The dog factor in brown dog tick Rhipicephalus sanguineus (Acari:Ixodidae) infestations in and near human dwellings

InU. Med. Microbiol.291 , Suppl. 33, 156·163 (2002) © Urban & Fischer Verlag http://WW1v.urbanlischer.de/journalslijmm

original article The dog factor in brown dog tick Rhipicephalus sanguineus (Acari:lxodidae) infestations in and near human dwellings Igor Uspensky' *, Inna loffe-Uspensky-

1 2

A. Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Israel Department of Parasitology, The Hebrew University-Hadassah Medical School, Jerusalem, Israel

Abstract Three cases of the tick Rbipicephalus sanguinous infiltration in or near human dwellings caus ed by dogs, and their influence on epidemiological features of human habitats have been investigated. (a) The observation of dogs kept indoors proved that single tick females could engorge and o viposit inside apartments followed by the development of subadulrs. (b) Abundant micropopularions of ticks were formed in small yards or gardens ncar the dwellings where dogs lived in kennels. (c) A huge field population of R. sanguinous was ob served on a farm where watchdogs constantly patrolled along the farm perimeter. Tick abundance ncar the kennels and in the permanent resting sites of the dogs reached more than 30 adults per 10 min of collecting, while the number of adults on a dog reached 100. Unfed adult females under cond itions of constant dog availability had a larger scuta I index than female s collected in the control field site. On the basis of circumstantial evideuce it is possible to conclude that under the above conditions tick development may change from the normal 3-host cycle to a 2-host cycle. Ticks in the field had one complete generation per year. Ticks on the farm, as well as ticks in kennels, developed faster and a significant part of their population had two complete generations per year. R. SCIIlgllillCIIS is the main vector and reservoir of a pathogen from the Rickettsia conorii complex, the causat ive agent of Israeli tick typhus. The described conglomerations of R. SCIIlgllillCIIS create a great risk to humans who can be attacked by infected ticks in and around their homes, even in large towns. Such a feature of the tick life history most likely exists not only in Israel bur in other countries as well. Key words: Rhipicephalus sanguineus - indoor ticks - tick conglomerations - scuta I index physiological age - life cycle - Israeli tick typhus

Introduction Pets have a large variety of ectoparasires that may be a source of various human infections. During the last decades the desire of people to possess pets has sharply increased. Pets carry their parasites irrespective of whether they live outdoors or indoors. Moreover, unmanaged expansion of suburbs into undisturbed environments may lead to the association of new parasites

with the pets and, hence, with human habitations. It was noted that cat owners in the U. S. A. suffer more often from Lyme disease and arc more often attacked by nymphal Ixodes scapularis, the main vector of the disease pathogen, than people without cats (Steere et al., 1978; Curran and Fish, 1989). Dogs have been implicated as an important link in the transmission of Rickettsia rickettsii, the causative agent of Rocky Mountain spotted fever, to man by Dermacentor uari-

(. Corresponding author: Igor Uspensky, Department of Biological Chemistry, A. Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel, Phone: 0097226586525; Fax: 0097226519597; E-mail: [email protected] 1438-4221/01/291/8-000 515.00/0

Dog factor in tick infestation

abilis (Fiset et aI., 1981), even in urban areas (Gratz, 1999). Cats and dogs infested with fleas have become a significant factor in the emergence of flea-borne rickettsioses in the U. S. (Azad et aI., 1997). Thus, closeness with pets creates additional epidemiological problems to humans. The cosmopolitan brown dog tick Rhipicephalus sanguineus is widely spread in all Mediterranean countries and is one of the main tick species in Israel (Feldman-Muhsam and Saturen, 1961; Theodor and Costa, 1967). This tick is the main vector and reservoir of a specific strain of the Rickettsia conorii complex, the causative agent of Israeli tick typhus closely related to Mediterranean spotted fever (Roux and Raoult, 1999). R. sanguineus is also the vector of Ehrlicbia canis, the causative agent of canine ehrlichiosis (Keysary et aI., 1996). Recently this tick was referred to as a potential vector of human monocytic ehrlichiosis (Keysary et aI., 1999). In Israel this tick lives not only in the field but also in towns where it is responsible for a significant number of Israeli tick typhus cases (Wilamowski et al., 1999). The goal of our observations was to show that the conditions of dog habitation, created by humans, may change the biology of this tick vector and thus render it more dangerous for both humans and dogs.

