Integrated Tick Management in Guilford, CT: Fipronil-Based Rodent-Targeted Bait Box Deployment Configuration and Peromyscus leucopus Rodentia: ...
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Journal of Medical Entomology, 59(2), 2022, 591–597 https://doi.org/10.1093/jme/tjab200 Advance Access Publication Date: 15 December 2021 Research Vector Control, Pest Management, Resistance, Repellents Integrated Tick Management in Guilford, CT: Fipronil- Based Rodent-Targeted Bait Box Deployment Configuration and Peromyscus leucopus (Rodentia: Cricetidae) Abundance Drive Reduction in Tick Burdens Downloaded from https://academic.oup.com/jme/article/59/2/591/6462405 by guest on 04 July 2022 Megan A. Linske,1,2,5 Scott C. Williams,1,3, Kirby C. Stafford III,1,2 and Andrew Y. Li4, Center for Vector Biology & Zoonotic Diseases, The Connecticut Agricultural Experiment Station, P.O. Box 1106, 123 Huntington 1 Street, New Haven, CT, 06504,USA, 2Department of Entomology, The Connecticut Agricultural Experiment Station, P.O. Box 1106, 123 Huntington Street, New Haven, CT, 06504, USA, 3Department of Forestry and Horticulture, The Connecticut Agricultural Experiment Station, P.O. Box 1106, 123 Huntington Street, New Haven, CT, 06504, USA, 4United States Department of Agriculture, Agricultural Research Service, Invasive Insect Biocontrol & Behavior Laboratory, BARC-West, Building 007, 10300, Baltimore Avenue, Beltsville, MD, 20705, USA, and 5Corresponding author, e-mail: megan.linske@ct.gov Subject Editor: Howard Ginsberg Received 13 July 2021; Editorial decision 3 November 2021 Abstract Integrated tick management (ITM) is a comprehensive strategy used to reduce presence of ticks and their associated pathogens. Such strategies typically employ a combination of host and non-host targeted treat- ments which often include fipronil-based, rodent-targeted bait boxes. Bait boxes target small-bodied rodents, specifically white-footed mice (Peromyscus leucopus Rafinesque) that not only play a crucial role in the black- legged tick (Ixodes scapularis Say (Ixodida: Ixodidae)) life cycle, but also in the transmission of numerous pathogens, primarily Borrelia burgdorferi Johnson, Schmid, Hyde, Steigerwalt & Brenner (Spirochaetales: Spirochaetaceae), the causal agent of Lyme disease. This study aimed to determine the effect of bait box de- ployment configuration on tick burden reduction while also further exploring bait consumption and P. leucopus abundances as measures of bait box usage and effectiveness. Boxes were deployed on nine properties within each of six neighborhoods (n = 54) in two different configurations: grid and perimeter. Multiple factors were analyzed as potential predictors for reduction in tick burdens using a backward stepwise selection procedure. Results confirmed the perimeter configuration was a more effective deployment strategy. In addition, overall P. leucopus abundance was a significant predictor of tick burden reduction while bait consumption was not. These findings not only further support the recommended perimeter deployment configuration but provide insight into effective utilization in areas of high P. leucopus abundance. The identification of this significant rela- tionship, in addition to configuration, can be utilized by vector control professionals and homeowners to make informed decisions on bait box placement to make sustained impacts on the I. scapularis vector and associated pathogens within an ITM framework. Key words: bait box, blacklegged tick, fipronil, integrated tick management, white-footed mouse More than 17% of all infectious diseases are vector-borne, resulting 300,000 reported cases occurring annually (CDC 2021). While med- in over 700,000 deaths reported annually worldwide (WHO 2021). ical treatments continue to evolve to combat vector-borne diseases In both North America and Europe, 90% of disease-causing patho- once contracted, effective and sustained management of ticks and gens are vectored by ticks (Lindgren et al. 2006, Sykes and Makiello their associated pathogens as a preventative strategy remains chal- 2016, Rosenberg et al. 2018). Lyme disease, while not usually fatal, lenging. The Lyme disease-causing pathogen (Borrelia burgdorferi comprises the vast majority of tick-borne illnesses in the U.S. with over Johnson, Schmid, Hyde, Steigerwalt & Brenner (Spirochaetales: Published by Oxford University Press on behalf of Entomological Society of America 2021. 591 This work is written by (a) US Government employee(s) and is in the public domain in the US.
