Questing behaviour of Ixodes ricinus ticks (Acari: Ixodidae)

The vertical distribution in the vegetation of questing Ixodes ricinus ticks was investigated in two different vegetation types (high and low vegetation) at two localities in south-central Sweden during 1992-1993 (Toro) and 1995 (Bogesund). Significant correlations were found between the vertical distribution of immature ticks and the height of the vegetation. The greatest mean availabilities of the larvae and nymphs in low vegetation were in the intervals 0-9 and 30-39 cm, respectively. The larval numbers were greatest close to the ground (0-29 cm) in both high and low vegetation. The larval : nymphal ratio, at ground level at localities free of ground vegetation, varied between 8 : 1 and 32 : 1. In high vegetation, the greatest mean numbers of nymphal and adult ticks were at height intervals of 50-59 and 60-79 cm, respectively. These ranges are within the estimated height interval (40-100 cm) of the main part of the body surface of their preferred host, the roe deer (Capreolus capreolus). The presence of most questing I. ricinus larvae at ground level would favour the transmission of Borrelia burgdorferi s.l., since this is where the highly reservoir-competent rodents and shrews usually occur.     

The effect of feeding status on sexual attractiveness of Ixodes ricinus (Acari: Ixodidae) females

Sexual attractiveness of unengorged, semiengorged and fully engorged females of both field and laboratory populations of Ixodes ricinus was studied under laboratory conditions by means of a computerised video tracking system. A male and a female were allowed to walk freely in a glass arena during 1 h and their behavioural interactions were observed. Obtained results revealed that the feeding status of I. ricinus females affects their sexual attractiveness. The highest attractiveness was observed in engorged females, the lowest in unengorged females of the field population. Copulation occurred in all experimental groups with the highest frequency observed in the unengorged virgin laboratory females. Despite engorged females being highly attractive for males on distance, the frequency of copulation was low. Differences between field and laboratory populations were found in both behavioural parameters and frequency of copulation. This revised version was published online in July 2006 with corrections to the Cover Date.     

Morphofunctional changes in the midgut of the Ixodes ricinus nymphs (Acari: Ixodidae) during developmental diapause

Changes in the midgut of the Ixodes ricinus nymphs at the stage of developmental diapause were studied. It is established, that the midgut of the tick nymphs undergoes the identical and synchronous changes at the development without diapause and in the state of diapause. In 7-8 months after feeding the midgut of the nymphs containes the digestive cells with gematine and food inclusions, as well as reserve cells, like the midgut of unengorged moulted female. But the midgut of diapausing nymphs retaines such condition during the whole period of diapause.     

Development of the salivary glands in embryos of Ixodes ricinus (Acari: Ixodidae)

We examined Ixodes ricinus embryos between 18 and 28 days of development with light, scanning and transmission electron microscopy. The differences in inner structure attested to establish three successive developmental stages: days 18–20, day 23, and days 26–28. Between 18 and 20 days the embryos are at early stages of organogenesis. Salivary glands cannot be identified at that stage. In 23-day-old embryos salivary glands are already outlined but the structure of alveoles is still different from that in larvae in which the embryonic development has been completed. Gland cells start to form alveoles and become active between 26 and 28 days of the development. This revised version was published online in July 2006 with corrections to the Cover Date.     

Development of the salivary glands in embryos of Ixodes ricinus (Acari: Ixodidae)

We examined Ixodes ricinus embryos between 18 and 28 days of development with light, scanning and transmission electron microscopy. The differences in inner structure attested to establish three successive developmental stages: days 18-20, day 23, and days 26-28. Between 18 and 20 days the embryos are at early stages of organogenesis. Salivary glands cannot be identified at that stage. In 23-day-old embryos salivary glands are already outlined but the structure of alveoles is still different from that in larvae in which the embryonic development has been completed. Gland cells start to form alveoles and become active between 26 and 28 days of the development.     

