Differential distribution of immature Ixodes dammini (Acari: Ixodidae) on rodent hosts

Ectoparasites such as ixodid ticks that remain attached to hosts for several days while feeding on blood are able to overcome the inflammatory and immune responses of some hosts and not others. The immature stages of the deer tick Ixodes dammini are found more frequently on the white-footed mouse, Peromyscus leucopus, than on other rodents. We propose that P. leucopus is more tolerant to I. dammini than is a less common host, the meadow vole, Microtus pennsylvanicus. To test this hypothesis, the distribution patterns and engorgement indices were determined for larval and nymphal I. dammini collected from wild-caught P. leucopus and M. pennsylvanicus. There were more immature ticks, which were more fully engorged, on P. leucopus than on M. pennsylvanicus. There were more and better engorged ticks on male than on female hosts. Laboratory studies on the number and weights of larval I. dammini collected off naive and previously exposed P. leucopus and M. pennsylvanicus support the results of the field study. Fewer larval ticks were recovered from previously exposed M. pennsylvanicus than P. leucopus, and the ticks weighed less. Larval and nymphal ticks aggregated among hosts in the study grid, and higher densities per male P. leucopus were correlated with higher engorgement indices, suggesting that immature I. dammini feed better at higher densities. The feeding success of I. dammini on its preferred host species might be due to its adaptation to the immune and inflammatory reactions of the host.     

Differential detachment from resting hosts of replete larval and nymphal Ixodes ticks

To determine whether replete subadult Ixodes ticks detach more frequently from resting than from active hosts, diverse rodents and lizards were caged in an apparatus designed to record the ticks' sites of detachment relative to the resting site of the host. Replete larval Ixodes ricinus and Ixodes dammini accumulated mainly beneath the resting places of the mice (Apodemus agrarius and Peromyscus leucopus) most frequently parasitized in nature. Although nymphal I. ricinus similarly detached where these mice rested, nymphal I. dammini detached more randomly. When lizards were used as hosts, both subadult stages of I. ricinus tended to detach away from their main resting sites; these ticks detached from squirrels more randomly. Detachment ratios for other rodent hosts, that are abundantly infested by the larvae of these ticks in nature (Apodemus flavicollis and Clethrionomys glareolus), could not be derived because nymphs generally failed to attach. Our observations are consistent with reports that both subadult stages of I. dammini, but not the adult, feed on the same kind of nest-dwelling hosts and that the host range of I. ricinus is less focused. Detachment of mouse-feeding larvae from resting mice promotes subsequent nymphal attachment to conspecific hosts, and the absence of such behavior among nymphs facilitates access of the resulting adults to deer.     

Vectorial capacity of North American Ixodes ticks.

Ixodes dammini, the vector of Lyme disease and babesiosis, is distributed in various locations in the northeastern quadrant of the United States and nearby Canada. The life cycle of this tick, which includes larval, nymphal, and adult stages, spans at least two years. The tick over-winters between larval and nymphal feeding. Horizontal transmission of pathogens is facilitated by a feeding pattern in which both the larval and nymphal stages feed on the white-footed mouse, Peromyscus leucopus, and by a seasonal pattern of activity in which nymphs precede larvae. The species range appears to have expanded from a single island location, and has invaded new sites since the 1940s, some as recently as 1980. This increased abundance appears to be related to the increased abundance of deer, the preferred host of the adult stage. I. muris predominated in coastal Massachusetts before I. dammini became abundant, but is probably now extinct. I. scapularis, which is present in the southern U.S., is a poor vector of mouse parasites because about 90 percent of these immature ticks feed on lizards. To the extent that horizontal transmission occurs, we suggest that mice serve as the principal reservoir for the Lyme spirochete as well as Babesia microti.     

Prevalence of the Lyme disease spirochete in populations of white-tailed deer and white-footed mice

The prevalence of the Ixodes dammini spirochete (IDS) in white-tailed deer (Odocoileus virginianus) and white-footed mice (Peromyscus leucopus) was studied on the eastern end of Long Island, New York. Both species commonly occur in a variety of habitats, are preferred hosts of Ixodes dammini, and can harbor the spirochetes in the blood. Each animal was examined for spirochetemia, tick infestation, and IDS infection rates in the ticks that were removed from it. The results obtained suggest that in winter deer can be infected by questing adult I. dammini. Adult ticks apparently are infected through transtadial transmission of spirochetes from subadult ticks which had fed earlier in their life history on infected animals. Deer are important hosts of adult ticks and the IDS in winter and probably are a reservoir host in other seasons. The patterns of spirochete prevalence suggest that deer and mice are reservoirs of the organism and thus are fundamental to the ecology of Lyme disease on Long Island.     