Materials and methods When we inspected dogs for adult Rhipicephalus sanguinetts, their ears, heads and necks as well as chests and bellies were examined. Depending on the size of the dog and on the number of ticks found, the examination of a dog took from 5 to 15 min. In the apartments where dogs were kept indoors, the bedding as well as the floor, walls and furniture around the bedding area were thoroughly examined. In the gardens, ticks were collected from the dogs and their kennel bedding as well as by dragging the lawn around the kennel. On the farm and in the field, ticks were collected by dragging the vegetation as well as by hand from the grass and clothes of the collectors. The life history of ticks living near human dwellings and in the field was estimated according to their physiological age (reviewed by Uspensky, 1995). To determine the tick physiological age, unfed females were weighed and the length and width of their scutum were measured with the aid of an ocular-micrometer. The scutal index, produced by multiplication of the scutal length by the scural width (McEnroe, 1974), directly correlates with the weight of ticks after molting and reflects the nymphal feeding success. The ratio weight/scural index allows the estimation of the physiological age of R. sanguineus according to our novel methodology (unpublished). The methodology is based on the gradual decrease of this ratio during tick starvation since the first parameter (weight) gradually diminishes its value while the value of the second (scutal index) remains constant. The age was estimated according to Balashov's schedule where four age

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groups were distinguished in unfed ticks (Balashov, 1972; Uspensky, 1995). The significance of the difference between mean values of the scutal indices or the ratio weight/scural index in ticks from different locations or in different months was estimated using Student's r-test. We limited our statistical operations by r-test without first doing an overall test with ANOVA. The maintenance conditions of a laboratory colony of ticks, from which some data were used for comparison, were described by Ioffe-Uspensky et al. (1997). Five longhaired indoor dogs whose owners complained to us about ticks in their apartments were observed. The owners lived in many-story buildings in several Israeli towns. In accordance with our instructions, the owners examined their dogs after walking, while we examined the dogs and the apartments for tick infestations monthly, from May until September. Five other dogs were observed in small yards or gardens of Jerusalem with lawns and wild vegetation where the dogs had a kennel. The qualitative observations were also carried out monthly during May-September. In a garden of about 200 m 2 where a German shepherd dog could freely walk, unfed adult ticks were collected in July from the dog and from the kennel, as well as by dragging the lawn around the kennel. In the Results section we will mainly present the data of our own observations and investigations, adding special remarks if the dog owners had obtained the data. During the course of a year we also observed a farm guarded by dogs in the central part of Israel. The farm of about 5 acres included the owner's house and had a rectangular shape. There was no wild vegetation on the territory of the farm and the soil was sandy. Along the farm perimeter was a belt of grass between the farm fence and a sandy road which was periodically interrupted by sandy spots. Some watchdogs patrolled outside the perimeter fence moving along a wire while the others could walk freely around the farm. The farm examinations were made in mid-April, midJuly, and late-September and included the collection of ticks on the dogs and from vegetation near the fence. The wild vegetation about 600-800 m from the farm fence was also dragged. At the same times of the year we also collected ticks in the control field site, approximately 60 km south of the farm. This site was chosen because of its previous use in investigations concerning R. sanguineus biology (Mumcuoglu et al., 1993a; b). \Ve were unable to continue our observations the following year because the owner treated all dogs and the territory outside the fence with chemicals.

Results Ticks in human dwellings In spite of regular checking of the dogs after walking by the owners, single adult Rhipicephalus sanguineus always remained undetected among the dog hairs. Some of the ticks left the dogs when they scratched themselves or rubbed against the furniture or the floor, and later these ticks were found in all 5 apartments either on people or elsewhere. In 4 out of 5 apartments, partially or fully engorged females were found and removed from the dogs by the owners or during our reg-

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Table 1. Data onticks found inside apartments where dogs were kept indoors during thesummer season. Dog breed

locality

Years of observation

Sites of dog walking

Findings of unfed adult ticks indoors 1

engorged females ondogs 2

engorged nymphs onwalls!

