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. 2021 Aug 16;58(6):2358–2367. doi: 10.1093/jme/tjab131

Integrated Tick Management in South Central Wisconsin: Impact of Invasive Vegetation Removal and Host-Targeted Acaricides on the Density of Questing Ixodes scapularis (Acari: Ixodidae) Nymphs

Jordan T Mandli 1, Xia Lee 1, Gebbiena M Bron 1, Susan M Paskewitz 1,✉
Editor: Dina Fonseca
PMCID: PMC8824448  PMID: 34397096

Abstract

As tick-borne disease incidence increases and pathogens expand into new areas, the need for effective tick management strategies is paramount. In this 5-yr study (2014–2018) conducted in south central Wisconsin, we assessed whether an integrated tick management approach, deployed during peak tick activity (May–August), was more effective at reducing black-legged ticks (Ixodes scapularis Say (Ixodida: Ixodidae)), than individual interventions. Using a factorial design, invasive vegetation removal (Amur honeysuckle, Lonicera maackii Ruprecht (Dipsacales: Caprifoliaceae) and common buckthorn, Rhamnus cathartica Linnaeus (Rosales: Rhamnaceae)) was coupled with deployments of permethrin-treated cotton nesting materials (tick tubes) that target the white-footed mouse (Peromyscus leucopus Rafinesque (Rodentia: Cricetidae)). Results show that the probability of encountering a larval tick by drag sampling was unaffected by treatments at the cumulative 5-yr level. However, vegetation removal significantly reduced larval encounters in 2014, 2015, and 2018, by 33%, 57%, and 61% respectively, and reduced the density of questing nymphal (DON) ticks by 45% in 2015 compared to controls. Despite the limited effect on DON, vegetation removal significantly reduced the cumulative 5-yr density of Borrelia burgdorferi sensu stricto infected nymphs (DIN) (70%) compared to controls as a result of decreased nymphal infection prevalence. Sites treated with tick tubes had lower DIN (66%) and DON (54%) across the study and nymphs were reduced every year following the initial year of deployment compared to controls. Combining treatments did not further reduce DIN or DONs. We conclude that long-term integration of tick tubes with invasive vegetation removal does not provide additional benefit over individual treatments alone.

Keywords: black-legged tick, Lyme disease, permethrin-treated cotton, tick tube, phenology

In North America, Lyme disease (LD) is caused by the spirochete bacteria, Borrelia burgdorferi sensu stricto (s.s) and Borrelia mayonii (Burgdorfer et al. 1982, Pritt et al. 2016), and transmitted by Ixodes scapularis Say (Ixodida: Ixodidae) (black-legged tick) and Ixodes pacificus ticks Cooley and Kohls (Ixodida: Ixodidae) (western black-legged tick). LD is the most commonly reported vector-borne disease in the United States with approximately 400–500,000 human cases estimated to occur each year (Kugeler et al. 2021). In the absence of a vaccine, risk mitigation for LD has predominately focused on minimizing contact with host-seeking ticks through the use of personal protection and environmental control. Protective clothing, repellents, and tick checks are staples of personal protection against tick bites but require a consistent season-long commitment that is easily exhausted (Eisen and Eisen 2018). Implementation of environmental tick control strategies including broadcast acaricide application (Schulze et al. 1987, Hinckley et al. 2016), habitat modification (Wilson 1986, Stafford et al. 1998, Williams et al. 2017), and wildlife host-targeted approaches (Mather et al. 1987; Dolan et al. 2004, 2008; Kilpatrick et al. 2014; Williams et al. 2018) have successfully reduced densities of questing ticks in previous studies and do not rely on human behavioral changes. However, results are mixed and are often influenced by local environmental characteristics, the scale of treatment (temporal and spatial), and host community composition as reviewed by (Eisen and Eisen 2018). The complex ecological relationships between habitat, ticks, wild hosts, and tick-borne pathogens often limit the broad effectiveness of single interventions (Williams et al. 2018).

Integration of environmental tick control methods may offer a better approach to effectively reduce ticks and infection prevalence with the overall aim of decreasing LD cases (Ginsberg and Stafford 2014, Eisen and Stafford 2020). However, empirical evidence from studies designed to assess tick and pathogen suppression under integrated tick management (ITM), especially in the Midwest, is lacking (Bloemer et al. 1990, Schulze et al. 2007, Williams et al. 2018, Eisen and Stafford 2020). Evidence is needed to determine which combinations of safe interventions are most effective for public use while accounting for the increased costs associated with integration. Cost is a crucial factor for uptake of tick control methods: in a 2008 survey, a majority of respondents in endemic regions showed an unwillingness to spend more than $100 a year on tick control ($121 in 2021 dollars) (Gould et al. 2008, U.S. Bureau of Labor Statistics 2021). Employment of do-it-yourself (DIY) techniques are an alternative to expensive commercial products and services.

Vegetation management offers a simple DIY strategy for homeowners. Dense-growing invasive species like Japanese barberry (Berberis thunbergii de Candolle (Ranunculales: Berberidaceae)), common buckthorn (Rhamnus cathartica Linnaeus (Rosales: Rhamnaceae)), and Amur honeysuckle (Lonicera maackii Ruprecht) have been positively associated with questing tick abundance (Lubelczyk et al. 2004, Elias et al. 2006). These exotic invasive plants outcompete native species and generate impenetrable layers of vegetation that produce favorable microclimates that may facilitate black-legged tick survival, especially larvae, by minimizing changes in temperature, relative humidity, and the vapor pressure deficit (Stafford 1994, Williams et al. 2009). Invasive plants may also impact wildlife community composition in a way that supports minimal species diversity and increases tick interaction with more competent hosts (Berryman and Hawkins 2006, Allan et al. 2010). Elimination of dense vegetation by mechanical destruction or physical removal has been shown to reduce questing adult tick densities (Wilson 1986, Williams and Ward 2010, Williams et al. 2017). These data suggest that vegetation removal affects all life stages, possibly with a cumulative effect; however, evidence for the effectiveness on juvenile host-seeking I. scapularis at small scales (<1.0 ha) is deficient.

Geographic distribution of LD cases in the northeastern and upper midwestern United States is strongly correlated with the overlapping ranges of highly competent reservoir hosts and I. scapularis ticks (Tilly et al. 2008). Small rodents, including white-footed mice (Peromyscus leucopus), maintain and perpetuate the enzootic cycle of B. burgdorferi (Levine et al. 1985). Reservoir-directed acaricides can inhibit tick infestation of the host and thereby interrupt pathogen transmission between hosts and ticks. Commercially available products called “tick tubes” or “tick control tubes” accomplish this by providing permethrin-treated cotton for mice to use as nesting substrates (Spielman 1988). This strategy has resulted in a reduced infestation of larval ticks on mice as well as a reduction in the abundance of host-seeking nymphs in the environment in the following year (Mather et al. 1987, 1988). In one study where the treatment was deployed over a large area (7.3 ha), the number of host-seeking nymphs became nearly undetectable (Deblinger and Rimmer 1991). However, several trials at smaller scales (<1.0 ha) in New York and Connecticut have shown much more limited or non-significant impacts of tick tube deployment on questing nymphal densities or pathogen prevalence (Daniels et al. 1991; Stafford 1991, 1992). Thus, the effectiveness of host-targeted permethrin-treated cotton as a control method for black-legged ticks remains uncertain.