Effect of deer reduction on abundance of the deer tick (Ixodes dammini)

To evaluate the role of deer in regulating the abundance of the deer tick (Ixodes dammini) we attempted to treat with acaricide, but eventually removed, about 70 percent of deer from Great Island, Cape Cod, Massachusetts. Deer were captured in box traps, a corral, an entanglement net, and with rifle-fired tranquilizer. Failure of these attempts, combined with ineffective acaricides, led us to deer destruction begun in fall 1982. Larval tick abundance on mice was monitored before and after deer removal. We concluded that deer removal, to the extent accomplished, did not markedly reduce the abundance of the tick. Reduced abundance of deer may not result in reduced abundance of immature ticks if deer removal follows the period of adult tick feeding, or if intensity of infestation per deer increases, or if other mammals substitute as suitable hosts. Reduced tick abundance may be delayed if unattached immature ticks survive more than one year.     

Bird-feeding ticks transstadially transmit Borrelia burgdorferi that infect Syrian hamsters

Bird-feeding Ixodes dammini ticks were documented for the first time to successfully molt and transstadially pass Borrelia burgdorferi spirochetes that were indistinguishable by sodium dodecyl sulfate-polyacrylamide gel electrophoresis from the type B31 strain. Forty-six of 73 blood-engorged larvae and 50 of 66 fully-fed nymphs, removed from wild-caught birds, successfully molted. Borreliae were isolated from 21 of 78 partially- and fully-fed larvae off birds, including six specimens that molted. Spirochete-positive cultures also were obtained from 35 of 60 partially- and fully-fed nymphs that had fed from birds, including 20 nymphs that molted into adult ticks. Transstadially passed borreliae by bird-feeding larval and nymphal I. dammini were infectious to hamsters, leading us to suggest that these ticks are capable of subsequently transmitting infectious spirochetes to mammals, including humans. An isolated of B. burgdorferi, recovered from a bird-feeding larval Ixodes dentatus, was indistinguishable by sodium dodecyl sulfate-polyacrylamide gel electrophoresis from the B31 strain. This isolate, unlike another from I. dentatus off a cottontail rabbit (Sylvilagus floridanus), had a protein band with a molecular weight of approximately 31,000 that reacted with murine monoclonal antibodies H3TS and H5332 in western blot analysis. Thus, closely related borreliae are present in both I. dentatus and I. dammini.     

Enzootic Babesia microti in Maine

Human babesiosis in the northeastern United States caused by Babesia microti (Apicomplexa: Piroplasmida) is mainly reported from coastal New England sites, where deer ticks (Ixodes dammini) are common. However, the piroplasm has been detected in microtine rodents elsewhere in association with I. angustus or other nidicolous ticks, suggesting that the agent is widely distributed but zoonotically significant only where a human-biting "bridge" vector is present. To determine whether this piroplasm may be enzootic in areas where I. dammini is absent, we surveyed small mammals collected from 2 sites in Maine, where I. angustus or I. muris is common but I. dammini is not. Of 43 chipmunks, voles, deer mice, and shrews examined, 3 (6.9, 95% confidence interval 0 to 14.5) were parasitemic, as determined by blood smear or polymerase chain reaction targeting a piroplasm-specific portion of the 18S ribosomal DNA gene. Phylogenetic analysis of the sequenced amplification products demonstrates the presence of 2 forms of B. microti. We conclude that B. microti may be enzootic in the absence of I. dammini but that human risk relates to dense infestations of this human-biting tick.     

Incompetence of catbirds as reservoirs for the Lyme disease spirochete (Borrelia burgdorferi)

We compared the relative infectivity to vector ticks of gray catbirds (Dumetella carolinensis) and white-footed mice (Peromyscus leucopus) for the Lyme disease spirochete (Borrelia burgdorferi). Of 28 catbirds captured in a site enzootic for this agent, 18 were infested by immature Ixodes dammini, the tick vector. By comparison, each of 32 mice sampled concurrently from the same site was infested, and by about 10 times as many ticks as were found infesting the 3 most commonly netted bird species. Although 76% of noninfected larval ticks placed on these mice in a xenodiagnosis became infected, none of the ticks similarly placed on 12 catbirds did so. Spirochetes were detected in ticks derived from 2 Carolina wrens (Thryothorus ludovicianus) and a common yellowthroat (Geothlypis trichas), but these species' potential contribution to infecting ticks does not compare with that of mice. Thus, although birds may help establish new foci of ticks, catbirds, at least, do not appear to contribute as reservoirs of infection.     

