The ecology of ticks transmitting Lyme - Review
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Experimental & Applied Acarology, 22 (1998) 249-258
Review
The ecology of ticks transmitting Lyme
borreliosis
J.S. Gray*
Department of Environmental Resource Management, University College Dublin, Belfield 4,
Dublin, Republic of Ireland
(Received November 1996; accepted 6 February 1998)
ABSTRACT
The main vectors of Borrelia burgdorferi sensu lato, the cause of Lyme borreliosis, are ixodid
ticks of the lxodes persulcatus species complex. These ticks, which occur throughout the northern
temperate zone, have very similar life cycles and ecological requirements. All are three-host ticks,
with the immature stages mainly parasitizing small to medium-sized mammals and birds and the
adult females parasitizing large mammals such as deer, cattle, sheep and hares. The host-seeking
stages show a distinct seasonality, which is regulated by diapause mechanisms and there appear
to be major differences in this respect between the Old World and New World species. Most
cases of human borreliosis are transmitted in the summer by the nymphal stages, with the
exception of the Eurasian species, I. persulcatus, in which the adult females are mainly
responsible. The ticks acquire the spirochaetes from a wide variety of mammals and birds but
large mammals do not seem to be infective, so that ticks that feed almost exclusively on large
mammals, for example in some agricultural habitats, are rarely infected. The greatest tick
infection prevalences occur in deciduous woodland harbouring a diver,.se mix of host species and
the diversity of the different genospecies of B. burgdorferi s.1. is also greatest in such habitats.
There is evidence that these genospecies have different host predilections but, apart from the fact
that I. persulcatus does not seem to be infected by B. burgdorferi sensu stricto, they do not seem
to be adapted to different tick strains or species.
Exp Appl Acarol 22:249-258 (C) 1998 Chapman & Hall Ltd
Keywords: Lyme borreliosis, spirochaete, genospecies, tick ecology, diapause, host require-
ments, life cycle.
THE DISEASE
Lyme borreliosis is caused by the spirochaete Borrelia burgdorferi and is trans-
mitted by ixodid ticks, particularly those of the Ixodes persulcatus species complex.
The symptoms of the disease, which include skin, nervous system, heart and joint
manifestations, are usually non-specific and often mimic other diseases. Lyme
borreliosis took several decades to emerge following the first documented descrip-
tion of the symptoms in Europe in 1883 (Buchwald, 1883). The causal agent, B.
burgdorferi, was eventually discovered in Ixodes ticks and found to be the cause of
a tick bite-associated epidemic of arthritis in the town of Old Lyme, Connecticut,
* To whom correspondence should be addressed at: Tel: 353 269 3244; Fax: 353 283 7328; e-mail:
jgray@ macollamh.ucd.ie
0168-8162 (C) 1998 Chapman & Hall Ltd250 J.S. GRAY
US (Burgdorfer et al., 1982). In the following year the same organism was found
in the common European tick, lxodes ricinus (Burgdorfer et al., 1993).
Lyme borreliosis is now considered to be the most prevalent arthropod-borne
human disease in Europe and the US and also occurs fight across temperate Asia.
Although rarely fatal, the disease can cause severe debilitation in untreated chronic
cases and an accurate early diagnosis is required for satisfactory treatment. The
non-specific nature of the symptoms together with the problems associated with
reliable serodiagnosis of the disease can make this difficult to achieve. Effective
prevention is therefore highly desirable and a thorough understanding of the
ecology of the tick vectors is necessary for the effective implementation of
preventive measures.
LYME BORRELIOSIS VECTORS
Although a considerable number of tick species have been reported as carriers of B.
burgdorferi, the presence of the spirochaete in unfed host-seeking ticks does not
necessarily mean that they are capable of transmitting it to new hosts. In fact there
is unequivocal evidence for vector competence in only eight species of ticks, all of
which are Ixodes spp. and four of which, the major vectors, belong to the I.