To address the need for effective low-cost interventions to reduce the number of infected I. scapularis nymphs in the environment, we implemented two DIY approaches, invasive vegetation removal (VR) and tick tubes containing permethrin-treated cotton (PTC). Using a factorial design, these two approaches were deployed individually and together during a five-year study in south central Wisconsin. Given that independent interventions have resulted in reductions in infected questing ticks in previous studies, we hypothesized that combined interventions would have an enhanced effect on the suppression of nymphal and infected nymphal abundance. Our study design also allowed us to evaluate the impact of tick tubes on reducing the density of nymphs in the south central Wisconsin.

Materials and Methods

Study Location

This five-year trial was conducted between 2014 and 2018 during peak questing activity from May to August at the University of Wisconsin (UW) Arboretum located in Madison, WI (WGS84: 43.04311, −89.42443). The UW Arboretum encompasses 486 ha of prairie, savanna, wetland, and deciduous forest surrounded by urban development. All study sites were located within a 50 ha oak-dominated forest with dense invasive vegetation dominating the forest understory. Tick collection in 2010–2011 confirmed this as a location with an established I. scapularis population. Before 2010, drag sampling efforts yielded no ticks suggesting the study location was only recently invaded.

Experimental Design

In a two-by-two factorial design, we evaluated a host-targeted intervention – permethrin-treated cotton nest material, and a habitat manipulation – invasive vegetation removal. Four treatment combinations were replicated four to five times (16–17 experimental sites): control sites underwent no invasive vegetation removal and received tick tubes containing untreated cotton nest material (CTRL), vegetation removal-only sites underwent invasive vegetation removal and received tick tubes containing untreated cotton nest material (VR), permethrin-treated cotton-only sites underwent no invasive vegetation removal and received tick tubes containing permethrin-treated cotton nest materials (PTC), and combined sites received both invasive vegetation removal and tick tubes containing permethrin-treated cotton nesting material (PTC + VR). Field crews were blinded to the permethrin-treated and untreated cotton intervention. In 2014, sixteen 50 × 50 m experimental sites were established, representing the average size of residential lots based on U.S. home sale census data from 2013 (U.S. Census Bureau 2017). These non-adjacent sites were first selected on a map and then verified for the presence of dense invasive understory vegetation consisting of common buckthorn (R. cathartica) and Amur honeysuckle (L. maackii), while hosting similar compositions of native vegetation. Sites were examined for barriers or large downed trees which might inhibit drag sampling and were spatially adjusted to avoid these obstacles. Distance between sites ranged from 35 to 610 m (Wolff 1985). Due to flooding in summer 2014, a PTC + VR site was relocated prior to the 2015 field season. At the same time, an additional site was established to increase the number of control sites to five for the remainder of the study.

Invasive Vegetation Removal

During site establishment in May 2014 and 2015, R. cathartica and L. maackii were identified and uprooted or clear-cut by trained field crews using loppers, handsaws, and brush cutters from a 20 × 20 m central plot embedded within the full 50 × 50 m experimental site (Fig. 1A). Vegetation removed from the central plot was transported outside the study site. The area not included in this central plot, but within the 50 by 50 m site was defined as the outer margins. In years following plot establishment, new growth of the targeted invasive species was similarly removed before each field season in early May by trained field crews. During removal of the two invasive species, care was taken to not remove non-targeted plant species and fallen trees were left undisturbed (Fig. 2). VR is expected to impact questing immature I. scapularis due to the physical removal, altered temperature and relative humidity conditions affecting tick survival, and altered rodent activity and thereby tick activity. These effects are expected to occur contemporaneously with plant removal and could amplify over time.

Fig. 1.

Fig. 1.

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A) Site layout with dimensions and region designations. B) Drag sampling scheme for central plot and outer margin. Central plot arrows represent 10 m. C) Tick tube deployment schema.

Fig. 2.

Fig. 2.

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Amur honeysuckle and common buckthorn in the understory of an oak-dominated forest A) before eradication and B) after eradication. University of Wisconsin Arboretum, Madison, WI.

Tick Tube Deployment

Twenty-five tubes were deployed across each site approximately 10 m apart, in line with recommended deployment densities of commercial tick tubes, with an emphasis on placement at preferred rodent habitat at the base of trees or along with downed logs (Fig. 1B). Permethrin-treated cotton was prepared from the Tengard SFR One Shot commercial permethrin product during 2014–2016 (United Phosphorus Inc., King of Prussia, PA) or the ProZap Insectrin X 10% permethrin concentrate in 2017 and 2018 (Chem-Tech Ltd., Lexington, KY) (providers were changed due to availability). Stock solutions were diluted with water to produce a 10% experimental formulation that was applied to cotton using a 7.6 liter pump sprayer (Roundup, Marysville, OH). Untreated cotton was prepared with water in a similar fashion, but in a separate location and sprayed using a dedicated 7.6 liter pump sprayer. Cotton tube reservoirs were prepared by cutting 6.1 cm (2.4 in) × 3.05 m (10 ft) PVC tubing into lengths of approximately 15.2 cm (6.0 in). Cotton was stuffed into each tube until a 2.54 cm (1 in) lip without cotton was generated at both ends (17 cotton balls per tube). Tick tube deployment occurred once before the peak of nymphal and larval activity during 2014–2015 (mid-May) and twice in 2016–2018 (mid-May and early to mid-July) with the second deployment designed to affect ticks that were active later in the season. Tubes were recovered from the field in October before snowfall and PVC tubes were reused each year. Permethrin-treated cotton is not expected to influence questing larvae as permethrin kills ticks feeding on mice, and questing larvae are predominately newly hatched from eggs. Reductions in questing nymphs due to PTC are expected a year after initial deployment, as reductions depend on the number of successfully fed larval ticks that overwinter and molt after the previous year. On PTC plots, a proportion of larvae are expected to attach to PTC-treated mice and be killed thereby not becoming part of the next season’s nymphal tick population.

Nest Material Usage

Presence of cotton nesting material in tubes and the surrounding area was monitored in 2014 through 2018 at the time of second tick tube deployment or tube collection at the end of the season. Data from 2018 are not discussed given the lack of effect on questing ticks within the study period. Due to a lack of observed uptake in early 2017, nesting material usage was quantified following the early deployment (May–July: ~ 55 d post-deployment) and once again following the late deployment (July–October: ~ 70 d post-deployment). For quantifying nest material usage, remaining cotton balls were individually counted and compared to amounts originally deployed.

Drag Sampling for Questing I. scapularis

The density of questing I. scapularis was estimated by drag sampling the forest floor with a 1.0 m2 white flannel cloth attached to a wooden dowel (drag). Drags were thoroughly examined every 10 m. All ticks discovered on drags were removed and placed in vials containing 70% ethanol. Collections of host-seeking I. scapularis occurred once a month during the first two weeks of the month from May to August. In 2014 and 2018, we could not conduct tick drag sampling during the month of May due to the availability of field personnel. In 2016, drag sampling was delayed in July due to weather (completed in the third week of July). During each monthly collection, a total of 800 m2 was drag sampled: the entire central plot (400 m2) and 100 m2 on each side of the central plot in the outer margins (400 m2; Fig. 1C). While we collected nymphs from the relocated combined site in 2015, these were not included in the 2015 dataset because of the delayed effect of PTC on host-seeking nymphs. Additionally, one control site was not drag sampled in May of 2015 due to flooding.

