Malpighian excreta with feces before elimination of both forms through the anus. In engorged female ixodid ticks, the Malpighian tubules are grossly distended and visible through the integument as wide yellowish lines which increasingly fill the body cavity, since the tick eliminates only a very limited amount of metabolic waste before dying. Ticks kept at constant temperatures under laboratory conditions appear to defecate less frequently, but in greater quantity at a time, than ticks exposed to natural diurnal temperature rhythms. This may be a factor contributing to the longer survival of many ticks kept under natural temperature regimes.
In ticks there is a very close association between the nervous and the circulatory systems. This is demonstrated by the enclosure of the entire central nervous system within a perineural sinus of the circulatory system; this receives a dorsal aortic vessel and gives rise to vessels enclosing the major nerve trunks.
No part of the central nervous system is located within the gnathosoma of the tick, which therefore does not correspond to the head in the generalized arthropod. The brain is located centrally at the level of the second coxa. Ticks can be killed quickly by crushing this region with a hard object (ticks are very resilient: a practical method of destruction is with hot water). The central idiosomal position of the central nervous system makes it poorly accessible for direct investigations.
The tick central nervous system is more condensed than in other Chelicerata. It is a synganglion, formed by the fusion of the brain ganglia and the abdominal nerve cord into a single mass. The nerve trunks arising from the ganglia are formed by axons of both receptor and motor cells. As in other acari, the synganglion is divided into two parts by the esophagus. Cranially, the esophagus lies beneath the synganglion, then crosses obliquely through the synganglion in a ventrodorsal direction to lie dorsally on the posterior portion before joining the midgut. The cranial, pre-esophageal part of the synganglion consists of the protocerebrum, the optic lobes, the cheliceral and pedipalpal ganglia, and the stomodeal pons or bridge.
All ticks examined have been found to possess well-developed photoreceptors, even the “eyeless” ticks (Aponomma, Ixodes, Haemaphysalis). They also have optic nerves and optic ganglia in the brain. A set of paired nerves extends from the optic lobes, a second set of paired nerves serves the chelicerae, and a third innervates the pedipalps. The unpaired stomodeal or pharyngeal nerve innervates the pharynx.
The postesophageal part of the synganglion gives rise to four pairs of pedal ganglia serving the four pairs of legs in the adult tick. Fine “sympathetic” nerves connect all four pedal nerve trunks laterally on each side of the synganglion. Several pairs of opisthosomal nerves innervate the viscera. The ventral lobes of the pedal ganglia of leg 1 contain discrete areas of highly differentiated neuropile which are thought to receive olfactory fibers from pedal nerve 1, and have been called olfactory lobes.
Associative centers are represented by several bilaterally symmetrical glomerular structures. Anterodorsal, posterodorsal, and ventral glomeruli in the pre-esophageal part are connected by nerve fiber trunks. A complex of nerve fibers and trunks in the postesophageal part of the synganglion forms a five-level commissure-connective system.
The synganglion and all peripheral nerves are covered by a connective tissue sheath, the neurilemma, below which there is a relatively thin layer of glial cells, the perineurium. Beneath these layers, subperineural glial cells are located on both sides of a cortex layer of nerve cell bodies surrounding the central fibrous neuropile, which constitutes the greater part of the synganglion mass.
There is some direct and indirect (effects of acaricidic activity) evidence that acetylcholine and catecholamines (dopamine, noradrenaline, norepinephrine) play a role as neurotransmitters in ticks. However, the role of these substances, which are known to act as neurotransmitters in other animal groups, must remain speculative until further evidence has been provided.
The various tick species show very different types of host-finding and feeding behavior patterns. E.g., they may find their hosts by active hunting or by ambushing behavior, they may use one host for their whole life cycle, or depend on the acquisition of 2 or more hosts, they may be specialized on a specific host type or show little specificity for particular animal groups. In one-host ticks host-seeking takes place once during the whole life cycle. The risks involved are thus reduced in comparison with two-, three-, or multiple-host ticks where there are correspondingly more critical periods for each individual. Ticks which can complete their whole life cycle within one limited environment (e.g., nest, burrow, cave) may nonetheless be exposed to long periods of starvation during migration and other seasonal or irregular absences of the host. This risk is reflected in the ability of starving soft ticks to survive for periods of up to 14 years. Judging by the large number of offspring and the long periods of starvation to which ticks can be exposed, the chances of finding a new host appear to be fairly poor.
Host-finding of most ticks can be divided into phases such as habitat selection, host recognition at a distance, change over to the host, enduring contact with the host and exploration (selection of a feeding site), and the sequence of behavior patterns related to the feeding process such as piercing (insertion of the mouth parts), attachment of the mouth parts, secretion of salivary gland contents, ingestion, detachment of the mouth parts, and leaving the host.