The longevity of the tick Ixodes ricinus (Acari: Ixodidae) in Central Russia

The longevity of the tick Ixodes ricinus has been studied on 27 samples from a wild population of the Moscow Region. Ticks were kept in small cages and glass tubes under conditions close to natural. About 2/3 of the specimens collected in spring survived till the next spring and later died out gradually during the second season of their activity. Very few specimens reached the beginning of the third winter in their life, but apparently none of them survived the end of the winter. The life span of males was the same as that of females. No mass activation of adult ticks was recorded in the autumn of the year of their molting. It seems that the rise of the autumnal density of adult ticks depends mainly on the increased activity of the females which molted from nymphs last year.     

Infestation of mammals by Ixodes ricinus ticks (Acari: Ixodidae) in south-central Sweden

Infestation by Ixodes ricinus ticks on rodents, hares and cervids was examined at Bogesund, 10 km north of Stockholm, in south-central Sweden during 1991-1994 and on varying hares (Lepus timidus) at Stora Karlso and Gotska Sandon in the Baltic Sea during 1992-1993. At Bogesund, there were great differences between two consecutive years in the number of I. ricinus larvae infesting bank voles (Clethrionomys glareolus). The seasonal pattern of infestation by I. ricinus larvae and nymphs on bank voles was unimodal in 1991, with peaks in June-July and bimodal in 1992, with peaks in June and August. Male bank voles, compared to females and older voles, compared to young voles, harboured greater numbers of I. ricinus ticks. Apodemus mice, compared to bank voles, harboured greater numbers of I. ricinus ticks. Ixodes ricinus larvae engorged on Apodemus mice were heavier than larvae engorged on bank voles and resulted in larger nymphs. However, there was no difference in the proportions of viable nymphs resulting from larvae engorged on mice or voles. The ranges in the numbers of I. ricinus ticks infesting individual hosts were 1-451 for rodents, 16-2374 for hares and 428-2072 for roe deer (Capreolus capreolus). These ranges of tick numbers are estimated to represent potential blood losses from individual hosts of approximately 0.2-65% for rodents, 0.2-13% for hares and 0.3-9.0% for roe deer. Within the populations of all host species examined, the distributions of all stages of I. ricinus were clumped, with most host individuals harbouring few ticks and only a few individuals harbouring many ticks. The data suggest that, even though a small proportion of tick hosts may be severely affected, the direct effects of feeding by I. ricinus are unlikely to play an important role on mammal population dynamics.     

Densities of Ixodes ricinus ticks (Acari: Ixodidae) on moorland vegetation communities in the UK

Unfed (questing) Ixodes ricinus ticks were collected by blanket dragging on a monthly basis from heather-dominated, Vaccinium-dominated and bracken-dominated vegetation communities from two different biogeographical regions of the UK (the Quantock Hills in Somerset, south west England and the North York Moors, north east England) throughout the spring and summer months of 1991 and 1992. Eighteen sites were monitored across the two regions and a total of 1920 blanket drags were carried out. Vaccinium sites showed high tick densities at all life stages, as did bracken sites. Significantly lower numbers of larval and nymphal ticks per drag were collected on heather sites than were collected on either Vaccinium (bilberry/whortleberry) or bracken sites, while similar numbers of adult ticks per drag were collected from each of the three vegetation communities. There was no significant difference between the mean numbers of any tick life stage collected on the Quantock Hills and those collected on the North York Moors on these vegetation communities or between the mean numbers of any tick life stage collected in 1991 and those collected in 1992 on these vegetation communities.     

Multiple paternity in Ixodes ricinus (Acari: Ixodidae), assessed by microsatellite markers

This investigation examines multiple paternity in Ixodes ricinus (Acari: Ixodidae). Previous studies have shown that multiple mating occurs in this tick, but this is the first evaluation of multiple paternity. Three family groups were examined by a panel of polymorphic microsatellite loci; all ticks were bred from wild-collected engorged females with a copulating male attached. For most larvae, the attached males could be excluded as possible sire, and in the 3 tested families, at least 2 of 3 females mated successfully with more than 1 male. This finding suggests that multiple paternity is a common reproductive strategy in I. ricinus, which may have consequences for the ticks' dispersal success by increasing the genetic diversity in broods from single females colonizing new sites.     

