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Keywords:

  • Amblyomma americanum;
  • lone star tick;
  • white-tailed deer;
  • 4-poster;
  • ehrlichiosis

ABSTRACT:

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

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.


INTRODUCTION

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

We investigated the process of managing Amblyomma americanum with 4-poster acaricide applicators in a golf-oriented retirement community of approximately 6,000 residents located in the Cumberland Plateau of Tennessee. The heavily forested area contains abundant wildlife that support large tick populations. In 1993, an outbreak of human ehrlichiosis occurred in the community (Standaert et al. 1995) and managers consequently implemented measures to attempt to control ticks and reduce human disease risk. Acaricide treatment of white-tailed deer was suggested as a method to reduce tick populations and therefore lower the risk of tick-borne disease in the treatment area (Pound et al. 1996). Initial research at the site involved an experimental permit to feed deer ivermectin-treated corn to reduce the survival and reproduction of A. americanum. Corn was treated at a rate of 50.0 ml pour-on insecticide (5 mg/ml) per 22.7 kg of whole kernel cleaned corn. The study confirmed reduced reproductive success of A. americanum, determined by fewer larval masses being found in the treated vs untreated areas. Ultimately, however, the potential risk of chemical residues in deer that were being harvested by hunters each fall was deemed to be too high with this method and it was consequently not approved by the USDA for use beyond the initial experimental permit.

In recent years, community residents and local health professionals have voiced increasing concerns that ticks may be continuing to transmit zoonotic pathogens to the local human population. Consequently, 4-poster devices (Pound et al. 2000) are currently being utilized to manage the tick population within the area. The 4-poster acts by attracting deer to a corn bait source where the head, neck, and ears come into contact with paint rollers treated with acaricide (Pound et al. 2000). Significant reductions in ticks have been achieved using this technique; however the initial studies documenting such reductions focused on deer populations within fenced-in or small-scale communities (Bloemer et al. 1990, Pound et al. 2000, Carroll and Kramer 2003). More recently, the Northeast Area-Wide Tick Control Project evaluated the 4-poster acaricide applicator for reducing the abundance of Ixodes scapularis ticks in Rhode Island, Connecticut, New York, New Jersey, and Maryland (Brei et al. 2009, Carroll et al. 2009, Hoen et al. 2009, Miller et al. 2009, Solberg et al. 2003). These studies found high variation in level of control in the first year of treatment with nymphal tick numbers decreasing in subsequent years by as much as 71% in 5.14 km2 treatment sites. When assessing efficacy of 4-poster devices in the first year of deployment, host-seeking nymphs of tick species with a two-year life cycle will show little reduction. For this study we focused on the application of 4-poster devices treated with 10% permethrin (Y-TEX 4-poster Tickicide, Y-TEX Corporation, Cody, WY) in a large 52.6 km2 community where heavily human populated areas border heavily wooded areas and the density of devices is limited by financial considerations, available manpower, and regulations constraining the use of 4-poster devices in close proximity to residences.

This study was intended to clarify the efficacy of the retirement community's current tick mitigation efforts to evaluate real-world usage of 4-poster acaricide applicators as well as provide data for the design of improved integrated management options. We evaluated the percent reduction of tick populations at set distances from the 4-poster devices through comparison with non-treatment sites where 4-poster devices have never been used. Finally, we sought to determine the gradient of control of 4-poster acaricide applicators in this area by assessing the level of tick reduction at increasing distances from the devices.

MATERIALS AND METHODS

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Study area and selection of sampling sites

Our study site is a golf-oriented retirement community of roughly 6,000 residents which encompasses 5,260 ha of heavily wooded land on the Cumberland Plateau in Tennessee. The community's attractions consist of championship golf courses, tennis courts, swimming, lakes for boating and fishing, horseback riding, sightseeing, trails, and shopping. The border along the north end of the community is adjacent to a 32,370 ha wildlife management area and as a result, white-tailed deer and other wildlife are common throughout the community. The northern part of the community is considered to have higher tick abundance and disease risk because of this shared border (R. Gerhardt, personal communication). The fragmentation of the community as a result of interspersed fairways, woodlands, and residences provides ample wildlife habitat, and therefore the opportunity for tick populations to thrive (Allan et al. 2003, Brownstein et al. 2005).