Tick Identification

Ticks collected from the field were identified to species and life stage using taxonomic keys (Clifford et al. 1961, Keirans and Litwak 1989, Durden and Keirans 1996). Ixodes scapularis nymphs were placed in individually marked 1.5 ml vials and stored at −20°C for DNA extraction and PCR analysis.

Borrelia burgdorferi s.s. Screening of I. scapularis Nymphs

Genomic DNA was extracted from bisected field-collected nymphs using the Bioline Isolate II Genomic DNA Extraction Kit (Bioline USA Inc., Taunton, MA) or the DNeasy Blood and Tissue Kit (Qiagen, Valencia, CA) according to the manufacturer’s instructions. Nymphs were tested for B. burgdorferi by nested polymerase chain reaction (PCR) targeting the outer surface protein B operon as previously described (Caporale and Kocher 1994, Lee et al. 2014). All collected nymphs were screened for B. burgdorferi with the exception of 40 nymphs from May 2017 that were lost after being identified.

Statistical Analysis

Nesting Material Assessment

For 2017, the number of remaining cotton balls was summarized as mean cotton balls per tube by site, and differences between treated and untreated cotton balls were compared using Welch’s two sample t-tests.

Treatment Effect on Immature I. scapularis

The effect of the treatments, PTC, VR, and PTC + VR on larval encounters, density of nymphs, and density of infected nymphs was assessed by multivariable analyses using generalized linear models (GLMs) for each year and generalized linear mixed effect models (GLMMs) when accounting for random effects in the cumulative study. Because PTC is expected to have a delayed impact on nymphs, PTC and PTC + VR data points from 2014 were removed from the cumulative analysis for DON and DIN. These statistical approaches were chosen because of the advantages of including multiple variables, adjusting for repeated measures, and processing non-normal data without transformation. Model fixed effects included Year, Month, and Treatments. Site was included as a random effect in GLMMs to control for natural variation among plots and autocorrelation (Richer et al. 2014, Cayol et al. 2018). Model selection was carried out based on corrected Akaike Information Criterion for small sample sizes (AICc) (Burnham and Anderson 2002). The simplest model containing treatment effects (PTC, VR, and PTR + VR) within 2 AICc of the model with the lowest AICc value was selected. Post-hoc tests assessing relative excess risk due to interaction (RERI-delta method) and multiplicative interaction were completed (VanderWeele and Knol 2014). Analysis was carried out in R version 1.3.959 (R Core Team 2019). GLMMs were developed in the lme4 package (Bates et al. 2015). Treatment effect associations were compared to CTRL unless otherwise stated.

Ixodes scapularis Larval Encounters

Larval encounters (LE) were reported as positive bivariate outcomes (i.e., the absence of larvae or presence of at least one larval tick per 10-meter drag sampled). We analyzed LE to alleviate skewness created by the clustering of recently hatched larvae. LE were modeled using logistic regression (with logit-link function) and relative risk was expressed as odds ratios (OR).

Ixodes scapularis Nymphal Density

Density of questing I. scapularis nymphal ticks (DON) was estimated as the sum of nymphs collected per 100 m2 of each site by Year/Month (same area dragged each time). In 2014, two instances of DON outliers were identified using a standard interquartile range assessment (1.5 * IQR) of total nymphs collected during that year and these were removed from the dataset. These outlying datapoints were of CTRL plot origin and greatly exceeded other CTRL plots. DON was modeled using negative binomial regression (with log-link function) and relative risk was expressed as incidence rate ratios (IRRs).

Infected I. scapularis Nymphal Density

Density of infected questing I. scapularis nymphal ticks (DIN) was estimated as the number of infected nymphs collected per 100 m2 of each site by Year/Month. DIN was modeled using negative binomial regression (with log-link function) and relative risk was expressed as incidence rate ratios (IRRs).

Results

Nesting Material Assessment

During the first three years (2014–2016), less than 5% of the cotton nesting material remained in tubes or on the ground nearby. In 2017, 48% (3,456/7,225) of the cotton balls remained at the conclusion of the first deployment (May–July). Closer examination revealed that PTC was removed less frequently than untreated cotton (UTC) with a mean 11.2 (95% CI: 9.53–12.8) and 5.44 (95% CI: 3.59–7.38) remaining balls per tube respectively (t = 4.18, P < 0.001). During the second deployment in 2017 (July–October), only 3% (227/7,225) of the cotton nesting material was left uncollected, aligning with trends seen in previous years. No difference in removal of treated or untreated nest material was detected with a mean 0.7 (95% CI: 0.39–1.04) (PTC) and 0.39 (95% CI: 0.19–0.62) (UTC) residual balls per tube (t = 1.39, P = 0.19).

Ixodes scapularis Abundance and Phenology

Over the course of the five-year study, a total of 8,348 I. scapularis larvae and 998 nymphs were collected. There was a high variation in abundance between years (Fig. 3, Supp Table 1 [online only]). Larval tick abundance declined precipitously with 93% fewer larval encounters sampled in 2018 as compared to 2014 (Fig. 3, Table 1). Nymphal tick abundance was also skewed: 53% of all nymphs captured during the five years were collected in 2015 (Supp Table 1 [online only]). Reduced nymphal tick abundance was observed in 2014, 2016, and 2018, suggesting a fluctuating two-year pattern (Fig. 3, Supp Table 1 [online only]). Two distinct questing patterns were detected for larvae. In 2014, 2016, and 2017 a unimodal larval peak was detected late in the season typically during the month of August (Fig. 3). In 2015, a bimodal distribution was detected with an early peak in June and a larger peak in August. In 2018, the abundance of questing larvae was too low to decern a clear trend in larval questing activity. Conversely, nymphs consistently displayed a unimodal pattern in which peak abundance occurred in May/June and declined through the rest of the season (Fig. 3).

Fig. 3.

Fig. 3.

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Total number of larvae and nymphs per 100 m2 of drag sampling per month by year and five-year average.

Table 1.

Sitewide GLMM results from the impact of tick tube and invasive vegetation removal on I. scapularis ticks larval encounters (LE), density of nymphs (DON), and density of infected nymphs (DIN) for the cumulative project (DIN and DON exclude 2014 PTC and PTC + VR values) Baseline effects are year: 2014, month: May, and treatment: CTRL. Differences between minimal model and best model given as 𝚫AICc. Additive and multiplicative interaction reported as RERI and ratio of ORs or IRRs (95% CI) respectively

Fixed Effects Larval Encounters (LE) ΔAICc = 2020 Density of Nymphs (DON) ΔAICc = 222 Density of Infected Nymphs (DIN) ΔAICc = 46
OR 95% CI P-value IRR 95% CI P-value IRR 95% CI P-value
Cumulative 2015 0.54 0.5–0.6 <0.001 15.68 8.5–28.8 <0.001 24.24 3.0–197.7 0.003
2016 0.20 0.2–0.3 <0.001 2.51 1.3– 4.7 0.004 2.52 0.3–24.0 0.422
2017 0.07 0.06–0.1 <0.001 5.94 3.2–11.0 <0.001 11.59 1.4–96.7 0.024
2018 0.07 0.05–0.09 <0.001 3.75 2.0–7.1 <0.001 5.67 0.6–49.5 0.117
June 0.95 0.7–1.3 0.703 1.34 1.0–1.7 0.021 2.65 1.2–5.7 0.013
July 0.55 0.4–0.8 <0.001 0.66 0.5–0.9 0.002 0.86 0.4–2.0 0.737
August 6.39 5.0–8.2 <0.001 0.31 0.2–0.4 <0.001 0.24 0.08–0.7 0.014
PTC 1.07 0.6–2.0 0.815 0.46 0.2–0.9 0.017 0.34 0.1–0.8 0.016
VR 0.85 0.5–1.5 0.591 0.57 0.3–1.1 0.087 0.30 0.1–0.7 0.008
PTC + VR 0.85 0.5–1.6 0.598 0.61 0.3–1.2 0.131 0.33 0.1–0.8 0.019
RERI −0.07 −0.9–0.8 0.58 0.08–1.1 0.69 0.2–1.1
Multiplicative 0.94 0.4–2.2 2.33 0.9–6.0 3.26 0.8–13.0
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Ixodes scapularis Larval Encounters