Differences in Borrelia infections in adult Ixodes persulcatus and Ixodes ricinus ticks (Acari: Ixodidae) in populations of north-western Russia

Dark-field microscopy was used to determine the number of Borrelia spirochetes in 630 standard preparations obtained from adult ixodid ticks (344 Ixodes persulcatus and 286 I. ricinus) collected in 1989-92 in the Leningrad region of Russia. The average numbers of Borrelia in I. persulcatus and I. ricinus preparations were 34.7 and 23.3 per 100 microscopic fields, respectively. The maximal individual values registered each year for ticks of both species were several hundred times greater than the minimal values. Ticks carrying relatively small numbers of Borrelia generally predominated. Proportions of more heavily infected ticks varied considerably from year to year. These parameters were significantly higher in foci with predominance of I. persulcatus ticks. As a consequence, risk to acquire Lyme borreliosis in such foci is considered greater than in foci where I. ricinus predominates.     

Hosts and Pathogen Detection for Immature Stages of Ixodes ricinus (Acari: Ixodidae) in North-Central Spain

To determine hosts of the immature stages of a southern population of Ixodes ricinus, we trapped rodents and birds in an area of north-central Spain in May–June and August–September of 1998 and 1999. The most frequently trapped rodents were Apodemus sylvaticus (230 specimens) and Clethrionomys glareolus (99), with a larval infestation prevalence of 49% and 81%, respectively (in spring) and 21% and 41% (in summer). C. glareolus was always more heavily parasitized by larvae (mean numbers 19.8 in spring, 3.4 in summer) than A. sylvaticus (6.1 and 1.2, respectively). No nymphs were collected from the rodents. The larval distribution pattern differed considerably between rodent host species but not according to the season of the year. The most commonly trapped birds were members of the Turdidae, which had infestation incidences of about 70% (larvae) and 10% (nymphs) in spring and 20–15% in summer. We also used molecular methods for the identification of reservoir hosts of the larval ticks and of the pathogens they contained, from nymphs collected in the same site in June of 2002 and 2003. The study showed that most of the ticks had fed on birds and few on rodents and ruminants. Pathogens detected in these ticks included Babesia microti, Borrelia garinii, B. valaisiana and B. afzelii. Borrelia afzelii was detected in a tick that had apparently fed on a wild boar.     

Diel activity of Ixodes ricinus Acari: Ixodidae at two locations near Stockholm, Sweden

The diel ‘activity’, i.e. availability, of Ixodes ricinus larvae, nymphs and adults was investigated in a meadow and a forest habitat near Stockholm during 1991–1993. Generally, the immature ticks were more prevalent in the forest than in the meadow. In the meadow, the mean larval and adult numbers varied significantly between 4 h time intervals with the peak activity from 2300 to 0300 h. In the forest, the tick numbers did not differ significantly between the time intervals. The association of the tick activity with certain meteorological variables was strongest in the meadow, where the mean numbers of all tick stages were negatively correlated with the temperature. The relative humidity was positively correlated only with the mean numbers of larvae. In contrast, the larval activity in the forest was positively and negatively correlated with the temperature and relative humidity, respectively, while the nymphal and adult activity showed no association with these climatic variables. The impact of the host activity on the tick diel activity is also discussed.     

Effects of Juvenoids and Retinoic Acid on Development of Larvae and Nymphs in the Tick Ixodes ricinus L. (Acari,Ixodidae) and Regeneration of Haller's Organ during Metamorphosis

Larvae and nymphs of the tick Ixodes ricinus L. display similar reactions to analogs of the insect juvenile hormones (methoprene and pyriproxyfen), which induce at both stages juvenalization of the Haller's sense organ regenerates. Similar effects were also described for retinoic acid. Unlike juvenoids, retinoic acid can affect not only regeneration, but also normal development of the Haller's organ and cause changes corresponding to so-called regenerative induction. Amputation of the leg and treatment with retinoic acid do not affect the duration of larval or nymphal development, while juvenoids somewhat accelerate their development.     