The managers of the retirement community selected eight sites for deployment of 4-poster acaricide applicators treated with 10% permethrin, with site selection based on previous treatment locations, proximity to inhabited areas, and areas of known high tick abundance. Managers operated the 4-poster acaricide applicators from April through September and recharged the devices with permethrin and corn weekly. Four 4-posters were located in the northern half of the community and four were located in the southern half (Figure 1). This was the first year of treatment using 4-poster acaricide applicators at transects 1, 7, 8, and 9, whereas 4-poster treatment had been used for at least two years at transects 4, 5, 12, and 13. Mitigation techniques had never been attempted at the six non-treatment sites (2, 3, 6, 10, 11, and 14).

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Figure 1. Mean counts of nymphal and adult A. americanum at 14 sites within the study area. Adult means are for the period March 24 – June 16, 2009; nymphal means are for the period May 11 – July 27, 2009. Treatments include all distances from 4-poster devices, including the range at which control was not achieved (300–399 m). (T=treatment site, UT=untreated site).

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Sampling method

Ticks were collected by ‘dragging’ vegetation (Falco and Fish 1992) at approximately 4-week intervals during the ticks’ active season to determine seasonal changes in population density and distribution in the community. Researchers dragged a white 1×1 meter corduroy cloth along 400 m transects at the eight 4-poster acaricide applicator sites and at six additional non-treatment sites where no applicator was present. Drag cloths were checked for ticks at 10 m increments. At 4-poster sites, transects began at the applicators. Nymphal and adult ticks that attached to the drag cloth were accumulated and placed into separate vials of 70% ethanol at 40 m, 100 m, 200 m, 300 m, and 400 m distances from the applicator. Larval ticks were collected from drag cloths using lint roller sheets and labeled by transect and distance, matching the corresponding ethanol vials. This allowed for subsequent analysis of tick abundance relative to distance from the device. Sampling at non-treatment sites consisted of two 200 m transects through equivalent habitat with all adults and nymphs collected per transect accumulated into a single vial and larval ticks collected on a single lint roller sheet. Non-treatment sites were located at least 1 km away from treatment sites. To avoid any effect of tick removal on consecutive abundance estimates, transects were adjusted 5–10 m to the left or right of the previous transect each subsequent month. Ticks were brought to the University of Tennessee Medical and Veterinary Entomology Laboratory, where they were identified to species, life stage, and sex. Larval tick lint roller sheets were analyzed by overlaying a 7×9 grid on each used sheet. A random number generator allowed for assignment of half of the grids for subsequent tick identification. The counts were then doubled to estimate the number of larvae collected on each sheet.

Trail camera monitoring

To assess deer and non-target species use of the 4-posters, Bushnell trail cameras (Bushnell Corporation, Overland Park, KS) were operated for 1-week intervals on three occasions in May-July, 2010 at four sites where applicators were located. These motion-triggered cameras took a picture after each 10 s of animal activity. Analysis of trail camera photos involved counting individuals of each species present in each photograph. Due to difficulty in determining one individual from another, every animal was counted in every photo regardless of whether or not it was present in previous photographs. Our counts of wildlife therefore represent the level of activity of each wildlife species at the sites rather than abundance of each species at the sites (Jennelle et al. 2002, Oliveira-Santos et al. 2010).

Statistical analysis

To correct for differences in sampling effort, all larval, nymphal, and adult counts were converted to counts per 100 m of dragging. For statistical analysis, these corrected counts were then double-log transformed to normalize their variance structure and reduce the influence of outliers. When reporting results, means and standard errors for these transformed data were back-transformed so that plots and tables could be presented in units of tick counts per 100 m2 dragged.

