Non-nidicolous ticks - mostly Ixodidae

Non-nidicolous (or exophilic) ticks are species that occupy open, exposed habitats. Most non-nidicolous tick species occur in forest, savannah, scrub, brush, or meadow vegetation; others remain buried in sand or sandy soils, under stones, crevices, and elsewhere in the open environment. Most of the Ixodidae are non-nidicolous ticks, at least in some stage of their life cycle.

Appetence initiates the series of behavioral responses that leads to host contact and successful parasitism. Appetence is the "locomotory hunting for a host or seeking one from a vantage point" (Waladde and Rice, 1982). Appetence is preceded by hunger, which in turn is influenced by the tick's physiological condition; appetence does not occur in diapausing ticks.

Two basic strategies are used by arthropod vectors for finding hosts, passive and active.

Passive species remain quiescent in their habitat and depend upon contact with vertebrate animals that invade it. Active species leave their resting environments and fly or walk to attack their hosts.

Most non-nidicolous ticks use the passive host-finding strategy, i.e., they acquire hosts by direct contact with a passing host (= ambush strategy). Ticks living in grass, herb, or brush covered habitats climb the vegetation, clinging to the tips of stems or branches where they wait for direct contact with hosts that brush against these vegetative supports.

The ticks rest with their forelegs folded and the other legs holding the stem or grass blade. This is termed the questing pose. Often, the ticks rest with the anterior end of the body pointed down towards of ground, but this does not occur in all individuals or all species.

Vibrations caused by animal movements as well as odors, body heat, and shadows from such hosts excite tick responses, causing extension and rapid waving of the forelegs. If contact is made, the excited ticks cling to the bodies of animals as they brush past.

In addition to these broad differences in host-seeking strategies, the height at which ticks quest also plays an important role in the types of hosts they acquire. Generally, tick questing height is strongly correlated with the specific life stage and size of the most common hosts of each species or life stage; immature ticks tend to occur near the base of vegetation or leaf layer, where small mammals and birds are active, while adults generally quest near the tips of vegetation where they encounter larger animals (Lees and Milne, 1951; Loye and Lane, 1988; Fourie et al., 1990).

Some ticks exhibit an active host-finding strategy, the so-called hunter ticks; in these species, the ticks actually crawl or run towards their hosts. Such ticks shelter under the ground of their habitats, and emerge to attack hosts when these animals appear nearby. They may crawl (or run) across distances of many meters to attack and feed on animals resting nearby.

Host-finding strategies may also differ in different life stages, e.g., larvae of Amblyomma variegatum and A. hebraeum find hosts by passive (i.e., ambush) questing while nymphs and adults are hunter ticks. Lone star ticks, A. americanum, exhibit both the ambush and hunter type of host-finding strategies. Most encounter their hosts by direct contact (ambush); others crawl considerable distances when attracted by host odors and body temperature.

In addition to the general principles discussed above, tick host-seeking activity is strongly influenced by daily rhythms of questing behavior, by the height in the vegetation at which ticks (passive or ambush ticks) quest and by tick responses to host stimuli.

Host Stimuli

Host-seeking ticks recognize a variety of stimuli from prospective hosts which in turn excites their host-finding behavior, e.g., running towards the hosts (hunter ticks) or reaching for them from their questing positions.

Odors are undoubtedly the most important and best studied stimuli. Host-originated odors provide specific information and, when carried on wind currents, also provide directional information. Electrophysiological studies showed that cattle tick larvae, Boophilus microplus, readily discriminated the odors in washings from cattle versus dry air, with strong responses to the former. Human breath also evoked a response, but at "a much lower impulse frequency than that caused by cattlewash" (Waladde and Rice, 1982).

Among the most important host-originated odorants are carbon dioxide, a component of animal breath and ammonia, common in urine and other animal wastes. CO2 and NH3 attraction bring hungry ticks into close proximity to potential hosts, whereupon other, shorter range stimuli become effective. At shorter ranges, butyric acid and lactic acid become effective.