Evaluation of 4-poster acaricide applicators to manage tick populations associated with disease risk in a Tennessee retirement community

In 1993, four residents of a retirement community in middle Tennessee were hospitalized with symptoms of ehrlichiosis causing community managers to implement mitigation methods to reduce tick numbers. For the past four years, managers have utilized 4-poster acaricide applicators that aim to reduce disease risk to residents by killing ticks that feed on deer. To determine the efficacy of this technique, we assessed Amblyomma americanum abundance in the vicinity of the devices by dragging 400 m vegetation transects once per month while ticks were active. In 2009, adult tick activity peaked in May, nymphal tick activity peaked in June, and larval activity peaked in September. Close to 4-poster devices, larval, nymphal, and adult tick abundances were reduced by 91%, 68%, and 49%, respectively (larval and nymphal p<0.001, adult p=0.005), relative to nearby untreated areas. No significant reduction in nymphal or adult A. americanum ticks was evident >300 m from 4-poster devices, however a ～90% reduction in larvae was observed to our sampling limit (400 m). At the low density at which these devices are currently being used (average distance between devices = 6.6 km), we conclude that they will have little large-scale effect on the health risk posed by ticks in this community.     

Prevalence of Borrelia burgdorferi and Babesia microti in mice on islands inhabited by white-tailed deer.

Borrelia burgdorferi and Babesia microti were isolated from 35 of 51 white-footed mice (Peromyscus leucopus) and meadow voles (Microtus pennsylvanicus) captured on two Narragansett Bay, R.I., islands inhabited by deer, the principal host for the adult stages of the vector tick, Ixodes dammini. Immature ticks parasitized mice from both islands. From 105 mice captured on four other islands not inhabited by deer neither pathogen was isolated, nor were I. dammini found.     

Prevalence of Borrelia burgdorferi and Babesia microti in mice on islands inhabited by white-tailed deer

Borrelia burgdorferi and Babesia microti were isolated from 35 of 51 white-footed mice (Peromyscus leucopus) and meadow voles (Microtus pennsylvanicus) captured on two Narragansett Bay, R.I., islands inhabited by deer, the principal host for the adult stages of the vector tick, Ixodes dammini. Immature ticks parasitized mice from both islands. From 105 mice captured on four other islands not inhabited by deer neither pathogen was isolated, nor were I. dammini found.     

Babesia microti: prolonged survival of salavarian piroplasms in nymphal Ixodes dammini

We determined how long Babesia microti survive in the salivary glands of nymphal Ixodes dammini. Of those ticks held at 21 C, the proportion with demonstrable piroplasms decreased from 95%, prior to 20 weeks post-larval-feeding (p-l-f), to less than 80% at 42 weeks p-l-f. Similarly, the number of infected acini decreased significantly. Nymphal I. dammini were kept alive for as long as 1 year, by transferring them to 4 C, at 20 weeks p-l-f. The proportion of infected ticks at 52 weeks p-l-f was less than half of the proportion of infected nymphs examined prior to 20 weeks p-l-f, and only 1/6 as many acini were infected. Ultrastructural observations of salivary glands from ticks at 44 weeks p-l-f revealed that B. microti parasites in older ticks remain in the sporoblast meshwork phase; such parasites rarely differentiated into sporozoites. Degenerating parasites containing autophagic vacuoles were also observed in older ticks.     

Spatial and temporal dispersion of immature Ixodes dammini on Peromyscus leucopus in northwestern Illinois.

Infestation by immature Ixodes dammini and infection by Borrelia burgdorferi of the white-footed mouse Peromyscus leucopus were studied in Castle Rock State Park in northwestern Illinois during June-October 1990. Prevalence and intensity of infestation of larvae on mice were highest in August with a smaller peak in early June. The distribution of larvae on mice was highly aggregated during each of the sampling periods. Aggregation appears to be the result of a series of nonrandom successful attachments by single larvae, rather than of simultaneous attachment by clumps of larvae. Infection rate of mice by B. burgdorferi averaged 21.4% with a peak of 28.6% in August. A comparison of the numbers of attached immature ticks collected from mice and of questing ticks collected through dragging indicated that the larvae-to-nymph ratio was higher on mice than on drags. Given the low total numbers of nymphs collected from mice, this suggests a potential role for other hosts of I. dammini nymphs in northwestern Illinois.     