As a measure of the abundance of questing nymphal and adult ticks that community residents are exposed to during the summer, we constructed a map showing average counts for the three peak months of nymphs and adults (April through June for adults; May through July for nymphs) at each of our sampling sites. Seasonal phenology was determined for adult, nymphal, and larval A. americanum ticks at treated and untreated sites from March, 2009-May, 2010 by calculating the mean number of collected ticks by visit for each transect and plotting these means vs week of visit. Differences in the abundance of nymphs and adults at treatment sites vs control sites were analyzed using separate General ANOVA models in Statistix 8 (Analytical Software, Tallahassee, FL) to assess TREATMENT, VISIT, and TREATMENT*VISIT effects. Interaction terms were non-significant, so these were removed and the models re-run.

Counts of ticks at specific distance intervals from the 4-poster applicators were compared using a General ANOVA model to assess DISTANCE, VISIT, and DISTANCE*VISIT effects, with the non-treatment area counts treated as a dummy distance category. Non-significant interactions were removed, and a post hoc Hsu's Multiple Comparisons test was run using Statistix 8 to assess the significance of differences of the tick counts at each distance interval vs tick counts at the non-treatment sites.

The 4-poster on treatment transect 5 required frequent maintenance due to damage by feral hogs, and we had problems with our transect markers being removed by local residents. Consequently we were concerned a priori about the data from this transect. Given that the counts from this transect were statistically outliers from the main data set (Figure 1), it seemed prudent to exclude them from the phenology and distance analyses described above.

RESULTS

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

The great majority of collected ticks (99.43%) were A. americanum followed by Dermacentor variabilis (0.47%) and Ixodes scapularis (0.10%). We excluded D. variabilis and I. scapularis from further analysis as their low abundance suggests they present minimal risk to humans in this community. In contrast, we found the A. americanum population to be widespread throughout the community, with all life stages of A. americanum ticks collected from all 14 sampling sites (Figure 1). Our data confirmed the perception of community managers that A. americanum numbers are highest in the northern part of the community. Sites in the northern half had an estimated 91% higher nymphal A. americanum population density and 35% higher adult A. americanum population density than did sites in the southern half of the community (Figure 1; p<0.001 for both comparisons). During the period of peak larval questing (August-October) the average abundance of larvae was 2.4 times higher on the northern transects than on the southern transects (p=0.0011). A strong seasonal effect was detected, with adults peaking slightly earlier in the year than nymphs. The observed seasonality was the same in the treatment and non-treatment areas, although there were fewer ticks overall at the treatment sites than at the non-treatment sites (Figure 2).

image

Figure 2. Seasonal variation in nymphal and adult tick abundance. Adults peak slightly before nymphal ticks and tick abundance at treated sites is less than at untreated sites in almost every month. Error bars indicate standard error.

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We observed a proximity effect of the 4-poster treatment on tick populations, with the treatment effect being statistically significant for nymphs and adults only within 300 m from the 4-poster. Therefore the diameter of measurable effect around the 4-poster acaricide applicators was 600 m (Figure 3). Treatment effects were more evident for nymphs than for adults, with an observed 68% reduction of nymphs and 49% reduction of adults within 40 m2 of the 4-poster devices (nymphal p<0.001, adult p=0.005). The overall 90.1% reduction of larval A. americanum ticks detected on treatment transects was highly significant compared to non-treatment sites for the entire sampled distance (Figure 4). These treatment effects existed at sites in the first year of treatment as well as sites in the second year of treatment, and the difference in effect for the two treatment classes was not significant.

image

Figure 3. Distance effect of 4-poster acaricide applicators on adult and nymphal tick abundance per 100m2; at alpha = 0.05, starred bars indicate tick abundance that significantly differs from untreated sites (UNT; nymphal p<0.001, adult p=0.005). Error bars indicate standard error.

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image

Figure 4. Distance effect of 4-poster acaricide applicators on larval tick abundance per 100 m2. At alpha = 0.05, tick abundance significantly differs from untreated sites up to 400 m from 4-poster acaricide applicators. Starred bars indicate statistical significance (p<0.001). Error bars indicate standard error.

