Engorged Ixodes ricinus nymphs collected from sheep resident in an upland UK field site were significantly lighter than nymphs that engorged on previously tick-naïve sheep, indicating that site-resident sheep continually exposed to ticks acquired anti-tick resistance. The weights of engorged nymphs that fed on naturally tick-resistant sheep increased significantly, however, when increasingly high numbers of adult female ticks fed on the sheep during seasonal peaks of tick activity. This relationship was unaffected by variations in nymph weight amongst individual sheep, between seasons and years, and potential effects of sheep infection with Ehrlichia phagocytophila; this suggests that high adult tick infestations may directly inhibit the expression of acquired anti-tick resistance by sheep. The length, width and weight of adult ticks and the scutum length of adult females were linearly related to their weight as an engorged nymph. The mean scutum length of adult female ticks feeding on sheep in the field site was greater than that of adult females obtained from engorged nymphs collected from sheep of the same site. This suggests that larger ticks have a survival advantage and that I. ricinus ticks exhibit density-dependent intraspecific facilitation at high infestation levels with potential consequences for the transmission of tick-borne diseases.
In a longitudinal study in a UK upland site, 38% of adult sheep were detected as infected with the tick-borne bacterium Ehrlichia phagocytophila by PCR of blood samples. Infection prevalence declined significantly with sheep age but varied significantly and non-linearly with the number of adult Ixodes ricinus ticks feeding per sheep. These findings suggested that under conditions of natural repeated tick-borne challenge sheep remain partially susceptible to re-infections, but the likelihood of re-infection depended on the numbers of feeding ticks. Transmission efficiency from sheep to immature ticks also varied significantly and non-linearly with the number of adult ticks feeding per sheep: transmission efficiency was almost zero in sheep with low adult tick infestations rising to 30% at certain levels of adult tick infestation. Infection intensity in infected engorged immature ticks also varied with the number of adult ticks feeding per sheep, but neither prevalence nor intensity of infection in engorged ticks were related to sheep blood PCR result. These findings suggest that variation in the numbers of ticks feeding per sheep may influence E. phagocytophila transmission by direct effects on transmission at the tick-host interface.
A total of 60 sheep were exposed to Anaplasma phagocytophilum infection on an enclosed area of Ixodes ricinus-infested pasture in North Wales, United Kingdom, and rapidly acquired acute A. phagocytophilum infections detectable by PCR and blood smear examination. Of the ticks that had engorged in the previous instar on infected sheep, 52% of adult ticks and 28% of nymphs were PCR positive; a significant, 10-fold increase in prevalence compared to that of ticks that engorged on sheep preinfection was observed (P ؍ 0.015). The likelihood that ticks were PCR positive, after feeding on the sheep and molting to the next instar, increased marginally with increasing numbers of infected neutrophils per milliliter of blood of their sheep host (P ؍ 0.068) and increased significantly when they were collected from sheep carrying higher numbers of adult female ticks (P ؍ 0.017), but increasing numbers of feeding nymphs had a significant negative effect on transmission (P ؍ 0.049). The numbers of circulating neutrophils and of infected neutrophils also varied significantly with the numbers of ticks feeding on the sheep when the blood was collected. Our study suggests that ruminants are efficient reservoirs of A. phagocytophilum during the acute and post-acute phases of infection. The risk of ruminant-derived infections may, however, be strongly affected by variations in tick densities, which may influence transmission from acutely infected animals via effects on the numbers of infected cells in the blood and possibly by within-skin modulation of infection.Anaplasma phagocytophilum (formerly Ehrlichia phagocytophilum, Ehrlichia equi, and the agent of human granulocytic ehrlichiosis [8]) is an obligate intracellular bacterium that mostly targets granulocytes in its mammalian hosts (43). Although it has been recognized for some years as a pathogen of veterinary importance, the discovery of human granulocytic ehrlichiosis in the United States and Europe (6, 21) has generated increasing public health interest in this organism.A. phagocytophilum is transmitted by ixodid ticks. In the United States the principal vectors are Ixodes scapularis and I. pacificus (35,36), while in Europe the main exophilic tick vector is I. ricinus (22). A. phagocytophilum is transstadially transmitted by these vector ticks, and there is no evidence of transovarial transmission (22,27,29,37). Most studies to date that have investigated the importance of mammalian hosts of A. phagocytophilum and its tick vectors have focused on rodents (e.g., see references 5, 20, and 37), but this organism has a wide mammalian host range, infecting domesticated cats, dogs, sheep, cows, and horses (4, 9, 13, 22). Ruminants such as deer and sheep are frequently very important hosts for vector ticks in North America and Europe (2, 26, 38) and are also potentially important reservoir hosts of A. phagocytophilum (2,3,22).In the present study we have investigated the role of sheep in the acute and post-acute phases of infection (rather than that of "carrier" sheep [29])...
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