Sperm precedence in the deer tick Ixodes dammini

ABSTRACT We determined whether female deer ticks Ixodes dammini Spielman, Clifford, Piesman & Corwin (Acari: Ixodidae) can be inseminated repeatedly and whether sperm from first or second matings take precedence in fertilizing eggs. Such information is essential to the design of attempts to reduce the fertility of these vectors of Lyme disease. Although spermatophores are present in about half of questing female ticks, they are present in virtually all those found on deer; the abundance of males on deer exceeds that of females and copulation is common. Females must be inseminated before commencing the rapid engorgement phase of feeding. Males need not be in attendance during feeding, provided that the female has been inseminated preprandially. Thus, preprandial insemination suffices to stimulate rapid engorgement, but less blood is taken than when the female is perprandially inseminated. Both types of insemination effectively fertilize eggs. Eggs from females sequentially inseminated by irradiated and non irradiated males, were fertilized mainly by sperm from the last male. Cobalt-irradiated males mate effectively and their sperm compete with those of non-irradiated males. Sperm from the second two sequential inseminations fertilize most of the eggs. By infesting deer with such irradiated male I.dammini , the abundance of these vector ticks may effectively be reduced.     

Avian and mammalian hosts for spirochete-infected ticks and insects in a Lyme disease focus in Connecticut.

Spirochetes and their vectors and reservoirs were studied in a Lyme disease focus in East Haddam, Connecticut, from mid-May through September 1983. Ixodes dammini subadults were comparable in number on white-footed mice (Peromyscus leucopus) (means = 2.9 +/- 3.6 SD) to those on 27 different species of birds (means = 2.3 +/- 4.2 SD) representing 11 families within the order Passeriformes. Less commonly found ticks on birds (means less than or equal to 0.1) were immature Ixodes dentatus and Haemaphysalis leporispalustris. Although spirochete-infected I. dammini larvae and nymphs were taken off eight and nine different species of birds, respectively, significantly fewer positive larvae were removed from birds than from white-footed mice. Spirochetes were detected in the midguts of I. dammini, Dermacentor variabilis, and H. leporispalustris and two species of insects (Cuterebra fontinella and Orchopeas leucopus). Possibly, arthropods other than I. dammini vector these spirochetes in northeastern United States. Spirochetes grew in a cell-free medium inoculated with bloods from four white-footed mice, one woodland jumping mouse (Napaeozapus insignis), one northern mockingbird (Mimus polyglottos), one gray catbird (Dumetella carolinensis), two prairie warblers (Dendroica discolor), one orchard oriole (Icterus spurius), one common yellowthroat (Geothlypis trichas), and one American robin (Turdus migratorius). We suggest that avian hosts, like mammals, develop spirochetemias of the causative agent of Lyme disease. Erythematous tissues from a white-footed mouse were infected with spirochetes.     

The effect of spatial heterogenity on the aggregation of ticks on white-footed mice

Parasites are often aggregated on a minority of the individuals in their host populations. Although host characteristics are commonly presumed to explain parasite aggregation on hosts, spatio-temporal aggregation of parasites during their host-seeking stages may have a dominant effect on the aggregation on hosts. We aimed to quantify, using mixed models, repeatability and autocorrelation analyses, the degree to which the aggregation of blacklegged ticks (Ixodes scapularis) on white-footed mice (Peromyscus leucopus) is influenced by spatio-temporal distributions of the host-seeking ticks and by heterogeneity among mice. Host-seeking ticks were spatially aggregated at both the larval and nymphal life-stages. However, this spatial aggregation accounted for little of the variation in larval and nymphal burdens observed on mice (3% and 0%, respectively). Conversely, mouse identity accounted for a substantial proportion of the variance in tick burdens. Mouse identity was a significant explanatory factor as the majority of ticks parasitized a consistent set of mice throughout the activity seasons. Of the characteristics associated with mouse identity investigated, only gender affected larval burdens, and body mass and home range sizes in males were correlated with nymphal burdens. These analyses suggest that aggregation of ticks on a minority of mice does not result from the distribution of host-seeking ticks but from characteristics of the hosts.     