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We obtained a total of 4,070 photographs from trail cams consisting of the following image counts for each species: 4,787 of deer, 1,694 of squirrels, 438 of raccoons, 285 of turkeys, 94 of crows, 54 of woodchucks, 50 of wild hogs, and one of a grey fox. Variation in activity was apparent, with as few as 56 photos taken during a session at one site and as many as 997 photographs taken during the same sampling period at another site.

DISCUSSION

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

Given the highly skewed relative abundance of collected tick species, the managers’ decision to focus tick mitigation strategies in this area specifically on management of A. americanum is appropriate. With limited resources for tick management, concentrating mitigation in the northern portion of the community may be favorable for better overall tick control. For long-term mitigation of ticks, management officials would likely benefit from investing in exclusion techniques to keep wildlife species from the bordering wildlife management area from coming into the community. In a similar area of Tennessee, this method in combination with vegetation management and acaricide application led to significant overall reduction of A. americanum compared to each mitigation method used alone (Bloemer et al. 1990).

The lower observed reduction in adults is likely a result of the relatively short time that the devices have been used at each site; half have been in use for only one year and thus have not had adequate time to impact the number of questing adults (i.e., adult ticks before they feed on deer). While 4-poster applicators have been used in the community prior to this study, management officials chose to relocate the devices every two years. The short duration of device deployment is therefore an aspect of the real-world management method we were assessing. Due to short periods of applicator use, we expect to see fewer nymphs in the second season of 4-poster utilization. It is also expected that a third year of treatment with 4-poster acaricide applicators will yield a larger percent reduction in the adult ticks. However, the lack of significance between the two treatment classes suggests that the decrease in ticks in close proximity may be a result of a high density of non-target wildlife hosts near the 4-poster devices rather than the acaricide treatment itself. Where high abundance of wildlife hosts exists, greater proportions of ticks are able to find hosts, decreasing the ability of drag sampling to accurately assess tick population density (Ginsberg and Zhioua 1999). The precise effect of high host activity on the presence of questing ticks near 4-poster acaricide applicators is unclear, but likely only occurs in close proximity of the devices. Environmental diffusion of acaracide to the vicinity of the 4-poster by wildlife, wind, rain, etc. may also contribute to the reduction of questing ticks.

Trail cams demonstrated that the 4-poster acaricide applicators were routinely used by non-target wildlife species often without those species coming into contact with the acaricide-treated paint rollers (Figure 5). The high number of photographed non-target wildlife at 4-poster acaricide applicator sites supports the hypothesis that the observed short-term (i.e., Year 1) decrease in ticks is a result of readily finding hosts near the acaricide applicators. High wildlife activity at the 4-poster devices also led to high corn consumption and thus increased costs of 4-poster maintenance. There are concerns that baiting individuals of several different wild species to a centralized feeding site could lead to the spread of other wildlife diseases, particularly if the 4-poster itself becomes a fomite. This is of particular concern in this area because of the community's proximity to a wildlife management area where the target species (deer) and many of the non-target species (turkey, hog, raccoon, and squirrel) are hunter harvested. The use of a battery-operated closure mechanism to block corn flow into 4-poster devices during the day can restrict feeding by squirrels without affecting deer usage (Carroll et al. 2008), however diurnal corn restriction would likely have little impact on feeding by nocturnal species such as raccoons. In several photographic series, certain species (primarily raccoons and hogs) were seen to chase deer away from the acaricide applicators and therefore prevent the target species from feeding and self-treating with acaricide. Future studies should assess whether being chased from 4-poster acaricide applicators has detrimental effects on deer self-treatment or whether deer simply return to the devices at a later time.

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Figure 5. Trail camera picture of a squirrel, a woodchuck, and a deer utilizing a 4-poster acaricide applicator. Non-target species were often documented at 4-poster devices.