LE were better explained by the cumulative five-year model including Year, Month, and Treatment effects and annual models including Month and Treatment effects compared to the intercept-only model. LE were not significantly associated with any treatment across the cumulative five-year study (Table 1). VR significantly reduced the likelihood of encountering a larva in 2014 (OR: 0.67, 95% CI: 0.5–0.9) and 2015 (OR: 0.43, 95% CI: 0.3–0.6) and 2018 (OR: 0.39, 95% CI: 0.2–0.9), and substantially reduced LE in 2017 (OR: 0.44, 95% CI: 0.2–1.0). In 2016, CTRL exhibited a large decline in larval abundance which resulted in greater LE in VR plots compared to CTRL (OR: 2.18, 95% CI: 1.4–3.3). In 2014 and 2015, the negative impact of PTC + VR on annual LE was similar to VR plots, but to a lesser extent (Table 2). Likewise, the probability of encountering larvae in PTC + VR plots increased in 2016. LE probability was lower in PTC plots solely in 2015 (Table 2). There were indications of joint effect on the additive scale (RERI) and multiplicative scale for integrated treatments. In 2015 and 2018, the RERI was 0.36 (95% CI: 0.1–0.6) and 0.72 (95% CI: 0.1–1.33) respectively, indicating a super-additive effect of treatments on LE (the observed impact of PTC + VR on LE was less than what was expected for individual treatments added together) (Table 2). In 2015, the ratio of ORs was 1.67 (95% CI: 1.1–2.6), indicating the presence of a positive joint effect of treatments on the multiplicative scale. (the observed impact of PTC + VR on LE was less than what was expected for individual treatments multiplied together)

Table 2.

Sitewide results from the impact of tick tube and invasive vegetation removal on I. scapularis ticks larval encounters (LE) and density of nymphs (DON) by individual year (Data from GLMs). Baseline treatments are month: May or June and treatment: CTRL. Differences between minimal model and best model given as 𝚫AICc. Additive and multiplicative interaction reported as RERI and ratio of ORs or IRRs (95% CI) respectively

Larval Encounters (LE) ΔAICc = 836 Density of Nymphs (DON) ΔAICc = −5
Fixed Effects OR 95% CI P-value IRR 95% CI P-value
2014 July 0.05 0.02–0.1 <0.001 0.26 0.07–0.7 0.020
Aug. 9.58 7.4–12.6 <0.001 0.36 0.1–0.9 0.050
PTC 1.05 0.8–1.4 0.724 0.78 0.2–2.5 0.676
VR 0.67 0.5–0.9 0.007 0.93 0.3–2.9 0.893
PTC + VR 0.55 0.4–0.7 <0.001 0.53 0.1–1.9 0.323
RERI −0.17 −0.5 to 0.2 −0.18 −1.6 to 1.3
Multiplicative 0.78 0.5–1.2 0.72 0.1–3.9
Larval Encounters (LE) ΔAICc = 187 Density of Nymphs (DON) ΔAICc = 20
Fixed Effects OR 95% CI P-value IRR 95% CI P-value
2015 June 1.03 0.7–1.5 0.881 2.18 1.4–3.4 <0.001
July 0.91 0.6–1.3 0.632 1.57 1.0–2.4 0.048
Aug. 3.87 2.9–5.3 <0.001 0.74 0.4–1.2 0.207
PTC 0.76 0.6–1.0 0.039 0.48 0.3–0.7 <0.001
VR 0.43 0.3–0.6 <0.001 0.55 0.3–0.8 0.003
PTC + VR 0.55 0.4–0.7 <0.001 0.42 0.3–0.7 <0.001
RERI 0.36 0.1–0.6 0.39 −0.01 to 0.7
Multiplicative 1.67 1.1–2.6 1.59 0.8–3.0
Larval Encounters (LE) ΔAICc = 192 Density of Nymphs (DON) ΔAICc = 21
Fixed Effects OR 95% CI P-value IRR 95% CI P-value
2016 June 0.25 0.07–0.7 0.013 0.64 0.4–1.0 0.078
July 2.16 1.24.0 0.012 0.25 0.1–0.5 <0.001
Aug. 7.95 4.8–14.0 <0.001 0.17 0.07–0.3 <0.001
PTC 0.63 0.4–1.1 0.109 0.45 0.2–0.8 0.015
VR 2.18 1.4–3.3 <0.001 0.86 0.5–1.5 0.568
PTC + VR 1.86 1.2–2.9 0.005 0.46 0.2–0.8 0.018
RERI 0.06 −0.8 to 0.9 0.16 −0.4 to 0.7
Multiplicative 1.36 0.7–2.7 1.21 0.5–3.1
Larval Encounters (LE) ΔAICc = 114 Density of Nymphs (DON) ΔAICc = 25
Fixed Effects OR 95% CI P-value IRR 95% CI P-value
2017 June 0.20 0.01–1.2 0.141 0.87 0.5–1.3 0.511
July 0.60 0.1–2.4 0.484 0.64 0.4–1.0 0.054
Aug. 12.34 5.4–35.4 <0.001 0.18 0.1–0.3 <0.001
PTC 1.26 0.7–2.3 0.449 0.46 0.3–0.8 0.003
VR 0.44 0.2–1.0 0.052 0.83 0.5–1.3 0.410
PTC + VR 0.91 0.5–1.7 0.767 0.73 0.5–1.1 0.168
RERI 0.20 −0.6 to 1.0 0.43 −0.03 to 0.9
Multiplicative 1.61 0.6–4.8 1.88 0.9–3.8
Larval Encounters (LE) ΔAICc = 36 Density of Nymphs (DON) ΔAICc = 39
Fixed Effects OR 95% CI P-value IRR 95% CI P-value
2018 July 4.9E−9 1.8E−246–1.5E23 0.991 0.11 0.05–0.2 <0.001
Aug. 0.96 0.6–1.7 0.888 0.04 0.01–0.1 <0.001
PTC 0.56 0.3–1.2 0.134 0.35 0.2–0.7 0.007
VR 0.39 0.2–0.9 0.032 0.74 0.4–1.4 0.359
PTC + VR 0.68 0.3–1.4 0.280 0.86 0.5–1.6 0.625
RERI 0.72 0.1–1.33 0.77 0.2–1.4
Multiplicative 3.08 0.9–10.8 3.33 1.2–9.5
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Ixodes scapularis Nymphal Density