Chow Chow

Jerusalem

6

Invarious sites

+

++

++

Bobtail

Jerusalem

6

Invarious sites

+

++

++

Airedale

Jerusalem

6

Mainly in a park

+

+

Mongrel

Ramat-Gan

3

In a forest and uncultivated fields

+++

++

Mongrel

Rehovot

3

Invarious sites

+

1

2 3

+ single cases (0-3 ticks annually); +++ numerous cases (> 5 monthly); - nocases; + single cases (0-1 tickannually); ++ several cases (0-5 monthly); - nocases; ++ several cases (0-3 times annually).

Table 2. Abundance of adult R. sanguineu5 in a Jerusalem garden, onthefarm and in thefield. locality

Time of collecting, month

Total number of adults collected I

Duration of collection, min

Density of adults, ticks/10 min/man

Jerusalem, A garden with 1 dog

July

47

15

15.7

Central part of Israel, a farm with 8 dogs

April July September

96 70 92

15 10 15

32.0 35.0 30.7

Northern Negev, control field site

April July September

32 41 49

90 60 90

1.8 3.4 2.7

1

All collections were carried out by2 persons.

ular inspections (Table 1). In 2 apartments successfully engorged females regularly dropped off indoor (Table 1). According to our as well as the owners' observations, the main sites of their location after dropping off were under or near bedding or sofas where dogs rested and slept. The owners gave us 15 fully engorged females while we collected 6 such ticks. The owners also informed us about several engorged females that were unexpectedly crushed. Undetected females oviposited (4 of the 6 engorged females we observed were at different stages of oviposition). Unfed or engorged larvae as well as unfed nymphs were never observed. Only engorged nymphs could be seen migrating upwards over the walls.

Ticks near human dwellings A great number of unfed adult ticks were found all over the kennels in yards or gardens and in small holes in the soil next to the kennels. Ticks were also found on wild vegetation in the yards. If the kennel was near a house, engorged nymphs could be seen forming clus-

ters in small cracks or depressions on the outside walls of the house, having migrated upwards over the walls. Unfed larvae, engorged larvae and unfed nymphs were never observed. On the farm, unfed Rs sanguineus were found in great numbers in and near the kennels and on the spots of grass in the permanent resting sites of the dogs during all three examinations. Only in July clusters of unfed larvae were collected several times from the grass. The results of tick collection in a Jerusalem garden, on the farm and in the control field site are presented in Table 2. Several points should be indicated. The first is connected with the methodology of tick collection. In the control site in April only single ticks were collected by dragging while many groups of adults positioned on the top of grass were collected by hand. In all other cases ticks were collected by dragging and by hand in order to obtain comparable data. Secondly, in July, the relative tick density in the garden near a human dwelling was approximately five times higher than in the field, while near the farm it was approximately one order of magnitude higher than in the field. Thirdly, the

Dog factor in tick infestation

relative tick density on the farm varied only slightly throughout the summer season (April through September). In the control site, the tick density in July was higher than in April and slightly higher than in September. Among ticks collected on vegetation at some distance from the farm, adult R. turanicus comprised up to 50 % in April and 15 % in July, but were never found on the dogs or near the farm. The abundance of ticks of both species in that area was between 7 and 16 adults per 1 km from mid-April until late-September (only R. sanguineus was collected in September). The mean number of adult ticks found attached to dogs on the farm was 64 ± 18 (SD) specimens/dog. Its maximal number was reached in July which was insignificantly lower in April and September. The maximal number of adults found attached to a dog in the garden in July was 15 specimens and on the farm at the same times about 100 specimens/dog. In April many unattached unfed adults, both males and females, were collected on the farm from the dogs where they moved about on the fur but made no attempt to attach. It was impossible to count them.