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Given the relatively small effective area of the devices apparent from our data, and the large size of the study area, it is clear that eight devices are not sufficient to reduce the risk of tick-borne disease in the community as a whole. Additionally, because the majority of 4-poster acaricide applicators in this area are located on the perimeter of the community, a high likelihood exists that deer in the interior part of the community never came into contact with the devices. Again, these results emphasize the necessity for the community managers to consider integrated techniques rather than solely using acaricide self-treatment of deer for tick mitigation efforts. Considerable uncertainty exists among the community managers about the mode of action of the 4-poster acaricide applicators. One 4-poster was utilized in close proximity to a golf course and had to be moved elsewhere due to resident complaints of deer-vehicle collisions on a nearby road. Half of the 4-poster devices were moved to new sites at the beginning of our survey and almost all had been moved in the previous year. At the start of the 2010 treatment season, seven of the eight 4-poster acaricide applicators were moved to new sites due to concern of poachers potentially using the devices to illegally hunt deer in the community. The highly significant reduction of A. americanum larvae at treatment sites, in contrast to the significant but less extensive reduction seen in nymphs and adults, demonstrates the importance of leaving 4-poster devices at a site long enough to affect the tick population as a whole rather than just affecting one life stage. This result raises the question of whether a 90% percent reduction of A. americanum larvae in one year necessarily means parallel reduction will be seen in nymphs in the following year. Small mammals have been shown to replenish early stage ticks at deer-focused tick management sites (Ginsberg and Zhioua 1999), raising the possibility that the attraction of non-target species to 4-poster acaricide applicators could lead to re-infestation of nymphal or adult ticks, despite removal of the local larvae. Time constraints and community set-up hindered our ability to test farther than the original 400 m transect distance, therefore the extent of 4-poster device distance effect on A. americanum larvae is unclear.

Pound et al. (2009) estimated the cost of maintaining a 4-poster to be $21.40 per device per week including costs of labor, corn, and acaricide. Using this estimate, the cost of maintaining the eight 4-poster devices currently utilized at our study site is $685/month, or $4,100 for the six-month period in which the devices are deployed each year. Estimates of the cost of treatment for Ehrlichia infections are not available, so Lyme disease estimates are used here for cost comparison. The estimated median total cost of diagnosis and treatment for Lyme disease patients in the early stage is approximately $397, increasing to approximately $923 for clinically defined late-stage Lyme disease (Zhang et al. 2006). These figures could be used as a starting point to assess whether the decrease in tick numbers seen in this community is worth the amount of money necessary for maintenance of the 4-poster devices and the potential increased risk to wildlife health.

Recommendations of one 4-poster for every 20 ha (Schulze et al. 2007, Solberg et al. 2003) suggest that in order to manage ticks in an area of this extent, roughly 200 4-poster acaricide applicators would need to be deployed. Even if that quantity of devices was affordable, finding a sufficient number of suitable sites for that many 4-poster acaricide applicators is likely not feasible given current restrictions on 4-poster use within 100 yards of residential dwellings. Because of regulations on the devices, most being used in the community are in areas with a low likelihood of human presence. Given the history of tick-borne disease in the community and high exposure risk related to golfing, an ideal mitigation technique would be to create a buffer zone or cluster of 4-poster devices around golf courses where residents are most exposed to ticks. Spraying around golf courses with acaricide would likely work well to accomplish this goal, but further investigation into affordability of this technique should be undertaken. Integrating vegetation management such as overstory and understory reduction one to two times per year in high human populated area with 4-poster utilization in the more heavily wooded areas and exclusion fencing along the wildlife management area border is an option for controlling the tick population within this community. However, managing the tick population in the community does not automatically equate to mitigating tick-borne disease and while it is important not to worry people or scare them away from participating in outdoor activities, investing money into resident education may be the most economical and efficient way to reduce disease risk for this residential area.

Acknowledgments

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED

We thank Dave Paulsen for his expert identification of ticks, Ellen Baker and Michelle Rosen for countless hours of field assistance, Nick Hendershot for his help with trail camera data analysis, and Marcy Souza and Reid Gerhardt for planning and editing assistance. We also thank the UT Agricultural Experiment Station for funding this project.

REFERENCES CITED

  1. Top of page
  2. ABSTRACT:
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. Acknowledgments
  8. REFERENCES CITED
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