Z O O E C O . O R G

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The biology of Ixodes ticks, with special reference to
Ixodes ricinus

J. S. Gray, Department of Environmental Resource Management, University College Dublin, Ireland.
 

Abstract

Ticks of the Ixodes ricinus (persulcatus) species complex are vectors for several zoonotic diseases including, babesiosis, ehrlichiosis, Lyme borreliosis and tick-borne encephalitis. An understanding of the biology of the vectors is fundamental to prevention and control of these diseases, and in addition to summarising established knowledge, this review addresses recent work on seasonal activity, host specificity, inter- and intraspecific variations in biology and factors affecting distribution and abundance.
 

Taxonomy

Ticks, which are related to spiders, are divided into two families, the Argasidae (soft ticks), and the Ixodidae (hard ticks). The two families differ in their morphology, feeding habitats and details of life cycles. All feed on the blood of vertebrates, but whereas the soft ticks (argasids) take relatively small frequent blood meals of short duration (minutes to hours), the hard ticks (ixodids) take just one very large blood meal at each instar (larva, nymph, adult female) and remain feeding at the same site for several days. Although members of both families can inflict direct damage, their main significance is as vectors of disease. The argasids generally occur in the immediate vicinity of their hosts e.g. burrows, nests etc (i.e. are endophilic) and visit their host(s) at frequent intervals to feed. Although a few soft tick species transmit important diseases such as human relapsing fever and African swine fever, they are far surpassed in veterinary and medical importance by the ixodids. The ixodids are considered to be globally the most important ectoparasites of livestock and are also vectors of many zoonotic diseases. Some ixodids have an endophilic habit, but the majority of important species are exophilic and when hungry they are found in the open, usually on the tips of vegetation from where they ambush passing hosts. The ixodids may be further classified as prostriate or metastriate, based primarily on morphological detail, but life cycle differences include the ability of the males of some prostriate species to undergo spermatogenesis and to mate without taking a prior blood meal. The majority of important ixodid species are metastriate, but the single prostriate genus Ixodes includes species that acquired added notoriety in the latter part of the 20th century as the vectors of several northern hemisphere zoonoses, such as Lyme borreliosis (LB), ehrlichiosis, babesiosis and tick-borne encephalitis (TBE) (Table 1). This review will focus primarily on the main vectors of these diseases, which are ticks of the Ixodes ricinus (persulcatus) species complex.
 

Distribution and life cycles

The Ixodes ticks responsible for the transmission of Lyme borreliosis and other zoonoses are distributed throughout temperate regions of the northern hemisphere (Table 1). This distribution does not, however, entirely coincide with the occurrence of the diseases they transmit. For example, even the most widely distributed zoonosis, Lyme borreliosis, does not occur in the southern states of the USA or in southern parts of Europe. Other diseases such as tick-borne encephalitis and murine babesiosis are even more restricted in their distribution, which may be due to the complexities of transmission dynamics in different areas and/or to variations in pathogenicity of the agents themselves.

Table 1. Zoonotic pathogens transmitted by ticks of the Ixodes ricinus species complex.