The density of nymphs (DON) was better explained by the cumulative five-year model including Year, Month, and Treatment effects and annual models including Month, and Treatment effects compared to the intercept-only model. A lack of a positive change in AICc (ΔAICc) in the 2014 annual model was a strong indicator that the treatments were not predictive of DON in that year. Across all other years of the study, PTC was negatively associated with DON (Table 1). At the cumulative level, PTC plots exhibited a 53% reduction in DON compared to controls (Table 1). After the initial year of treatment, DON was negatively associated with PTC during each subsequent year and with PTC + VR in 2015 and 2016 (Table 2). Comparing the impact of PTC with PTC + VR, we observed that DON tended to be higher in the PTC + VR treatment plots compared with PTC alone starting in 2017 (Table 1, Supp Table 1 [online only]). For example, DON was 2.5 times greater in PTC + VR plots compared with PTC only plots in 2018 (Table 2). No impact of single versus two PTC treatments was detected on DON. Densities of nymphs were substantially reduced (OR: 0.57, 95% CI: 0.3−1.1) by VR across the study (Table 1), and VR was negatively associated with DON in 2015 (Table 2). At the cumulative level, a super-additive effect was detected (the impact of PTC + VR on DON was less than what was expected for individual treatments added together) (RERI: 0.58, 95% CI: 0.08–1.1). This was also evident in 2015 (RERI: 0.39, 95% CI: 0.07–0.7) and 2018 (RERI: 0.77, 95% CI: 0.2–1.4). The ratio of IRRs was 3.33 (95% CI: 1.2–9.5) in 2018 indicating the presence of a positive joint effect of treatments at the multiplicative scale.

Infected I. scapularis Nymphal Density and Prevalence

Prevalence of B. burgdorferi in nymphal ticks remained low throughout the study limiting our ability to model treatment effect on the density of infected nymphs (DIN) in each year. During the five-year study, only 9% (n = 920) of all nymphs captured within the experimental plots were infected with B. burgdorferi (Supp Table 1 [online only]). Annual B. burgdorferi prevalence in nymphs was 13% (n= 22) in 2014, 9% (n = 525) in 2015, 5% (n = 97) in 2016, 13% (n = 166) in 2017, and 10% (n = 100) in 2018. DIN models including Year, Month, and Treatment performed better than the intercept only model (Table 1). Both PTC and VR were negatively associated with DIN across the cumulative study with reductions of 66% and 70% respectively. Similarly, the likelihood of collecting a Borrelia-positive nymph decreased by 67% on the PTC + VR plots. The presence of super-additive interaction was detected (RERI: 0.69, 95% CI: 0.2–1.1).

Discussion

During five years of integrated tick management, both PTC and VR reduced the density of infected nymphal I. scapularis. However, integration of treatments did not significantly improve outcomes. Observed reductions of DON (53%) and DIN (66%) by PTC support the value of this intervention in reducing nymphal ticks. As expected, PTC exhibited a delayed impact on DON and reliably reduced nymphal densities in all years after the initial deployment. While these results do not achieve the level of effectiveness reported by Mather and colleagues (89% reduction in DON and 97% reduction in DIN) (Mather et al. 1988), PTC was an effective intervention to reduce the density of infected nymphs at a small scale in a newly invaded area in south central Wisconsin. Conversely, VR had no significant cumulative impact on DON, but a negative effect was detected the year after initial treatment (2015). Unexpectedly, despite the limited impact on DON, VR reduced the overall DIN by 70%. This suggests the presence of an undetected mechanism that hinders nymphal infection or affects the presence, likelihood of collection, or survival of nymphs infected with B. burgdorferi more strongly.

We originally hypothesized that integration of VR and PTC would have an enhanced impact on the reduction of DIN and DON. However, the interaction of PTC and VR suggested a diminished impact of treatments when integrated. It is suspected that VR plots had little ground cover and were open which may have altered mouse foraging activity thereby modifying the distribution of PTC among the local mouse community. Alternatively, this landscape modification could have changed the behavior and availability of alternative hosts, offsetting the reductions due to PTC.

While we did not measure changes to temperature and humidity in our sites, the removal of invasive vegetation resulted in seven times greater light penetration at the forest floor compared to vegetation intact sites (Bartowitz and Orrock 2016). This increase in solar radiation altered abiotic conditions. Therefore, declines in LE could have been caused by the removal of favorable microclimates for questing, as proposed by Williams et al. (2009), or may have increased larval tick mortality.

Removal of invasive vegetation has been shown to decrease adult black-legged tick densities 2–3 yr following removal (Williams and Ward 2010, Williams et al. 2017). However, our results show a limited effect of VR on nymphal densities. Impacts of treatments on adult tick densities may be more readily detectable due to an accumulated effect. In this study, resources constrained our ability to examine questing adult density, which typically peaks during October/November. These observations indicate a need to evaluate the effect of VR on all life stages in future work. Additionally, easier drag sampling in VR-treated areas may have facilitated more direct contact with the ground substrates. While VR may reduce the presence of ticks, it could also have improved sampling conditions.

This study was designed to reflect ITM at residential plot sizes in the Upper Midwest. Scale has been implicated as a key factor influencing treatment outcomes. For example, effectiveness of tick tubes has been shown to be less reliable when distributed on plots of less than 1.0 ha (Daniels et al. 1991, Stafford 1991, 1992). At a small scale, immigration of black-legged ticks from outside the treated area, as a result of the movement of larvae by P. leucopus or other hosts, may inflate the number of host-seeking nymphs and reduce treatment effects. Furthermore, when mouse densities are low, individual mice may travel further, collect more ticks, and facilitate increased tick migration into sites (Wolff 1985, Ostfeld et al. 1996). Our results demonstrate that reductions of nymphs by PTC can be achieved even within small scale treatment plots, which differs from some prior studies (Daniels et al. 1991; Stafford 1991, 1992). However, the ecological conditions of our treatment plots in an urban forest may not fully reflect those of residences or neighborhoods used in previous unsuccessful trials. For example, small, fragmented patches of forest (less than 0.5 ha), common in urban areas, have the potential to concentrate mice and ticks (Barko et al. 2003, Nupp and Swihart 2011). This suggests that a uniform treatment of PTC around a residence may not be effective if ticks and mice originate from nearby untreated patches. Additionally, our study was implemented in a newly invaded area. Tick densities were much lower than previous trials of tick tubes that occurred in the northeast. Therefore, PTC may be more effective at inhibiting tick feeding when densities are lower. Further investigation is warranted to examine how PTC effectiveness varies under different scales and tick densities.

Complete cotton removal from tick tubes occurred throughout the study with the exception of 2017. Roughly half of all nesting material, especially cotton treated with permethrin, was discovered uncollected from tick tubes during redeployment midway through the 2017 season (July). A change to a more aromatic commercial permethrin product may have contributed to the lower cotton removal; however, material uptake returned to normal levels during the second deployment. Subdued uptake may also have been the result of a low mouse population during 2017 (Mandli Doctoral Thesis 2021). In contrast to previous reports of poor control of questing nymphs following periods of low cotton collection (Daniels et al. 1991; Stafford 1991, 1992), our study demonstrated significant effects of PTC on DON the following year. In this case, protection may have been established during the second deployment prior to peak larval activity. Regardless, the impacts of mouse population dynamics on uptake and material dispersal remain unknown and warrant further investigation.