Following hatching or molting and a period of quiescence, host finding is aided by orientation responses, which in ixodid ticks lead to a favorable distribution on the vegetation or other sites. In argasid ticks, orientation may depend on the presence of suitable hosts and may be more marked at night, as in the case of Argas persicus or A. reflexus in which the adults and nymphs feed on roosting avian hosts, remaining hidden during the day.
Much of the behavior of ticks seems to be dedicated to selecting optimal resting sites. Host-finding behavior is often only displayed when the environmental and physiological conditions support their survival. During host seeking, ticks normally select microhabitats with good opportunities to encounter a host. Many species ascend vegetation to heights favorable for contacts with the particular hosts. Also, the time of day has an effect on the microhabitat selection. For example, the larvae of the cattle tick Boophilus microplus ascend vegetation in the early morning and again in the evening. The microhabitat selection is achieved by responses to environmental cues such as gravity, light and humidity.
Ticks respond to hosts at a distance with various behavior patterns, depending on their host-finding strategy: Many ticks, in particular certain Hyalomma, Amblyomma, Ornithodoros and Dermatocentor species, seek their hosts by hunting, they move actively in the direction in which the host is seen or sensed. Due to their limited mobility, more abundant among ticks is the ambushing strategy, in which the parasites await the hosts in their selected microhabitats in the vegetation. They respond to host cues with questing behavior, i.e., an erect posture, in which the first pair of legs is waved in the direction of the host stimuli. The larvae of Boophilus spp., and probably the larvae of most ixodid ticks, show marked ambushing behavior. The larvae of B. microplus ascend the vegetation early in the morning and again in the evening to a height favorable for attaching to cattle passing close by. In other species, similar ambushes are prepared at heights appropriate to the preferred host species.
The approach of a suitable host is heralded by several stimuli such as volatile host emanations, vibrations, visual cues, radiant heat and touch. These cues are taken up by sense organs concentrated at the anterior end of the tick which indicate proximity of the host. There may be no response from quiescent ticks. Sense organs suspected to be involved in the host location and feeding behavior of ixodid ticks have so far been located at four main sites: on the tarsi of the first pair of legs, on the mouth parts, and on the scutum. They include olfactory, gustatory, mechano-, photo- and thermoreceptors, and probably humidity receptors. The dorsal surface of the tarsi on leg 1 of ticks has a unique set of sensory structures which include Haller's organ complex housing some of the tick's olfactory chemoreceptors. Other sensory organs on the tarsi are gustatory, mechano-, and thermoreceptors. The involvement of Haller's organ in host perception is evident from the “questing” posture of an alert ick, which lifts its first pair of legs and waves them while taking up a position favorable for dropping or crawling onto the host. In this function, the legs and the olfactory receptors correspond to the antennae of insects.
Volatile host emanations are the most important cues in tick host-finding. Most tick species are attracted by sources of carbon dioxide which can function as an “artificial host” and be used to demonstrate how active a tick is in finding a host. Activity ranges between hunting and ambushing behavior. Hunters are attracted to the carbon dioxide-emitting source and can be trapped with this gas, and ambushers respond sensitively with questing behavior. Amblyomma americanum is actively attracted by a carbon dioxide source from a distance of 21 m and carbon dioxide appears to also act as a phagostimulant. The more specific a tick species is in its choice of host, the more likely it is to require additional highly specific chemical stimuli to alert and attract it to the host. However, little is known on how different host specificities are encoded in the odors. The characteristics of tick olfactory sensilla suggest that they use very different compounds of the odors for host identification. This may be concluded in particular from data on the sensilla of tarsus I (including those of Haller's organ) of Amblyomma variegatum. Gas chromatography-coupled electrophysiology recordings using different vertebrate odors allowed the identification of specific receptors for lactone (2 receptor types), methylsalicylate, carbon dioxide (2 types), sulfide (2 types), benzaldehyde, 2-hydroxybenzaldehyde, aliphatic aldehydes, 2,6-dichlorphenol, nitrophenol, pentanoic acid, 2-methylpropanoic acid, butanoic acid, ammonia (2 types), and 3-pentanone.