The basic life cycles of the four tick species primarily involved in the transmission of these zoonoses are very similar and, unless otherwise stated, the following account refers to the European tick, Ixodes ricinus. The three instars, larva, nymph and adult, each climb the vegetation in order to attach to a passing host. Once on the host the tick crawls to a feeding predilection site where it slits the skin with scalpel-like mouthparts (chelicerae) and inserts a barbed proboscis (hypostome) that together with cement secreted by the salivary glands, anchors the tick firmly in place. The tick remains in place for several days (larva, 2–3 days; nymph, 4–5 days; adult female, 7–9 days) during which time active growth of gut and cuticle occurs in order to accommodate the enormous blood meal, most of which will be acquired in the final 24 hours of engorgement. The adult male rarely feeds and never engorges. The tick does not neatly pierce blood vessels but creates a feeding pool by secreting vasoactive mediators and immunomodulators (Grubhoffer, 1999) that keep the blood flowing and suppress host attempts to resist the process. During feeding the blood meal is concentrated by the extraction of water which is then secreted back into the host by specialised salivary gland cells and is an important means by which tick-borne pathogens invade their hosts. Once fully engorged the tick withdraws its hypostome and tumbles to the ground where it begins digesting the blood meal and developing to the next instar. The digestive process consists of pinocytosis (microphagocytosis) and endocytosis of blood components by cells lining the gut, followed by intracellular digestion rather than intralumenal enzymic digestion as occurs in most other haematophagous arthropods. The lack of digestive enzymes in the tick gut favours the survival of ingested microorganisms and may explain why ticks transmit a greater variety of pathogens than any other group of arthropods (Sonenshine, 1991). Digestion is slow, and development of the new instar takes several months in the temperate regions inhabited by these ticks. The newly moulted (or hatched) unfed tick may remain quiescent for a time but will eventually ascend the vegetation to quest for another blood meal. In I. ricinus a full year may separate the active feeding periods of successive instars.
 

Tick habitats

The free-living stages of these Ixodes ticks are very sensitive to desiccation and cannot survive relative humidities of less than 80% for any length of time. This requirement restricts the ticks to habitats in which humidity at the base of vegetation rarely falls below 85% RH, even at the height of summer. Unfed ticks and those that have recently engorged can acquire water from humid air by ingestion of hygroscopic material secreted by the salivary glands (Kahl & Knülle, 1988). This capability enables the unfed stages to make host-seeking excursions into the upper vegetation where they can lie in wait for hosts for several days before having to descend to the vegetation base in order to rehydrate. Ticks may occur in open areas where there is high rainfall and dense vegetation, such as rough hill-land in the UK and Ireland, and where the main hosts for all instars are usually sheep, cattle or deer. More typical habitats for I. ricinus and other members of the species complex throughout their ranges are deciduous and mixed woodlands, that generally provide the conditions for the free-living phases of the life-cycle and usually also harbour a diverse array of tick hosts.

Host specificity

The three instars tend to occur in different proportions on different hosts. In most regions larvae feed most readily on rodents, nymphs on birds and medium-sized mammals, and adults on large hosts, such as deer. The different instars quest at different heights in the vegetation (Gigon, 1985, Mejlon & Jaenson, 1997), apparently in response to desiccation stress (Randolph & Storey, 1999). This stratified occurrence in the vegetation probably makes a major contribution to instar host specificity, but attachment and feeding preferences are also likely to play a part (Nilsson & Lundquist, 1978). As a result of the wide variety of hosts present in woodland, ticks in this habitat may serve as vectors of several pathogens, some of which cause human disease. All instars of I. ricinus bite humans, but the few studies on this aspect indicate that nymphs are involved more often than either larvae or adult females (Table 2).

Table 2. Proportions of Ixodes ricinus instars infesting humans.

The relative abundance and distribution of nymphs are partly responsible for these statistics, but it is also probable that nymphs are more likely to attach to human skin than are larvae or adult females. However, it is interesting to note that the data from south-west Germany show a much greater proportion of bites caused by adult females than in the UK study. This may be due to sampling bias (general practitioner data compared with data from an on-site clinic in a recreation area), but it is also possible that differences exist in the aggressiveness of different I. ricinus populations to humans. Epidemiological evidence suggests that nymphs of I. scapularis and I. pacificus are also the instar most responsible for human tick bites (Clover & Lane 1995; Falco et al, 1999). Thus nymphs are apparently responsible for most cases of zoonotic disease that these three species transmit (LB, ehrlichiosis, TBE, murine babesiosis). In contrast I. persulcatus nymphs rarely bite humans, and where I. persulcatus transmits LB and TBE most cases are caused by adult females (Korenberg, 1994).