persulcatus species complex (Table 1). Some of these, such as Ixodes dentatus,
Ixodes neotomae and Ixodes spinipalpis in the New World and lxodes hexagonus in
the Old World, seem to be involved in enclosed enzootic cycles and may have an
important role in the maintenance of the spirochaetes in nature. The specialist
European rodent tick, Ixodes trianguliceps, may also have this role and although
spirochaetes have been found in specimens of this tick (Gorelova et al., 1996),
transmission has not been demonstrated. The role of Ixodes uriae, which infests
seabirds and consequently has a global distribution is uncertain. While it almost
certainly transmits a genospecies of B. burgdorferi (Olsen et al., 1993) and also
bites humans, no disease has so far been associated with this tick. The intrusion of
TABLE
Species of ixodid tacks capable of transmitting B. burgdorferi
Species Distribution Role Hosts
I. persulcatus Eastern Europe and Major vector Many
temperate Asia
I. ricinus Northern Europe and Major vector Many
North Africa
I hexagonus Europe Enclosed enzootic cycle? Hedgehogs (carnivores)
I scapularis (dammini) Eastern north America Major vector Many
I pacificus Western north America Major vector Many
I. dentatus North America Enclosed enzootic cycle Rabbits
I neotomae Western north America Enclosed enzootic cycle Wood rats, and deer
I. spinipalpis Westem north America Enclosed enzootic cycle Mice, and deer
I. uriae Worldwide Unknown SeabirdsTHE ECOLOGY OF TICKS TRANSMITTING LYME BORRELIOSIS 251 human-biting bridge vectors, such as the members of the I. persulcatus complex, into enclosed enzootic cycles is an important factor in the appearance of zoonotic disease. Four members of this species complex, I. persulcatus and I. ricinus in the Old World and Ixodes pacicus and Ixodes scapularis (dammini) in the New World are significant vectors of Lyme borreliosis and their distribution is a good indication of the geographical distribution of the disease (Fig 1). There are, however, areas where Lyme borreliosis is rare, despite the presence of vectors. A good example of this situation is in the area inhabited by I. scapularis in the southern states of the US. This tick is distributed throughout the eastern seaboard of the US extending to the southern coast, but cases of Lyme borreliosis occur mainly in the north eastern states. Until recently, it was thought that another vector species, Ixodes dammini, was responsible for these cases, but this species is now considered to be conspecific with I. scapularis (Oliver et al., 1993). Southern races of I. scapularis have been shown to be efficient vectors of B. burgdorferi in the laboratory (Piesman and Sinsky, 1988) and reasons other than vector competence must be sought for the relative rarity of Lyme borreliosis in the southern states of the US. In Europe, Lyme borreliosis is rarely reported from the south eastern Mediterranean countries, although I. ricinus is apparently present, as is another member of the I. persulcatus species complex, Ixodes gibbosus, which is of unknown vector competence for B. burgdorferi. TICK HABITATS The habitats utilized by the I. persulcatus complex ticks that transmit Lyme borreliosis are determined by the sensitivity of these ticks to desiccation during the Fig. 1. Global distribution of major vectors of Lyme borreliosis (shaded area).
252 J.S. GRAY non-parasitic phases of their life cycle and also the availability of suitable hosts. All four species are three-host exophilic ticks with an ambush strategy for host acquisition by questing on vegetation. The ticks are vulnerable to desiccation during this questing phase, which may last for several weeks and also during the prolonged development phase, in which they locate on or near the soil surface while they are transforming to the next instar or, in the case of adult females, laying eggs. In both the questing and developing phases ticks can obtain water from sub- saturated air by secreting and then reingesting hygroscopic fluid that is produced by the salivary glands (Kahl and Kntille, 1988). This activity enables the ticks to maintain a stable water balance as long as the relative humidity of their micro- climate does not fall below 80% for any length of time. These ticks can therefore only survive in areas where a good cover of vegetation and a mat of decaying vegetation occur so that the relative humidity at the base of the vegetation remains above 80% throughout the driest times of the year, usually the summer. However, some habitats can also be too wet and the ticks will not survive in areas that are flooded for extended periods in winter. The host requirements of these ticks are best met by a diverse mix of fauna, but a minimal requirement is that a significant number of large animals, such as deer, should be present in order to feed the adult female ticks, which, with few exceptions, only engorge successfully on animals larger than a hare (Lepus spp). The larvae and nymphs are more catholic in their host preferences and, in addition