Both immature stages of I. scapularis feed on similar hosts. The ≥2-yr lifecycle of the tick is such that nymphs are often active before larvae of the following generation. Many tick-borne pathogens like B. burgdorferi are transmitted between cohorts of ticks by passage through competent hosts, thus maintaining the cycle of infection. We documented seasonal activity of immature ticks with peak nymphal abundance occurring in May/June and two distinct patterns of larval abundance characterized by unimodal or bimodal peaks subject to diapause (Ogden et al. 2018). Observed larval and nymphal asynchrony closely aligns with tick questing and feeding patterns reported in northern Illinois (Siegel et al. 1991, Jones and Kitron 2000), but we also detected variability between years. Elements of synchronous and asynchronous phenology, as well as unimodal and bimodal juvenile tick phenologies have been reported throughout the upper Midwest (Siegel et al. 1991, Lindsay et al. 1999, Jones and Kitron 2000, Gatewood et al. 2009, Hamer et al. 2012). Therefore, tick questing patterns are not static, but constitute a continuum of phenologies across space and time (Hamer et al. 2012). Successful use of tick tubes may require both spring/early summer and mid/late summer deployments to address variability in seasonal activity.

Environmental and ecological relationships further define the local B. burgdorferi sylvatic cycle (Arsnoe et al. 2015, Eisen et al. 2016). Successful implementation of environmental control methods requires interventions and operational strategies that align with these conditions and achieve protection during periods of greatest transmission. For example, PTC is likely to be ineffective in settings in which P. leucopus is not the primary reservoir or if tick tubes are deployed following peak juvenile tick activity. If control remains the responsibility of homeowners, regional testing of ITM and guidance is imperative to helping the public implement successful cost-conscious strategies.

Cost represents a key barrier to widespread use and acceptance of ITM strategies (Gould et al. 2008, Eisen and Eisen 2018, Jordan and Schulze 2019). DIY approaches offer an attractive alternative to expensive control practices at the expense of effort especially in the context of ITM. There are currently no permethrin products that are labeled for treatment of cotton nest material, so the use of permethrin for home-made tick tubes would be off-label use of pesticide at this time and therefore illegal for PCO’s and the general public. However, commercially available products like Damminix tick tubes (Ecohealth, Inc., Brookline, MA) and Thermacell tick control tubes (Thermacell Repellents, Inc., Bedford, MA) offer readily available alternatives (~$75 per case of 24 tick tubes; sufficient to cover 0.40 ha). The commercial products also provide consistent and even application of acaricide to nesting material. Nonetheless, tube placement by homeowners, yard composition, and proximity to other public or privately-owned forested sites may be variable and could alter the effectiveness of the intervention.

In summary, we evaluated the impact of integrated DIY control strategies on host-seeking I. scapularis in south central Wisconsin. Following five years of intervention, we determined that PTC and VR effectively reduce infected host-seeking nymphs; however, the treatment combination does not yield improved results. Further investigation is needed to identify tick control approaches that offer complementary protection, especially when effectiveness is delayed. As part of the ongoing efforts to provide guidance to the public, future research is warranted to assess the potential of alternative cost-conscious ITM combinations, continue refinement of established techniques, and determine how reductions in DIN translate into reduced human Lyme disease risk.

Supplementary Material

tjab131_suppl_Supplementary_Table_S1
Click here for additional data file. (99.7KB, pdf)

Acknowledgments

We thank the following individuals for their support of our research efforts: staff at the UW Arboretum, especially ecologist Brad Herrick; K. Bartowitz and J. Orrock for advice on experimental design and assistance in the field; Sam Engle with the UW College of Agricultural and Life Science Statistical Consulting Center; and our undergraduate and graduate students for their help with field work. Jordan Mandli was a doctoral student supported by the Parasitology and Vector Biology Training Program T32AI007414. Gebbiena Bron was supported by the Centers for Disease Control and Prevention, Cooperative Agreement Number U01CK000505. This work was supported by the USDA National Institute of Food and Agriculture, Hatch project 0232758 and the Centers for Disease Control and Prevention, Cooperative Agreement Number U01CK000505. Its contents are solely the responsibility of the authors and do not necessarily represent the official views or position of the Centers for Disease Control and Prevention, the Department of Health and Human Services, or the U.S. Government.