Regulation of seasonal activity 

In order to acquire a host, ticks climb to vantage points in the vegetation and are particularly vulnerable to desiccation during this phase of their life cycle. They can rehydrate by descending to the humid base of the vegetation, but this costs energy and most species appear to time their host-seeking activity to avoid dry or cold periods of the year. In the majority of habitats host-seeking activity is most intense in spring and early summer, with relatively little activity in mid-summer. In some areas a second, usually lower peak of activity, occurs in autumn. This basic pattern is subject to considerable variation, even within local areas, due to the influence of host availability and macro- and microclimate effects (Gray, 1991). For diseases such as bovine babesiosis that can be easily diagnosed and recorded, the seasonal nature of disease transmission by I. ricinus is readily apparent (Fig. 1.).

Appreciable experimental and field evidence is now available to suggest that ticks make use of diapause mechanisms to regulate these periods of host-seeking activity (Belozerov, 1982). The use of diapause can be viewed as a "strategic" approach by ticks responding to appropriate seasonal cues to ensure that host-seeking activity occurs at favourable times of the year. For example, in I. ricinus a behavioural diapause, manifesting as quiescence of newly moulted unfed stages, occurs in ticks conditioned in the previous instar by a long-day photoperiod, and this tends to delay questing until the spring of the following year. Another form of diapause, arrested development (morphogenetic diapause), occurs in eggs, engorged larvae and engorged nymphs and is stimulated by decreasing day length perceived by unfed and feeding ticks that acquire hosts in autumn. This morphogenetic diapause prevents ticks from commencing development in early winter and delays the appearance of the unfed questing stages until after mid-summer. In areas where a significant proportion of the tick population utilizes both forms of diapause, two separate cohorts occur, one feeding in spring and the other (usually smaller) in autumn, with significant interchange occurring between the two (Gray, 1991). Similar diapause mechanisms have been identified in the related species I. scapularis (Yuval & Spielman, 1990) and I. persulcatus (Belozerov, 1982) though there are also minor differences. I. persulcatus displays a more strongly developed behavioural diapause (Kheisin et al, 1955 cited by Balashov, 1972) suggesting that this species is adapted to long harsh winters. In contrast behavioural diapause appears to be entirely absent in I. scapularis, indicating a southern origin for this species, as originally suggested by McEnroe (1984) and supported by recent work on genetic diversity (Norris et al, 1996). Most aspects of the seasonal activity of I. ricinus can also be explained by "tactical" responses of ticks to such ambient conditions as temperature and humidity (van Es et al, 1999; Jensen, 2000; Perret et al, 2000). Such responses constitute the "fine-tuning" of seasonal activity regulation and may be the dominant regulatory process in some tick populations. However, in the absence of studies on development under natural or quasi-natural conditions regulation of seasonal activity by underlying diapause mechanisms cannot be ruled out.

Population variations

It is probable that populations of I. ricinus differ in their propensity to undergo diapause, which may explain variations in results obtained by investigators of this topic. Such differences particularly apply to behavioural diapause, which although well documented in some metastriate ticks (Sonenshine, 1993) appears to be less obvious in I. ricinus, and may, in some regions, be more of a temperature-induced quiescence. There may be regional differences in other aspects of the biology of I. ricinus and although few studies have been conducted so far, there are some indications that differences exist that may affect disease transmission. For example, it is possible that there are regional differences in the readiness of adult female I. ricinus to bite humans (referred to above). There are also data suggesting that a greater proportion of the nymphal I. ricinus population feeds on wood mice (Apodemus sylvaticus) in some European regions than in others (Table 3).

Table 3. Regional differences in I. ricinus larva/nymph ratios on wood mice (Apodemus sylvaticus)