Sites of attachment and density assessment of female Ixodes ricinus (Acari: Ixodidae) on dairy cows

A sample of 110 lactating dairy cows was examined to describe the attachment sites of female Ixodes ricinus ticks and to assess whether counts on one or two body areas can predict infestation and its level. Seventy per cent of the cows were infested by I. ricinus and the average tick burden on the infested cows was 15, ranging from 1 to 136. Preferred attachment sites were the axilla, udder/groin, neck, dewlap and flank. Udder/groin and axilla carryied respectively 35.3% and 44.1% of the total tick burden. To predict infestation (yes/no), sensitivity of counts on axilla, on udder/groin and on both areas was respectively, 76.6%, 80.6% and 94.8%. Total burden prediction equations based on count on axilla and udder/groin are presented.     

The extensible alloscutal cuticle of the tick, Ixodes ricinus

The proteins in the distensible alloscutal cuticle of the blood-feeding tick, Ixodes ricinus, have been characterized by electrophoresis and chromatography, two of the proteins were purified and their total amino acid sequence determined. They show sequence similarity to cuticular proteins from the spider, Araneus diadematus, and the horseshoe crab, Limulus polyphemus, and to a lesser extent to insect cuticular proteins. They contain a conserved sequence region, which is closely related to the chitin-binding Rebers-Riddiford consensus sequence present in many insect cuticular proteins. Only a fraction of the alloscutal proteins can be readily dissolved, and the dissolved proteins are difficult to separate by electrophoresis and column chromatography. The insoluble fraction can only be dissolved after degradation to smaller peptides. The mixture of extractable proteins as well as hydrolysates of the insoluble fraction are fluorescent when exposed to ultraviolet light, and the fluorescence corresponds in excitation and emission maxima to the fluorescence of the rubber-like arthropodan protein, resilin, and to the amino acid dityrosine. Small amounts of dityrosine were obtained from ticks in the early phase of a blood meal when the cuticle weighs less than 4 mg; increasing amounts were obtained from animals in the initial period of feeding, during which the cuticular weight increases from 4 to 11 mg, whereas little increase in dityrosine content was observed during the final period of engorgement. Cuticle from fully distended ticks contains about 60-80 nmole dityrosine per tick, corresponding to 2-3 microg/mg cuticle. It is suggested that the major part of the cuticular proteins is made inextractable by cross-linking by dityrosine residues, and that dityrosine plays a role in stabilizing the cuticular structure during the extensive distension occurring during a blood meal. Small amounts of 3-monochlorotyrosine and 3,5-dichlorotyrosine were obtained from the distended tick cuticle, corresponding to chlorination of between 0.5% and 1.5% of the tyrosine residues. It is suggested that the chlorotyrosines are a side-product of oxidative processes in the cuticle.     

Morphofunctional changes in the midgut of tick females of the genus Ixodes (Acari: Ixodidae) during and after feeding

Cyclic changes of the midgut epithelium were observed in females of 5 ticks species of the genus Ixodes during 7-10 days of feeding. The midgut epithelium of unfed females is represented by the digestive cells of nymphal phase and stem cells. The digestive cells of nymphal phase are functional during 1.5-2 days after attachment of the tick, and then, after the tearing away they go into the gut lumen. The secretory cells substitute the digestive cells of nymphal phase and finish their growth during the 4-4.5 days. Secretion of digestive enzymes is performed by the holocrine type with tearing away a whole cell. Intracellular digestion takes place in the digestive cells of four consequent generations. The secretory and digestive cells form a peritrophic matrix on their surface. The presence of peritrophic matrix gives an evidence the maturity and functional activity of the secretory and digestive cells. We suggest, that the peritrophic matrix takes part in intracellular digestion, namely in the process of micropinocytosis. The phagocytosis was not found in the ticks investigated. Digestion in the midgut lumen is performed by enzymes of the ruptured secretory and digestive cells, that is proved by the haemolysis of erythrocytes in the zone of their contact with these cells. The digestive cells of each generation functioned almost synchronously, with largest difference in starting about 12 hours.