References Cited

  1. Allan, B. F., Dutra H. P., Goessling L. S., Barnett K., Chase J. M., Marquis R. J., Pang G., Storch G. A., Thach R. E., and Orrock J. L.. . 2010. Invasive honeysuckle eradication reduces tick-borne disease risk by altering host dynamics. Proc. Natl. Acad. Sci. U. S. A. 107: 18523–18527. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arsnoe, I. M., Hickling G. J., Ginsberg H. S., McElreath R., and Tsao J. I.. . 2015. Different populations of blacklegged tick nymphs exhibit differences in questing behavior that have implications for human lyme disease risk. PLoS One. 10: e0127450. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barko, V. A., Feldhamer G. A., Nicholson M. C., and Davie D. K.. . 2003. Urban habitat: a determinant of white-footed mouse (Peromyscus leucopus) abundance in southern Illinois. Southeast. Nat. 2: 369–376. [Google Scholar]
  4. Bartowitz, K. J., and Orrock J. L.. . 2016. Invasive exotic shrub (Rhamnus cathartica) alters the timing and magnitude of post-dispersal seed predation of native and exotic species. J. Veg. Sci. 27: 789–799. [Google Scholar]
  5. Bates, D., Mächler M., Bolker B., and Walker S.. . 2015. Fitting linear mixed effects models using lme4. J. Stat. Softw. 67: 1–48. [Google Scholar]
  6. Berryman, A. A., and Hawkins B. A.. . 2006. The refuge as an integrating concept in ecology and evolution. Oikos. 115: 192–196. [Google Scholar]
  7. Bloemer, S. R., Mount G. A., Morris T. A., Zimmerman R. H., Barnard D. R., and Snoddy E. L.. . 1990. Management of lone star ticks (Acari: Ixodidae) in recreational areas with acaricide applications, vegetative management, and exclusion of white-tailed deer. J. Med. Entomol. 27: 543–550. [DOI] [PubMed] [Google Scholar]
  8. Burgdorfer, W., Barbour A. G., Hayes S. F., Benach J. L., Grunwaldt E., and Davis J. P.. . 1982. Lyme disease-a tick-borne spirochetosis? Science. 216: 1317–1319. [DOI] [PubMed] [Google Scholar]
  9. Burnham, K. P., and Anderson D. R.. . 2002. Model selection and multi-model inference: a practical information-theoretic approach. Springer, New York. [Google Scholar]
  10. Caporale, D. A., and Kocher T. D.. . 1994. Sequence variation in the outer-surface-protein genes of Borrelia burgdorferi. Mol. Biol. Evol. 11: 51–64. [DOI] [PubMed] [Google Scholar]
  11. Cayol, C., Jääskeläinen A., Koskela E., Kyröläinen S., Mappes T., Siukkola A., and Kallio E. R.. . 2018. Sympatric Ixodes-tick species: pattern of distribution and pathogen transmission within wild rodent populations. Sci. Rep. 8: 16660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Clifford, C. M., Anastos G., and Van der Borght-Ebl A.. . 1961. The larval ixodid ticks of the eastern United States (Acarina-Ixodidae). Misc. Publ. Entomol. Soc. Am. 2: 213–237. [Google Scholar]
  13. Daniels, T. J., Fish D., and Falco R. C.. . 1991. Evaluation of host-targeted acaricide for reducing risk of Lyme disease in southern New York state. J. Med. Entomol. 28: 537–543. [DOI] [PubMed] [Google Scholar]
  14. Deblinger, R. D., and Rimmer D. W.. . 1991. Efficacy of a permethrin-based acaricide to reduce the abundance of Ixodes dammini (Acari: Ixodidae). J. Med. Entomol. 28: 708–711. [DOI] [PubMed] [Google Scholar]
  15. Dolan, M. C., Maupin G. O., Schneider B. S., Denatale C., Hamon N., Cole C., Zeidner N. S., and K. C.Stafford, 3rd. 2004. Control of immature Ixodes scapularis (Acari: Ixodidae) on rodent reservoirs of Borrelia burgdorferi in a residential community of southeastern Connecticut. J. Med. Entomol. 41: 1043–1054. [DOI] [PubMed] [Google Scholar]
  16. Dolan, M. C., Zeidner N. S., Gabitzsch E., Dietrich G., Borchert J. N., Poché R. M., and Piesman J.. . 2008. A doxycycline hyclate rodent bait formulation for prophylaxis and treatment of tick-transmitted Borrelia burgdorferi. Am. J. Trop. Med. Hyg. 78: 803–805. [PubMed] [Google Scholar]
  17. Durden, L. A., and Keirans J. E.. . 1996. Nymphs of the genus Ixodes (Acari: Ixodidae) of the United States: taxonomy, identification key, distribution, hosts, and medical/veterinary importance. Entomological Society of America, Lanham, Md. ©1996. [Google Scholar]
  18. Eisen, R. J., and Eisen L.. . 2018. The blacklegged tick, Ixodes scapularis: an increasing public health concern. Trends Parasitol. 34: 295–309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Eisen, L., and Stafford K. C.. . 2020. Barriers to effective tick management and tick-bite prevention in the United States (Acari: Ixodidae). J. Med. Entomol. 58: 1588–1600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Eisen, R. J., Eisen L., Ogden N. H., and Beard C. B.. . 2016. Linkages of weather and climate with Ixodes scapularis and Ixodes pacificus (Acari: Ixodidae), enzootic transmission of Borrelia burgdorferi, and lyme disease in North America. J. Med. Entomol. 53: 250–261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Elias, S. P., Lubelczyk C. B., Rand P. W., Lacombe E. H., Holman M. S., and R. P.Smith, Jr. 2006. Deer browse resistant exotic-invasive understory: an indicator of elevated human risk of exposure to Ixodes scapularis (Acari: Ixodidae) in southern coastal Maine woodlands. J. Med. Entomol. 43: 1142–1152. [DOI] [PubMed] [Google Scholar]
  22. Gatewood, A. G., Liebman K. A., Vourc’h G., Bunikis J., Hamer S. A., Cortinas R., Melton F., Cislo P., Kitron U., Tsao J., . et al. 2009. Climate and tick seasonality are predictors of Borrelia burgdorferi genotype distribution. Appl. Environ. Microbiol. 75: 2476–2483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ginsberg, H. S., and Stafford K. C. III. 2005. Management of ticks and tick-borne diseases, pp. 65–86. InGoodman J. L., Dennis D. T., and Sonenshine D. E. (eds.), Tick-borne diseases of humans. ASM Press, Washington, DC, USA. [Google Scholar]
  24. Gould, L. H., Nelson R. S., Griffith K. S., Hayes E. B., Piesman J., Mead P. S., and Cartter M. L.. . 2008. Knowledge, attitudes, and behaviors regarding Lyme disease prevention among Connecticut residents, 1999-2004. Vector Borne Zoo. Dis. 8: 769–776. [DOI] [PubMed] [Google Scholar]
  25. Hamer, S. A., Hickling G. J., Sidge J. L., Walker E. D., and Tsao J. I.. . 2012. Synchronous phenology of juvenile Ixodes scapularis, vertebrate host relationships, and associated patterns of Borrelia burgdorferi ribotypes in the midwestern United States. Ticks Tick Borne Dis. 3: 65–74. [DOI] [PubMed] [Google Scholar]
  26. Hinckley, A. F., Meek J. I., Ray J. A., Niesobecki S. A., Connally N. P., Feldman K. A., Jones E. H., Backenson P. B., White J. L., Lukacik G., . et al. 2016. Effectiveness of residential acaricides to prevent lyme and other tick-borne diseases in humans. J. Infect. Dis. 214: 182–188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jones, C. J., and Kitron U. D.. . 2000. Populations of Ixodes scapularis (Acari: Ixodidae) are modulated by drought at a Lyme disease focus in Illinois. J. Med. Entomol. 37: 408–415. [DOI] [PubMed] [Google Scholar]
  28. Jordan, R. A., and Schulze T. L.. . 2019. Ability of two commercially available host-targeted technologies to reduce abundance of Ixodes scapularis (Acari: Ixodidae) in a residential landscape. J. Med. Entomol. 56: 1095–1101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Keirans, J. E., and Litwak T. R.. . 1989. Pictorial key to the adults of hard ticks, family Ixodidae (Ixodida: Ixodoidea), east of the Mississippi River. J. Med. Entomol. 26: 435–448. [DOI] [PubMed] [Google Scholar]
  30. Kilpatrick, H. J., LaBonte A. M., and Stafford K. C.. . 2014. The relationship between deer density, tick abundance, and human cases of Lyme disease in a residential community. J. Med. Entomol. 51: 777–784. [DOI] [PubMed] [Google Scholar]