These differences in nymphal infestations may be partly due to habitat characteristics such as air humidity, which affects the questing height of larvae and nymphs (Randolph & Storey, 2000). However, though they were abundant at ground level, nymphs were rarely found on rodents in several Irish woodland habitats (Gray et al, 1999). Since rodents are regarded as important reservoir hosts of several zoonotic pathogens, such differences in nymphal infestations could have profound implications for disease transmission and it is interesting to note in Table 3 that the larva:nymph ratios are inversely related to the proportion of B. burgdorferi-infected wood mice in the same biotopes. These data indicate that nymphs are primarily responsible for transmitting B. burgdorferi s.l. to rodents and differences in nymphal infestations of these reservoir hosts may influence the regional prevalence of the pathogen. For example, infrequent nymphal infestation of rodents has been suggested as a possible reason for the low prevalence of B. afzelii in parts of Ireland (Gray et al, 2000). Variations in susceptibility of different tick populations to tick-borne pathogens may also occur. For example, in a study on the susceptibility to B. afzelii of larvae derived from Spanish, Irish and German I. ricinus females it was apparent that the Spanish ticks were more susceptible (though B. afzelii does not occur in Spain) than either German or Irish I. ricinus (Estrada-Peña et al, 1998). Surprisingly, the German ticks were the least susceptible to this German B. afzelii strain, which was from the same region. Regional differences in the epidemiology of tick-borne diseases are often explained in terms of pathogen behaviour, but these studies suggest that more attention should be given to variations in tick populations. Few attempts have been made to determine intraspecific taxonomic markers in ticks. However, a recent study on cuticular hydrocarbons, which can be useful markers for insect taxonomy, showed the existence of at least 10 distinct I. ricinus groups and a geographical pattern in their distribution (Estrada-Peña et al, 1996). This is in general agreement with an unpublished study of genetic variation of I. ricinus based on analysis of 16S mitochondrial rDNA (Ames et al), which concluded that there is significant intraspecific diversity in I. ricinus from different countries, but that genetic variation within countries is negligible. A similar study on the population genetics of I. scapularis in the USA (Norris et al, 1996) suggested that this species occurs as two clades and their conclusions also support the view (cited above, McEnroe, 1984) that I. scapularis arose in the south. Further research is necessary on the comparative biology of tick populations discriminated by phenotypic and DNA criteria.
 

Tick abundance 

Identification of the factors that determine tick abundance and quantification of their importance is necessary if there is to be any understanding of spatial and temporal differences in questing tick population densities. Tick abundance in any particular habitat is determined by factors such as vegetation cover, climate and weather, which affect the survival and development of the free-living phases, and by the success of host acquisition and feeding by the parasitic phases. The free-living phases are highly dependent on the year-round availability of a humid microclimate and adequate temperatures for development. The optimal habitats in these respects are deciduous woodlands in temperate climates, and such woodlands usually harbour diverse and numerous hosts so that the immature tick instars are rarely limited in their feeding opportunities. However, the adult ticks require large mammals such as deer to feed successfully and produce the next generation, and there are now ample data to suggest that the availability of such hosts has a major impact on the population density of ticks within tick-permissive habitats (Wilson et al, 1984, 1990; Gray et al, 1992; Deblinger et al, 1993). Where the habitat is especially favourable for the free-living phases of the tick life cycle, relatively small numbers of deer can maintain very large tick populations (Robertson et al, 2000). An understanding of the factors that determine the density of tick populations has predictive value for the effects of such phenomena as climate change. In a recent study in Sweden the northward expansion and increased density of I. ricinus between the 1980s and 1990s, resulting in increased incidence of TBE, was examined by Lindgren et al. (2000) and they concluded that these changes were related to warmer winter temperatures. Such a temperature rise could boost tick densities and distribution in several different ways, including longer periods for tick development, increased vegetation growth thus extending tick-permissive habitats, increased host acquisition opportunities in autumn and winter, and better wintering of the main host for adult ticks, the roe deer (Capreolus capreolus). Additionally, roe deer populations in Sweden are thought to have increased in the mid-1980s as a result of reduced predation following a scabies outbreak in the fox population. This study illustrates the complex dynamics underlying tick-transmitted zoonoses and the value of developing good mathematical models for their analysis. It is increasingly evident that a sound knowledge of the biological processes involved in the transmission of these diseases is vital for an understanding of their eco-epidemiology and the full exploitation of predictive models.

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Part of the proceedings of the symposium Current Research on Tick-Borne Infections, Kalmar, Sweden, March 28–30, 2001. © 2001, J. S. Gray, Department of Environmental Resource Management, University College Dublin, Ireland.