Scutal index values for ticks of different groups The mean scutal indices of unfed females from the control field site (Table 3) did not differ seasonally (maximal value of t = 0.83) which indicates an insignificant difference in the weight of unfed females after molting during the whole summer. As for the farm population, there was a significant difference between the scutal index of ticks in September (maximal value) and that of ticks in July (t = 2.33, P < 0.01) but not with that of ticks in April (t = 1.05). The mean scural index of unfed females from the garden measured only in July (Table 3) was significantly higher than that of the field ticks in April (t = 3.34, P < 0.001) but insignificantly

higher than that in July and September (t = 1.38, P < 0.3; and t = 1.6, P < 0.18, respectively). The scutal index of the garden ticks was significantly higher than that of the farm ticks in July (t =2.2, P < 0.05), insignificantly higher than the scural index of the farm ticks in April (t =0.86) and slightly lower than that in September (Table 3). Comparing the scural indices between the field and farm populations by particular months, we found that the farm ticks had insignificantly higher indices in April and September (t = 1.44, P < 0.25 and t = 1.75, P < 0.08, respectively) and a slightly lower index in July. In all cases, the mean scuta I indices of the farm, garden and field ticks were significantly lower than that of the ticks from the laboratory colony (t =5.26, P < 0.001 for maximal value of the index in the farm population in September and 1-month-old colony ticks) (Table 3).

Physiological age of ticks from different groups The ratio weight/scuta I index in unfed females was always higher in the farm ticks than that in the field ticks at the same time (Table 4). In April and July the differences were highly significant (t =4.19, P < 0.001 and t =3.04, P < 0.01, respectively). In April, the field ticks were physiologically very old (overwintered) (more than 75 % of ticks were of the very late 3rd and the 4th physiological age with a weight/scuta] index ratio < 1.2). Only single ticks adhered to the flag while dragging, but the majority of ticks were observed on the top of grass and were collected by hand (see above). The farm ticks were very young, some of them being of the 2nd physiological age (ratio> 2.3). In September the difference was insignificant (t = 1.56, P < 0.17). Comparing these ratios for ticks from the same location collected at different times (Table 4) we can see

Table 3. ScutaI indices of adult female Rhipicephalus sanguineus from different groups. Group of ticks

Time of measuring

No. females measured

Scutal indices (in rnm/) Mean ± SD'

Range

laboratory colony

1 month after molting

38

1.977 ± 0.185a

2.397-1.451

Control field population

April July September

28 25 25

1.577 ± 0.21b 1.625 ± 0.21bc 1.618 ± 0.19bc

1.966-1.079 1.933-1.049 2.130-1.194

Garden micropopulation

July

25

1.701 ±0.18c

2.170-1.161

Farm population

April July September

25 40 25

1.656 ± 0.19bcd 1.602 ± 0.17bd 1.714 ± 0.20bc

1.977-1.151 1.933-1.314 2.150-1.266

1

159

Significant differences are marked bya different letter (Student's t-test, P<0.05).

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Table4. Physiological conditionsof unfed females from field and farm populations. Month

No. ticks

Values ofweighUscutal index ratio 0.8<

0.8-1.0

1.0-1.2

1.2-1.4

1.4-1.6

1.6-1.8

> 1.8

Mean ±SD1

% ticks witha given value ofweighUscutal index ratio

Field ticks IV VII IX

28 25 25

Farm ticks IV VII IX

25 40 25

1 1

25.0

14.275 4.0 8.0

39.3 48.0 68.0

21.425 36.0 12.0

12.0 12.0

32.0 20.0 44.0

48.0 47.5 48.0

12.0 25.0 4.0

1.015 ± 0.19a 1.215 ± 0.15b 1.172 ± 0.14b 8.01 7.5 4.0

1.345 ± 0.35c 1.330 ± 0.15c 1.225 ± 0.1 Db

Significant differences are marked bya different letter (Student's r-test, P< 0.05). weighUscutal index ratio inthe limits 2.3-2.5 .

that physiologically old females in the field in April significantly differed from much younger females in July (t =4.26, P < 0.001). Females in September did not significantly differ from those in July (t = 1.05) but were also significantly younger than females in April (t =3.44, P < 0.001). On the farm, the ratio weight/scutal index in ticks in April and July was rather similar (t = 0.2) but it was significantly higher when compared with ticks in September (t = 3.5, P < 0.001 comparing July and September ticks) . This means that from April to July the farm population continues to be physiologically rather young, but significantly ages by September. At the same time, the farm population has been younger than the field population at any month of study.