Radiant heat is synergistic when combined with odors, as Lees (1948) showed in his experiments with I. ricinus. Adult ticks responded much more strongly to a cloth-wrapped tube containing circulating water at 37 °C and emitting sheep body odors than to either the cloth or the warm tube alone. Close range stimuli include radiant heat, such as body heat from the host, odorants characteristic of sweat and other body odors (e.g., lactic acid or butyric acid) and contact.

Other stimuli which ticks are able to use in host-finding activities have been little studied, especially visual cues and vibrations. Visual images are probably most important in hunter ticks, which are believed to discriminate dark shapes against the bright background of the sky. Questing ticks of many species will respond to distinct shadows, with outstretched legs in the case of ambushing ticks or running by hunter ticks.

Vibrations are also excitatory; rustling the grassy or weedy stems on which ticks are perched in ambush will provoke their characteristic "grabbing" behavior, with the forelegs outstretched to cling to a passing host.

Some species respond to sounds within a particular range of frequencies. B. microplus larvae are highly responsive to sounds in the 80-800 Hz range, frequencies commonly emitted by feeding cattle, while Rhipicephalus sanguineus are attracted to the sounds made by barking dogs (Waladde and Rice, 1982).

Finally, tactile stimuli come into play only upon host contact, contributing, along with short-range odorants and body heat, to the selection of the feeding site and the commencement of blood-sucking activity.

In some instances, tick-originated rather than host-originated stimuli are of critical importance in tick host-seeking behavior. Thus, A. variegatum and A. hebraeum are excited by CO2 from cattle but select tick-infested animals when they detect the aggregation-attachment pheromone emitted by previously attached, feeding ticks (Norval et al., 1989).

Nidicolous ticks - mostly Argasidae

In contrast to non-nidicolous ticks, nidicolous ticks (from nidis, Latin for nest) live in secluded enclosures such as caves, burrows and nests of their hosts or harborages near these nests.
Nidicolous ticks include almost all of the Argasidae as well as many of the Ixodidae (especially in the Prostriate genus Ixodes). The differences in the host finding strategies, feeding behavior, survival parameters, activity periods, and other adaptations required for either of these two types of existence are enormous.

In general, nidicolous ticks respond to the same spectrum of host-originated stimuli as non-nidicolous ticks, e.g., CO2 body heat, and various odors.

However, the range at which these stimuli are perceived is considerably shorter than in non-nidicolous ticks. Typically, these stimuli are most effective when presented simultaneously, i.e., ticks respond more strongly to synergized stimuli than to individual stimuli. In addition, gradients are important and, in some cases, provide essential directional information without which the ticks either fail to respond, or are misdirected and fail to find hosts.

An example of how hungry nidicolous ticks respond to the sudden arrival of a host in their nest or harborage is shown by the work of Beelitz and Gothe (1991) on the behavior of Argas walkerae, a parasite of domestic fowl in southern and central Africa.
When a chicken was introduced in a chamber where ticks were confined; more than 90 % of these parasites responded by running without hesitation towards the host. That this response was the result of a combination of many stimuli acting synergistically was demonstrated by specific experiments in which host odors were presented without CO2 or without a CO2 gradient towards the host, or other stimuli were presented without the host odors.

CO2 alone is a potent excitant, as it is in many non-nidicolous ixodid species, but it is a secondary stimulus. In this species at least, successful host-finding behavior requires host body odors as well as CO2- radiant energy, such as heat from the host body, was found to be important but only in a secondary and complementary role.

Gravity appeared to have no effect on the orienting behavior of A. walkerae, but it is important in host-seeking behavior of several other species. As is the case with many other argasid species, intense radiation, especially in the range corresponding to daylight conditions (450-580 nm), depresses tick activity, inducing the ticks to remain in tree roosts and various crevices of their natural habitat.

The relative importance of different stimuli may vary greatly among nidicolous species. In some, such as endophilous nidicoles, host body heat and odors are likely to be of paramount importance, since the distance from parasite to host is extremely short. For others, such as harborage-infesting parasites that must migrate over considerable distances (e.g., meters) to reach their hosts, gravity, CO2, and even sound (A. cooleyi) serve as general excitants, bringing the searching ticks to a point where shorter range stimuli, such as host body odors and radiant heat, can lead the parasites to the host body.