Impact of the experimental removal of lizards on Lyme disease risk

The distribution of vector meals in the host community is an important element of understanding and predicting vector-borne disease risk. Lizards (such as the western fence lizard; Sceloporus occidentalis) play a unique role in Lyme disease ecology in the far-western United States. Lizards rather than mammals serve as the blood meal hosts for a large fraction of larval and nymphal western black-legged ticks (Ixodes pacificus--the vector for Lyme disease in that region) but are not competent reservoirs for the pathogen, Borrelia burgdorferi. Prior studies have suggested that the net effect of lizards is to reduce risk of human exposure to Lyme disease, a hypothesis that we tested experimentally. Following experimental removal of lizards, we documented incomplete host switching by larval ticks (5.19%) from lizards to other hosts. Larval tick burdens increased on woodrats, a competent reservoir, but not on deer mice, a less competent pathogen reservoir. However, most larvae failed to find an alternate host. This resulted in significantly lower densities of nymphal ticks the following year. Unexpectedly, the removal of reservoir-incompetent lizards did not cause an increase in nymphal tick infection prevalence. The net result of lizard removal was a decrease in the density of infected nymphal ticks, and therefore a decreased risk to humans of Lyme disease. Our results indicate that an incompetent reservoir for a pathogen may, in fact, increase disease risk through the maintenance of higher vector density and therefore, higher density of infected vectors.     

Borrelia Burgdorferi Sensu Lato in Ixodes Ricinus Ticks and Rodents in a Recreational Park in South-Western Ireland

Ixodes ricinus ticks infected with Borrelia burgdorferi sensu lato were numerous on the edges of paths and roads in a recreational park in south-western Ireland. The abundance of ticks at different sites was related to the presence of deer, but a negative relationship was shown between tick abundance and tick infection rates. This is thought to be due to the deposition of large numbers of uninfected ticks by deer, which are apparently not good reservoir hosts of B. burgdorferi s.l. Blood meal analysis only detected deer DNA in uninfected nymphs. Reservoir competent rodents, Apodemus sylvaticus and Clethrionomys glareolus, were abundant at all sites and a high proportion of captured specimens were infested with larval ticks. However, very few rodents were infected with B. burgdorferi s.l. and none of the unfed infected nymphs analysed for the identity of their larval blood meal had fed on rodents. The spirochaetes detected in I. ricinus in the study area may be poorly adapted to rodents or are not transmitted readily because of the absence of nymphal infestation. The majority of spirochaetes in these ticks were apparently acquired from non-rodent hosts, such as birds.     

Spirochetes in ticks and antibodies to Borrelia burgdorferi in white-tailed deer from Connecticut, New York State, and North Carolina

Ticks were screened for spirochetes and serum samples from white-tailed deer (Odocoileus virginianus) were assayed for antibodies to Borrelia burgdorferi during 1983-1984. Using fluorescein isothiocyanate-labeled rabbit antibodies produced to B. burgdorferi, the etiologic agent of Lyme disease, spirochetes were detected in Ixodes dammini (10.5% of 1,193) and Dermacentor albipictus (0.6% of 157) adults from Connecticut, I. dammini nymphs (49.1% of 108) and adults (64.7% of 99) from Armonk, New York, and in I. scapularis (0.4% of 531) and Amblyomma americanum (3.5% of 173) adults from North Carolina. Infected ticks were either seeking hosts or feeding on deer during the summer and fall. Direct fluorescent antibody staining also revealed spirochetes in two larvae of I. scapularis that emerged from eggs deposited by separate females in the laboratory. Using indirect immunofluorescence tests, antibodies to B. burgdorferi were identified in white-tailed deer living in tick-infested areas of all three states. Aside from minor cross-reactivity, there was no serologic evidence of Treponema or Leptospira infections. Ixodes dammini is a primary vector of B. burgdorferi in northeastern United States, but in North Carolina, other ixodid ticks may transmit this spirochete to humans and wildlife.     

Host association and seasonal activity of Amblyomma americanum (Acari: Ixodidae) in Missouri

From June 1993 through June 1996, 2,260 adult, 4,426 nymphal, and 2,178 larval lone star ticks Amblyomma americanum (L.) were collected in Missouri from vertebrate hosts and by dragging a cloth over vegetation. Prevalence, mean intensity, and relative abundance of each stage varied among hosts. The relative abundance of adult lone star ticks was highest on white-tailed deer, but this stage was also collected from raccoons, opossum, red fox, coyotes, and wild turkey. Nymphs were collected from gray squirrels, eastern cottontail rabbits, opossums, red fox, Carolina wren, and bobwhite quail, but the highest relative abundance occurred on wild turkey, white-tailed deer, and raccoons. Eastern cottontail rabbits, white-tailed deer, raccoons, and squirrels had the highest relative abundance of larval lone star ticks, but they were also found on opossums and wild turkey. The activity of adult lone star ticks was greatest from May through July. The activity for nymphs was highest from May through August, and for larvae, July through September.