Also, the behavior responses of ticks indicate that they may react to different components of host odor and that they may discriminate the odors of different host types. For example, the larvae of the bovine-specific B. microplus responded sensitively with questing behavior to skin surface odors of cattle, but only weakly or not at all to those of humans, pig, mouse and deer, whereas the larvae of the generalist Ixodes ricinus responded similarly to the different odors. Blends of synthetic odor compounds stimulated questing in both species. The stimulating activity of a blend of 37 compounds was achieved by a combination of only 7 of the compounds which as single substances were without effect (benzoic acid, 2-ethylhexanoic acid, hexanoic acid, 2-nitrophenol, 1-octen-3-ol, pentanoic acid and pyruvate). Under these conditions B. microplus achieved its specificity for bovine odors by responding more to the bovine-specific compounds 1-octen-3-ol and 2-nitrophenol, whereas I. ricinus reacted to each of the 7 compounds with similar intensity. Obviously, the response of ticks to odor is stimulated by a combination of different compounds, rather than by particular individual compounds, and also specific hosts may be recognized via the interplay of different odor compounds.
A special attraction to hosts occurs in certain species of Amblyomma. Females are attracted to the ungulate hosts by attraction/aggregation attachment pheromones which are emitted by feeding males on the hosts. The major chemical components in the pheromone are ortho-nitrophenol, methyl salicylate and pelargonic acid.
The ocelli of some tick species are sufficiently developed to play a significant role not only in perception of light and darkness, but also in perception of the host itself. Paired ocelli are found at the edge of the scutum at about the level of the second pair of legs. In argasid ticks they are smaller and found in folds at the sides of the idiosoma. In Omithodoros savignyi there are two pairs of ocelli. Even “eyeless” ixodid ticks (of the genera Aponomma, Haemaphysalis, Ixodes) have been found to have well-developed photoreceptors and optic ganglia in the brain. In ticks with ocelli there is a lens, a hemispherical, transparent, flat or convex cuticular thickening, underneath which a small group of photoreceptors or optic cells are situated. An optic nerve extending from this location leads to the optical center of the synganglion. This has been studied in Amblyomma americanum and in Hyalomma asiaticum. Vision in some species of Hyalomma and O. savignyi is thought to enable these ticks to actively pursue their hosts over long distances.
Also, vibrations which stimulate host-finding responses in many ticks may signal some host specificity. Sounds in the range of 3000–8000 Hz, as produced by swallows, stimulate hunting in Ornithodoros concanensis, and airborne vibrations in the range of 80–800 Hz, as elicited by grazing cattle, activate B. microplus larvae.
Radiant heat as another host cue may be effective over certain distances and offers directional information. Hunting species are attracted to heat sources and ambushers respond to heat with questing behavior.
Alert ticks cling to any moving substrate touching them. Particular host cues do not seem to be necessary for the change over to a host. However, on the host's surface gustatory and olfactory cues seem to decide whether the parasites will remain on the host, and they guide the parasites to particular feeding sites. Some species prefer feeding sites where they are out of reach of the attacks by the grooming behavior of the hosts. Little is known on how the feeding sites are found. On artificial substrates ticks orientate towards certain host skin extracts, but the chemical nature of the directing cues still has to be analyzed.
Once on the host animal, many tick species will not probe until they have arrived at the preferred feeding site and are out of reach of grooming by the host. On the few occasions that male ticks climb onto unsuitable hosts, they may probe immediately. Female ticks appear to avoid or reject inappropriate hosts more than males, but may engorge in exceptional cases. The carnivore tick Haemaphysalis leachi may engorge on bovines and lay viable eggs under conditions where dogs and cattle are kept in close contact.
In certain Amblyomma species an aggregation of the parasites at specific feeding sites is supported by the male-emitted attraction/aggregation attachment pheromones which attract conspecific males, females and nymphae. In the majority of the hard ticks studied so far, feeding females produce an attractant sex pheromone containing 2,6-dichlorophenol which attracts males to the feeding site.
The drop-off periodicity and its correlation with the distribution and habits of possible hosts for the next feeding are particularly important for ectoparasites of host animals that do not exhibit nesting behavior. In some tick species, it has been observed that drop-off times are regulated by a circadian rhythm related to the daily light cycle. There may also be a host-induced rhythm. Darkness plays the principal role in setting the phase of the rhythm. This may be combined with changes in temperature, such as those during movement from the shade of trees to light or vice versa, or from the stable to sunshine. In some ixodid ticks, such as Boophilus spp. females or Amblyomma variegatum nymphs, the sudden exposure of bovine hosts to increased light can trigger a rapid drop-off of engorged ticks. Such an effect is likely to cause the next tick stage to be found close to host resting places. In tick species where the next stage has different host preferences, more complicated strategies may arise to ensure the availability of the next host candidates. After dropping off, the engorged larvae of some ixodid tick species tend to move downward, whereas in other species there may be a tendency towards upward movement. These movements may reflect the nesting or non-nesting habits of the resultant nymphal tick's preferred next host.