Discussion Humans acquiring pets are at risk of bringing ticks into their apartments or creating tick conglomerations ncar their dwellings. It was shown on a kibbutz near our control field site that the prevalence of Israeli tick typhus cases was 5 times higher among people having dogs than among people without dogs (Mumcuoglu et al., 1993a). People usually interrupt tick development when they detect engorged nymphs on the walls of their rooms. However, several cases of long-existing domestic rnicropopularions of Rhipicephalus sangttinells brought indoors by dogs were described in the literature. In some cases it was connected with the introduction of dogs infested with R. sanguineus outside the tick range, in Denmark (Haarlov, 1969), in Poland (Szymanski, 1979) and in Switzerland (Peter et al., 1984); in the latter case 4 people were infected with Rickettsia conorii by ticks indoors. Gilot et al. (1992)

observed numerous unfed and engorged adult R. sanguineus and their eggs in a Marseille suburb apartment where a dog came to stay overnight. Recently, the number of dogs in Israel has dramat ically increased (our unpublished observation). Under these conditions the probability of infection by Israeli tick typhus in or near human dwellings becomes rather high. Clusters of cases have been reported, e. g. among children who played on a lawn frequented by dogs (Shazberg et al., 1999). Increased dog infestation by ticks is hazardous for the dogs as well. During th e period of our observation, 3 out of 8 dogs on the farm died, supposedly from canine ehrlichiosis. The postmolting development of larvae after hatching takes a very short time (1-3 days according to Ioffe-Uspensky [unpublished)). Because of the very small size of larval R. sanguineus (Uspensky et al., 1999), it is almost impossible to find them attached to the dogs. The period of larval postmolting development is rather short (about 2 weeks at 24°C) (IoffeUspensky et al., 1997) and in dog hair at higher temperature it might be even shorter. Taking these data into account together with the failure of our numerous attempts to find unfed or engorged larvae and unfed nymphs of R. sanguineus indoors, we suggest that unfed larvae attached to dogs and after feeding did not leave the dogs but molted into nymphs that fed on the same dogs. This means that indoor R. sanguineus, at least a great portion of them, might develop according to the 2-host cycle. The lack of findings of engorged larvae in the gardens suggests that the 2-host developmental cycle occurs in the majority of the tick micropopulations too. On the farm where the environmental conditions are close to natural field conditions, tick development might be rather similar to the normal 3-host cycle. However, detailed analysis of the data

Dog factor in tick infestation

presented by Mumcuoglu er al. (1993a) indicates strong circumstantial evidence of the 2-host developmental cycle in some part of the field population. The number of unfed nymphs collected by the authors in the field over two years by flagging was extremely small, more than 30 times smaller than that of unfed larvae and 75 times smaller than that of unfed adults. It is logical to explain this fact by the development of a significant part of the tick population according to a 2-host cycle. If so, the proportion of such ticks in the farm population should be even higher. Balashov (1972) presented numerous cases of changes in the tick development types, especially among evolutionary young ticks, such as Rhipicephalus or Hyalomma. Such a change can be provoked by various environmental factors (hosts, temperature, time of season, etc.] and may not always be adequately explained (Balashov, 1998). Obviously, the conditions for tick feeding are better when they are in close contact with dogs than in the field where ticks must seek for their hosts. When dogs are constantly available for ticks, a considerable part of the tick population successfully engorges. This conclusion is supported by the data on comparative tick abundance on the farm and in the control field site (see above). At the same time, ticks in the field seeking for their hosts, sometimes for many weeks, gradually age, expending their nutritional resources. The greatest mortality was noted among unfed ticks that could not find a host, especially in ticks inhabiting steppe and arid environments (Balashov, 1998). Not only the portion of ticks that successfully feed, but also the amount of blood they engorge is higher in artificially created conglomerations of R. sanguineus. The larger size of the scutal index in ticks from the farm and garden as compared with field ticks supports this conclusion. The prevailing opinion about the R. sanguineus life cycle in Mediterranean countries in general and in Israel in particular is that there are two generations of ticks per year (Feldrnan-Muhsam, 1968; GiIot et al., 1992). Using the known data on R. sanguineus biology as well as our data on the physiological state of unfed females from the field and the farm, we can introduce some correction in this general scheme and show the influence of tick conglomeration on the duration of tick development. The net duration of R. sanguineus development from adult to adult (without hostseeking) has been estimated as about 100 days at 24°e (Ioffe-Uspensky et aI., 1997). According to the data of Mumcuoglu et ai. (1993a, b), there is no indication of two seasonal peaks either of tick abundance in the field or of dog infestation. At the same time, ticks were not found in the field from November through March. This period is characterised by much lower maximal and mean temperatures than the period from April