  31. Kugeler, K. J., Schwartz A. M., Delorey M. J., Mead P. S., and Hinckley A. F.. . 2021. Early release - estimating the frequency of lyme disease diagnoses, United States, 2010–2018. Emerg. Infect. Dis. 27: 616–619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lee, X., Coyle D. R., Johnson D. K., Murphy M. W., McGeehin M. A., Murphy R. J., Raffa K. F., and Paskewitz S. M.. . 2014. Prevalence of Borrelia burgdorferi and Anaplasma phagocytophilum in Ixodes scapularis (Acari: Ixodidae) nymphs collected in managed red pine forests in Wisconsin. J. Med. Entomol. 51: 694–701. [DOI] [PubMed] [Google Scholar]
  33. Levine, J. F., Wilson M. L., and Spielman A.. . 1985. Mice as reservoirs of the Lyme disease spirochete. Am. J. Trop. Med. Hyg. 34: 355–360. [DOI] [PubMed] [Google Scholar]
  34. Lindsay, L. R., Mathison S. W., Barker I. K., McEwen S. A., and Surgeoner G. A.. . 1999. Abundance of Ixodes scapularis (Acari: Ixodidae) larvae and nymphs in relation to host density and habitat on Long Point, Ontario. J. Med. Entomol. 36: 243–254. [DOI] [PubMed] [Google Scholar]
  35. Lubelczyk, C. B., Elias S. P., Rand P. W., Holman M. S., Lacombe E. H., and Smith R. P.. . 2004. Habitat associations of Ixodes scapularis (Acari: Ixodidae) in Maine. Environ. Entomol. 33: 900–906. [Google Scholar]
  36. Mandli, J. T. 2021. New frontiers in integrated tick management: harnessing environmental and molecular technologies to reduce the threat of tick-borne disease. (Publication No. 28315159) [Doctoral dissertation, University of Wisconsin-Madison; ]. ProQuest Dissertations & Thesis Global. [Google Scholar]
  37. Mather, T. N., Ribeiro J. M., and Spielman A.. . 1987. Lyme disease and babesiosis: acaricide focused on potentially infected ticks. Am. J. Trop. Med. Hyg. 36: 609–614. [DOI] [PubMed] [Google Scholar]
  38. Mather, T. N., Ribeiro J. M. C., Moore S. I., and Spielman A.. . 1988. Reducing transmission of Lyme disease spirochetes in a suburban setting. Ann. N. Y. Acad. Sci. 539: 402–403. [Google Scholar]
  39. Nupp, T. E., and Swihart R. K.. . 2011. Effect of forest patch area on population attributes of white-footed mice (Peromyscus leucopus) in fragmented landscapes. Can. J. Zool. 74: 467–472 [Google Scholar]
  40. Ogden, N. H., Pang G., Ginsberg H. S., Hickling G. J., Burke R. L., Beati L., and Tsao J. I.. . 2018. Evidence for geographic variation in life-cycle processes affecting phenology of the lyme disease vector Ixodes scapularis (Acari: Ixodidae) in the United States. J. Med. Entomol. 55: 1386–1401. [DOI] [PubMed] [Google Scholar]
  41. Ostfeld, R. S., Miller M. C., and Hazler K. R.. . 1996. Causes and consequences of tick (Ixodes scapularis) burdens on white-footed mice (Peromyscus leucopus). J. Mammal. 77: 266–273. [Google Scholar]
  42. Pritt, B. S., Mead P. S., Johnson D. K. H., Neitzel D. F., Respicio-Kingry L. B., Davis J. P., Schiffman E., Sloan L. M., Schriefer M. E., Replogle A. J., . et al. 2016. Identification of a novel pathogenic Borrelia species causing Lyme borreliosis with unusually high spirochaetaemia: a descriptive study. Lancet Infect. Dis. 16: 556–564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. R Core Team. 2019. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ [Google Scholar]
  44. Richer, L. M., Brisson D., Melo R., Ostfeld R. S., Zeidner N., and Gomes-Solecki M.. . 2014. Reservoir targeted vaccine against Borrelia burgdorferi: a new strategy to prevent Lyme disease transmission. J. Infect. Dis. 209: 1972–1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Schulze, T. L., McDevitt W. M., Parkin W. E., and Shisler J. K.. . 1987. Effectiveness of two insecticides in controlling Ixodes dammini (Acari: Ixodidae) following an outbreak of Lyme disease in New Jersey. J. Med. Entomol. 24: 420–424. [DOI] [PubMed] [Google Scholar]
  46. Schulze, T. L., Jordan R. A., Schulze C. J., Healy S. P., Jahn M. B., and Piesman J.. . 2007. Integrated use of 4-Poster passive topical treatment devices for deer, targeted acaricide applications, and Maxforce TMS bait boxes to rapidly suppress populations of Ixodes scapularis (Acari: Ixodidae) in a residential landscape. J. Med. Entomol. 44: 830–839. [DOI] [PubMed] [Google Scholar]
  47. Siegel, J. P., Kitron U., and Bouseman J. K.. . 1991. Spatial and temporal distribution of Ixodes dammini (Acari: Ixodidae) in a northwestern Illinois state park. J. Med. Entomol. 28: 101–104. [DOI] [PubMed] [Google Scholar]
  48. Spielman, A. 1988. Prospects for suppressing transmission of Lyme disease. Ann. N. Y. Acad. Sci. 539: 212–220. [DOI] [PubMed] [Google Scholar]
  49. Stafford, K. C., 3rd. 1991. Effectiveness of host-targeted permethrin in the control of Ixodes dammini (Acari: Ixodidae). J. Med. Entomol. 28: 611–617. [DOI] [PubMed] [Google Scholar]
  50. Stafford, K. C., 3rd. 1992. Third-year evaluation of host-targeted permethrin for the control of Ixodes dammini (Acari: Ixodidae) in southeastern Connecticut. J. Med. Entomol. 29: 717–720. [DOI] [PubMed] [Google Scholar]
  51. Stafford, K. C., 3rd. 1994. Survival of immature Ixodes scapularis (Acari: Ixodidae) at different relative humidities. J. Med. Entomol. 31: 310–314. [DOI] [PubMed] [Google Scholar]
  52. Stafford, K. C., 3rd, Ward J. S., and Magnarelli L. A.. . 1998. Impact of controlled burns on the abundance of Ixodes scapularis (Acari: Ixodidae). J. Med. Entomol. 35: 510–513. [DOI] [PubMed] [Google Scholar]
  53. Tilly, K., Rosa P. A., and Stewart P. E.. . 2008. Biology of infection with Borrelia burgdorferi. Infect. Dis. Clin. North Am. 22: 217–2 34, v. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. (U.S. Bureau of Labor Statistics). 2021. Inflation calculator. Available from https://www.bls.gov/data/inflation_calculator.htm
  55. (U.S. Census Bureau). 2017. Characteristics of new housing; Historical data. Available from https://www.census.gov/construction/chars/how_the_data_are_collected/
  56. VanderWeele, T. J., and Knol M. J.. . 2014. A tutorial on interaction. Epidemiol. Methods. 3: 33–72. [Google Scholar]
  57. Williams, S. C., and Ward J. S.. . 2010. Effects of Japanese barberry (Ranunculales: Berberidaceae) removal and resulting microclimatic changes on Ixodes scapularis (Acari: Ixodidae) abundances in Connecticut, USA. Environ. Entomol. 39: 1911–1921. [DOI] [PubMed] [Google Scholar]
  58. Williams, S. C., Ward J. S., Worthley T. E., and K. C.Stafford, 3rd. 2009. Managing Japanese barberry (Ranunculales: Berberidaceae) infestations reduces blacklegged tick (Acari: Ixodidae) abundance and infection prevalence with Borrelia burgdorferi (Spirochaetales: Spirochaetaceae). Environ. Entomol. 38: 977–984. [DOI] [PubMed] [Google Scholar]
  59. Williams, S. C., Linske M. A., and Ward J. S.. . 2017. Long-term effects of Berberis thunbergii (Ranunculales: Berberidaceae) management on Ixodes scapularis (Acari: Ixodidae) abundance and Borrelia burgdorferi (Spirochaetales: Spirochaetaceae) prevalence in connecticut, USA. Environ. Entomol. 46: 1329–1338. [DOI] [PubMed] [Google Scholar]
  60. Williams, S. C., K. C.Stafford, 3rd, Molaei G., and Linske M. A.. . 2018. Integrated control of nymphal Ixodes scapularis: effectiveness of white-tailed deer reduction, the entomopathogenic fungus Metarhizium anisopliae, and fipronil-based rodent bait boxes. Vector Borne Zoo. Dis. 18: 55–64. [DOI] [PubMed] [Google Scholar]
  61. Wilson, M. L. 1986. Reduced abundance of adult Ixodes dammini (Acari: Ixodidae) following destruction of vegetation. J. Econ. Entomol. 79: 693–696. [DOI] [PubMed] [Google Scholar]
  62. Wolff, J. O. 1985. The effects of density, food, and interspecific interference on home range size in Peromyscus leucopus and Peromyscus maniculatus. Can. J. Zool. 63: 2657–2662. [Google Scholar]

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