to the larger hosts, can feed on smaller mammals and on birds. The large hosts that feed the adult ticks are the main determinants of tick abundance in tick-permissive habitats (Gray et al., 1992) and this is probably mainly due to their necessity for adult tick reproduction. They may therefore be termed 'reproduction' hosts, as distinct from 'reservoir' hosts, which refer to those that permit long-term survival and amplification of the infection and are significantly involved in the infection of the ticks. A reproduction host may also be a reservoir host, as is the case with hares (Tilleklint and Jaenson, 1993) and hedgehogs (Gray et al., 1994), but the most important reproduction hosts, for example deer and cattle, do not seem to be reservoirs (Gray et al., 1992, 1995; Jaenson and Tilleklint, 1992). In some areas, small populations of ticks can persist in the absence of the large reproduction hosts. Although less obvious reproduction hosts such as hedgehogs are sometimes involved, these tick populations seem to be maintained by birds which acquire infestations of the larvae and nymphs from surrounding areas and deposit engorged ticks in the habitat. They are usually characterized by relatively small numbers of nymphs and adults and an absence of larvae and are typically found in areas which are not accessible to deer, such as certain islands (Kirstein et al., 1997). The microclimate and host requirements of the Lyme borreliosis vector ticks mean that in most of their range they are found in deciduous woodland, particularly those containing oak and beech, harbouring significant numbers of large animals, such as deer, However, the ticks will also survive in coniferous forest as long as there is sufficient litter on the ground and the climate is moist. In some areas ticks
THE ECOLOGY OF TICKS TRANSMITTING LYME BORRELIOSIS 253 may be found in large numbers in meadows and on open hillside. These areas are characterized by rough vegetation and high rainfall and the major hosts involved are usually livestock such as cattle and sheep which feed all stages of the ticks. THE SEASONAL ABUNDANCE OF TICKS The life cycles of the members of the I. persulcatus species are very similar, differing mainly in the seasonal activity of the unfed stages. The following account refers particularly to the European vector, I. ricinus. Each stage (larva, nymph and adult female) feeds for a few days and then detaches and develops in the vegetation to the next stage, a process that takes approximately 1 year. Both the questing and developing stages are sensitive to desiccation and require a relative humidity of at least 80% throughout the year, so that they are confined to areas where a good cover of vegetation and a mat of decaying vegetation are present. A distinct seasonality in host seeking occurs and in the case of I. ricinus this consists of a large spring- and early summer-feeding population and a smaller one active in the autumn (Gray, 1991). This temporal abundance of host-seeking ticks is strongly influenced by the seasonal availability of suitable hosts, but the primary factor in determining seasonality is diapause. Diapause in ixodid ticks can occur at several different life cycle stages and may manifest in different ways (Belozerov, 1982), but may be categorized as (1) behavioural diapause, involving a form of quiescence of the unfed ticks at a time when environmental conditions are unsuitable for host seeking or (2) developmental diapause, involving arrested development of the engorged stages or of eggs. The most important entrainment stimulus seems to be day length, though temperature may have a modifying influence. The diapause mechanisms seem to enable the ticks to avoid entering host-seeking phases at unfavourable times of the year, such as high summer and midwinter and the proportion of the population that exhibits them will vary according to local conditions. Thus, areas which have hot summers and cold winters are most likely to show both forms of diapause in the majority of the population. They help to explain the extremely flexible life cycle of these ticks, which may take 2-6 years for completion and also the highly variable patterns of seasonal activity. For I. ricinus and I. persulcatus a behavioural diapause prevents spring- and early summer-feeding cohorts from feeding again that year even though they will have moulted in late summer. This is most marked in the adult ticks but the proportion exhibiting this behaviour may vary in different areas. This applies particularly to I. ricinus, which in western regions frequently shows some autumn adult activity of the spring-feeding nymphal cohort, thus giving rise to autumn-active populations. In the case of I. persulcatus, this behavioural diapause is further developed in that even adults that have moulted in late summer from the previous year's autumn- feeding nymphal cohort do not become active until the following spring (Balashov, 1972). A developmental diapause is utilised by./. ricinus and I. persulcatus that feed in the autumn and this prevents the engorged ticks from proceeding with their