Much information on the host-recognition phases of the ticks on the host's surface comes from studies dealing with the development of artificial feeding methods. The feeding sequence consists of behavior patterns such as piercing the skin with the cheliceral digits, anchoring with the hypostome-chelicerae complex to the attachment site (possibly with cement material), salivary gland secretion, uptake of host body fluids, withdrawal of the mouth parts, and leaving the host. Important cues for successfull feeding on artificial membranes are unknown chemical compounds of skin extracts, heat, humidity, carbon dioxide and mechanical properties of the membranes. Reduced glutathione, nucleotides and amino acids seem to function as phagostimulants. In vitro feeding systems now provide the means to investigate tick – pathogen relationships without the complication of feeding ticks on acutely infected hosts.
As in many other arthropod taxa, several groups of tick species are not sufficiently defined for a reliable differentiation and classification of species and subspecies. The scanning electron microscope has provided a tool to support morphological differentiation, but few investigations have included a biological background to validate the authenticity of species based on minor morphological differences and/or on host preferences. This is not required where the morphology is unique, and is nearly impossible in the ectoparasites of rare and elusive host animals.
Cross-breeding trials have been used to substantiate the results of morphological investigations. Thus Argas persicus, A. arboreum and A. walkerae have been confirmed as separate species. The males of two ixodid species, Rhipicephalus appendiculatus and R. pulchellus, can induce females of the other species to complete feeding although mating does not take place. In this way, some R. appendiculatus females can produce viable eggs and larvae, which can normally only take place after being triggered by conspecific mating. There is no parthenogenetic development in R. pulchellus. The phylogenetic relationship appears to be close enough for common pheromones to be present even though appropriate behavioral patterns are lacking. Intersubspecific hybrid formation between R. evertsi evertsi and R. e. mimeticus has confirmed the separation at subspecies level rather than at species level. When Boophilus annulatus and B. microplus are mated, sterile hybrid males and fertile hybrid females are produced. The female hybrids produce sterile males when back-crossed with males of the male parent species. Theoretically, sterile hybrid Boophilus ticks could be used to eradicate low-level Boophilus populations.
Studies on the cytogenetics of tick species may eventually provide a useful means of investigating phylogenetic relationships and may also provide a taxonomic tool for studying living tick specimens. The chromosomes of several tick species have been described. Most species are diploid. The diploid chromosome number in ticks ranges from 12 to 36, the whole range being present in the genus Omithodorus, where O. guerneyi has 12 and O. alactagalis has 34. Both species of Otobius (O. megnini and O. lagophilus) possess 20 chromosomes. In Argas most investigated species have 26 chromosomes (with 24 autosomes plus two sex chromosomes), exceptions being A. vespertilionis (20) and A. brumpti, with 24.
In the ixodid bisexual species which have been studied, there is a range of 17 to 28 chromosomes. The most common number of chromosomes and sex-determining mechanism found in metastriate ticks is 20 + XX in females and 20 + X in males. This combination is found in 11 species of Rhipicephalus, 12 species of Hyalomma, three species of Boophilus, and in some species of Amblyomma. The range in Amblyomma is from 19 to 22, in Aponomma from 17 to 21, in Dermacentor from 20 to 22, and in the bisexual species of Haemaphysalis from 19 to 22. In the parthenogenetic races of Haemaphysalis longicornis there is a triploid chromosome set with 30–35 chromosomes. The prostriate genus Ixodes has a chromosome range of 23 – 28, with 23 in I. holocyclus, 24 in I. cornuatus and I. tasmani, and 28 in others.
The male usually has one chromosome less than the female, except in Ixodes. With six exceptions, all members of the Metastriata have XO:XX male: female sex chromosome systems. Four species possess an XY:XX system, as do the Prostriata with the exception of I. holocyclus, which has XO: XX.All argasid species described have XY:XX chromosome systems. Two Amblyomma species have multiple sex chromosomes, with two different X-chromosomes in males and females. Chromosome polyploidy is suspected in some ixodid species, too. In general parthenogenesis is rare in ticks. If it does occur, it is accomplished by thelotoky; in such cases all the progeny are female and polyploidy is frequently associated with this type of reproduction. An obligate parthenogenetic tick is Amblyomma rohindatum, in Haemaphysalis longicornis this phenomenon occurs more often than in Dermacentor variabilis. The morphology of the chromosomes is species-specific. An X-chromosome is invariably longer that the autosomes – often 3–4 times as long – and represents the isobranchial type (= metacentric), while the Y-chromosome is usually heterobranchial (= submetacentric). The autosomes are mostly acrocentric.