161

through October. Only unfed adults and engorged nymphs of R. sanguineus can successfully overwinter in significant numbers under such conditions (Feldman-Muhsarn, 1981). During a long Summer period, the mean maximal temperature reaches 30 (with maximal day-time temperatures up to 40°C) and the mean temperature increases from approximately 10 0 e in April up to 20 in July-August (data from (Mumcuoglu et al., 1993a)). The net duration of tick development under such conditions should be shorter than 100 days but the necessity of host seeking considerably increases the gross duration of tick development. Unsuccessful host seeking is followed by tick death from exhaustion (Uspensky, 1995). Under farm conditions, the development must be much shorter and more successful because of the 2-host developmental cycle and due to the constant availability of hosts. The comparison of the mean values of the weight! scuta I index ratios between field and farm adult ticks in different months supplements the above data and permits some conclusions on the life cycles of R. sanguineus in both locations observed. The obvious appearance of young unfed adults in the field from April to July in contrast to the stable and physiologically much younger farm ticks indicates completely different types of development for these populations. Apparently, the young field adults inJuly appear from overwintered engorged nymphs. Another cohort of ticks appears from overwintered adults and goes through their metamorphosis until the middle of the summer. The adults from this cohort exist until the end of the summer showing a gradual ageing of the field population. The first cohort produces adults of the new generation only at the end of the summer. The small percentage of physiologically young ticks at this moment, the failure to collect overwintering adults in the field as well as the lack of attachment to dogs of farm adults of the 3rd physiological age in April (see above) may be regarded as circumstantial evidence of behavioural diapause in unfed adult R. sanguineus during the winter. Behavioural diapause was found in unfed adult R. turanicus, the species closely related to R. sanguineus (Belozerov, 1982). Ageing of both populations at the end of September apparently reflects the decrease of the temperature conditions of the season that prevent further development of R. sanguineus populations. Under natural field conditions of southern and central Israel, this species can have only one complete generation per year (actually, one and a half: from engorged nymphs molted to adults to unfed adults of the next generation or from unfed adults through one complete generation to engorged nymphs). This coincides with a very accurate approach to estimate the number of R. sanguinous generations by Walker et al, (2000, p. 388) who wrote about "2 generations of adult ticks" and not of tick populations. Since 0e

0e

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the metamorphosis of R. sanguineus in tick conglomerations under conditions of constant dog availability must go faster which is supported by their younger physiological age during the entire summer season, we can conclude that the farm ticks might have two complete generations per year. In fact, there are two and a half generations, from engorged nymphs molted to adults through two complete generations or from unfed adults through two complete generations to engorged nymphs. The increasing number of dogs in many countries most likely create such conditions more often now than several decades ago. The practical conclusion from the material presented is that it is necessary to avoid the creation of conditions where tick conglomerations might appear, and to pay more attention to the pets, especially when they are kept indoors. The same holds true not only for Israel but also for any other country where R. sanguineus is an abundant species. Acknowledgements. We are greatly indebted to the farm owner for his kind permission to carry out our study at his property and to examine his dogs and to H. Uspensky and A. Vilenkin for participation in tick collections. The participation of K. Y.Mumcuoglu in the very beginning of this study is acknowledged. We thank two anonymous reviewers for their attentive reading of the manuscript and very helpful comments. We are grateful to H.]. Bromley-Schnur for her excellent linguistic assistance.

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