254 J.S. GRAY development through the winter months. The eggs, larvae and nymphs of both species exhibit a developmental diapause, but this has not been detected in the adults, which continue to lay eggs throughout the winter whenever the temperatures are high enough. The ticks in this form of arrested development may be quite mobile and overwinter as engorged stages, continuing with their development in early summer of the next year and moulting or hatching in the case of eggs in late summer or early autumn. These newly moulted ticks usually become active within 1-2 weeks except in the case of I. persulcatus in which the adults then seem to enter a behavioural diapause (Balashov, 1972) as mentioned above. The role of diapause in the life cycles of the New World species I. pacicus and I. scapularis are less clear. From the few studies carried out it would appear that the main difference between I. scapularis and the Old World species is the absence of a behavioural diapause in adults that moult in late summer (Yuval and Spielman, 1990). These adult ticks thus become active in the autumn even though in many parts of their range the winter climate is harsh. This would appear to support the suggestion that the northern race, formerly known as I. dammini, is a relatively recent extension of the southern race of I. scapularis (McEnroe, 1984). A nymphal developmental diapause is thought to occur, but its significance is not known. An ovipositional diapause rather than an egg diapause has also been reported (Yuval and Spielman, 1990). The published life cycle of I. scapularis is extremely simple compared with those of the Old World species and it is curious that such closely related species inhabiting similar biotopes on different continents appear to have evolved very different life cycle strategies. More studies under quasi-natural conditions on developing ticks of all four species are required to resolve this apparent anomaly. THE TRANSMISSION OF LYME BORRELIOSIS Much remains to be learned about the details of Borrelia burgdorferi transmission, but some facts are now well-established. In most unfed ticks, the spirochaetes inhabit the midgut and during feeding they penetrate the midgut wall and trans- locate to the salivary glands via the haemolymph. They then pass into the feeding lesion with the saliva. The migration of spirochaetes from the gut to the salivary glands during feeding means that most infections do not take place for at least 2 days after attachment; however, in a proportion of unfed ticks the spirochaetes are already present in the salivary glands and transmission can take place much sooner (Korenberg et al., 1994; Leuba-Garcia et al., 1994). At one time regurgitation of the gut contents into the feeding lesion was considered to be possible and could explain early transmission, but so far no convincing evidence has appeared to support this hypothesis. Trans-stadial transmission (stage to stage) rather than transovarial transmission (from an infected female to her eggs) normally takes place so that the infection is usually acquired from a reservoir host by the larvae or nymphs, and transmitted by the nymphs or adults. Transovarial transmission is uncommon and the larval infection rates are usually less than 1% so that the larvae
THE ECOLOGY OF TICKS TRANSMITTING LYME BORRELIOSIS 255
are considered to be a significant source of infection for humans. However, in
not
an attemptto explain the fact that in Europe rodents seem to become infected
despite feeding few infecting nymphs, it has been suggested that transovarial
transmission may have a considerable role in maintaining the circulation of the
spirochaete in nature (de Boer et al., 1993). So far no consistent experimental
transmission of spirochaetes by the larvae has been shown and the precise role of
rodents in the circulation of spirochaetes between the hosts and ticks remains to be
determined.
The prevalence of infection in the nymphs and adults is highly variable, ranging
from 0 to more than 50%, with the adults generally showing the higher infection
rate in a particular habitat, presumably because they will have had the chance to
become infected at both the larval and nymphal stages and also possibly because of
co-feeding transmission (see below). In the cases of I. pacificus and I. scapularis,
most human cases of Lyme borreliosis seem to be caused by the nymphs, which are
much more abundant than adults and are also less readily detected while feeding. In
the case of I. persulcatus, human infections are caused mainly by the adult ticks
apparently due to the relative lack of aggression of the nymphs of this species
(Korenberg et al., 1994). I. ricinus nymphs readily bite humans and it is assumed
that they are responsible for most cases; however this is not obvious, because their
feeding activity is concurrent with that of the adults and no detailed studies seem to
have been carried out on this aspect.
THE ABUNDANCE OF THE TICK HOSTS
The abundance of infected ticks in a particular habitat, which is a measure of
infection risk, is determined by the interaction of the abundance of reproduction
hosts and that of reservoir hosts. All of the significant reproduction hosts studied so
far, such as deer, cattle and sheep, seem to have little if any role in the maintenance
of infection in ticks (though the significance of co-feeding where infected ticks may
infect uninfected individuals feeding simultaneously on any host remains to be
assessed). These reproduction hosts can therefore be responsible for the generation
of very large numbers of uninfected ticks in a particular habitat and the proportion
of infected ticks may be very low where reservoir hosts are scarce or where
reproduction hosts are very common. The latter situation is typical of farm
situations where the majority of ticks of all stages are fed by livestock (Gray et al.,
1995). Where reservoir hosts are abundant, the density of reproduction hosts may
have more effect on the absolute number of infected ticks than on the proportion of
ticks that are infected. This situation seems to occur in many forested habitats with
a rich mix of fauna..In such situations the abundance of infected ticks is likely to
be consistently proportional to the overall abundance of ticks in the habitat
(Tilleklint and Jaenson, 1996). This is more likely to occur if the immature stages
of the ticks show a greater predilection for small mammals and birds than for the
larger reproduction hosts and this probably occurs to differing extents in different
geographical populations of particular tick species.256 J.S. GRAY Since the abundance of reservoir hosts in a habitat is crucial to the establishment of infected tick populations it is important to identify both the presence of particular reservoir hosts in a habitat and also their role in generating infected ticks. This is extremely difficult in that it is necessary to calculate their contribution to both the tick and spirochaete populations and this may change over time. At present, it is only possible to obtain estimates of the role of a particular reservoir host species by extrapolation from laboratory data on the infectivity of that host for ticks and from field data on the infestation rate of that host relative to the abundance of unfed ticks. At present, it is apparent that many species of rodent (e.g. Apodemus, Cleth- rionomys, Microtus and Peromyscus) can serve as reservoir hosts and, since they are plentiful in most woodland habitats, they are generally thought to be the most important source of infection for ticks. However, it is also known that many medium sized animals that share the habitat with such animals, such as chipmunks (Tamia), squirrels (Sciurus) and hedgehogs (Erinaceus), while less numerous, frequently carry far more ticks and may even be more significant as a source of infection than mice and voles in some habitats (Craine et al., 1995). Furthermore, it has recently become apparent that several woodland bird species such as pheasants (Phasianus) (Kurtenbach et al., 1998) and blackbirds (Turdus) (Humair et al., in press; Wallich and Gem, in press) may be of significance as reservoir hosts. Licensing problems make it much more difficult to assess the role of such species by trapping (followed by the harvesting of engorged larvae or by xenodiag- nosis), as commonly used for rodents. However, a recently developed test for the identification of hosts responsible for the infection of unfed nymphs by the analysis of blood meal remnants (Kirstein and Gray, 1996) may provide a means of resolving the situation in particular habitats. GENOSPECIES OF B. BURGDORFERI The nature of the circulation of spirochaetes between hosts and vectors has recently become much more difficult to understand and analyse with the realization that the species B. burgdorferi in fact consists of several genospecies (Postic et al., 1994). Only one of these, B. burgdorferi sensu stricto, has been implicated as the cause of disease in North America, but in Europe three genospecies, Borrelia afzelii, Borrelia garinii and B. burgdorferi s.s., are known to be pathogenic and still others such as B. lusitaniae (formerly potiB2) (Le Flech et al., 1997) and B. valaisiana (formerly VS116) (Wang et al., 1997) and are of unknown pathogenicity at present. There are some indications that these different genospecies cause different disease manifestations, for example B. garinii is usually associated with neuroborreliosis, B. burgdorferi s.s. with arthritis and B. afzelii with a degenerative skin condition (acrodermatitis chronica atrophicans); however, this is not clear-cut and there seems tobe considerable overlap (van Dam et al., 1993). The different genospecies may also have varying predilections for different reservoir hosts, for example B. garinii seems to have a special association with birds and B. afzelii with rodents (Olsen et al., 1993; Humair et al., 1995). Borrelia burgdorferi s.s. is commonly found in
THE ECOLOGY OF TICKS TRANSMITTING LYME BORRELIOSIS 257
both. Once again there seems to be a lack of definition in these host preferences.
Different genospecies have not been associated with particular tick strains or races,
but it is interesting to note that so far B. burgdorferi s.s. has not been isolated from
I. persulcatus (Korenberg, 1994).
There is no doubt that very much more work is required before a satisfactory
understanding of the circulation of B. burgdorferi s.1. is reached and at present the
increasing knowledge of the subject seems to be creating more questions than
answers.
ACKNOWLEDGEMENT
This manuscript was presented at the Third Symposium of the European Associa-
tion of Acarology (EURAAC) which was held on July 1-5, 1996 in Amsterdam,
The Netherlands.
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