592 Journal of Medical Entomology, 2022, Vol. 59, No. 2 Spirochaetaceae)) as well as others including, but not limited to, as they enter to consume nontoxic bait within. Bait boxes have those that cause Powassan virus disease, anaplasmosis, and babe- been used in ITM approaches with other host or nonhost targeted siosis are primarily vectored by blacklegged ticks (Ixodes scapularis treatments and have succeeded in reducing, and often sustaining, Say (Ixodida: Ixodidae)) in the upper midwestern, northeastern, and low numbers of ticks within treatment areas (Schulze et al. 2008; mid-Atlantic U.S. The need and demand for effective reduction strat- Williams et al. 2018a, b; Little et al. 2020). Bait box effectiveness is egies have increased as I. scapularis abundances and their associated primarily connected to the fact that rodents are readily available and pathogens too have increased over time. There have been numerous easily accessible on the landscape to be treated. While all rodents in a studies investigating the impact of varied tick management interven- given area have the potential to be treated by bait boxes, P. leucopus tions and combinations thereof. The findings of such studies largely are of primary concern as they are considered the most abundant suggest an integrated approach is the most effective strategy for both vertebrate host for I. scapularis throughout the northeastern United short- and long-term tick reduction (Ghosh et al. 2007, Perez de States (Schmidt et al. 1999, Giardina et al. 2000). While other species León et al. 2014, Stafford et al. 2017, Little et al. 2020). Such an inte- such as eastern chipmunk are also present in residential develop- grated approach is referred to as integrated tick management (ITM). ments and will readily utilize fipronil-based bait boxes, P. leucopus The overarching concept of ITM is that the strategic applica- are habitat generalists and, therefore, are present and abundant in tion of combinations of treatments targeting multiple hosts and tick nearly all habitat types (Hoffmeister 1989, Nupp and Swihart 1996, Downloaded from https://academic.oup.com/jme/article/59/2/591/6462405 by guest on 04 July 2022 life stages is more effective than single treatments alone (Stafford Nupp 1997, Linske et al. 2018). et al. 2017). Previous studies conducted on different tick manage- The application of bait boxes can be used in a variety of habitats ment strategies to be used in an ITM approach have included host- in successful ITM approaches for P. leucopus-targeted tick reduc- and nonhost-targeted applications. Nonhost-targeted treatments tion. Additionally, P. leucopus are a primary host for juvenile stages include habitat modification (Meyer et al. 1982, Stafford et al. 1998, of I. scapularis and are reservoir competent for B. burgdorferi, Williams et al. 2017) and use of less toxic acaricides, repellents, and/ Anaplasma phagocytophilum Dumler, Barbet, Bekker, Dasch, or biopesticides (Stafford and Allan 2010, Flor-Weiller et al. 2011, Palmer, Ray, Rikihisa, Rurangirwa (Rickettsiales: Ehrlichiaceae), Bharadwaj et al. 2015). Less-toxic alternatives are employed largely Babesia microti Franca (Aconoidasida: Piroplasmida), Powassan as a result of public reluctance to synthetic pyrethroids due to poten- virus, among others (Anderson and Magnarelli 1984, Mather et al. tial negative impacts to beneficial insects and perceived/misinformed 1989, Telford and Spielman 1993, Ebel et al. 2000, Levin et al. 2002). negative impacts to pets, family members, or on-site aquifers (Jordan They are responsible for not only further propagating I. scapularis and Schulze 2019a, Eisen and Stafford 2021, Linske and Williams abundances, but also perpetuating and accelerating pathogen trans- unpublished data). Host-targeted methods include, but are not lim- mission cycles. The consistency in the effectiveness of bait boxes as ited to, 4-poster devices (C. R. Daniels, Inc., Ellicott City, MD) to well as the epidemiological importance of P. leucopus makes this target all tick stages on deer (Schulze et al. 2008, Williams et al. treatment particularly relevant within an ITM framework. 2021), deer reduction (Rand et al. 2004, Telford 2017, Williams et al. Quantifying use and effectiveness of bait boxes has been the in- 2018a), perimeter fencing/host exclusion (Stafford 1993, Ginsberg tent of research efforts for some time, most commonly by using para- and Stafford 2005), rodent-targeted vaccines (Gomes-Solecki sitizing tick abundance data and bait consumption from used boxes. 2014, Stafford et al. 2020), Thermacell (Thermacell Repellents, The primary application of bait boxes is in residential areas, specifi- Inc., Bedford, MA) or Damminix (EcoHealth Inc., Brookline, MA) cally backyards and adjacent woodland edges. However, their effec- tick control tubes (Deblinger and Rimmer 1991, Eisen and Dolan tiveness could potentially be increased by manipulating deployment 2016, Jordan and Schulze 2019b, Eisen and Stafford 2021), and configuration for more effective reduction of ticks and their associ- fipronil-based rodent-targeted bait boxes (Select TCS, Connecticut ated pathogens. We deployed bait boxes in two different configur- Tick Control, LLC, Norwalk, CT; Williams et al. 2018b, Jordan ations on 54 residential properties: grid and perimeter. Our main and Schulze 2019a) to target juvenile tick stages on rodents. Four- objective was to compare the success of the two different configur- poster devices use bait to lure deer to self-apply an acaricide to their ations on tick burdens on P. leucopus. We suspected that the grid heads and necks and have had variable success based on arrange- configuration may intercept more P. leucopus (and thus, kill more ment, deployment density, availability of bait, as well as social and parasitizing ticks) using woodland portions of residential properties hierarchical behavior (Rand et al. 2000, Solberg et al. 2003, Pound as it would provide more protection from predators than on the edge et al. 2009, Curtis et al. 2011, Williams et al. 2021). Host reduction, of open lawn area. Secondary objectives included identifying meas- specifically white-tailed deer (Odocoileus virginianus Zimmermann urable parameters that might explain the ability of bait boxes to (Artiodactyla: Cervidae)), has had limited success mostly due to successfully reduce tick burdens on P. leucopus. For the purposes of public concerns and objections, but also due to the intelligence and this study, we were investigating the impact of bait box deployment wariness of deer educated to the lethal threat (Williams et al. 2008, configuration on tick burdens found on the P. leucopus reservoir Kugeler et al. 2016). Rodent use of permethrin-treated material trapped from within said bait box configurations only; the intent of found within Thermacell and/or Damminix tubes is somewhat lim- this work was not to document the areawide control of host-seeking ited by the availability of other natural, preferred bedding mater- I. scapularis using bait boxes alone because of the presence of other ials and may not be used by eastern chipmunks (Tamias striatus L. interventions. (Rodentia: Sciuridae); Jordan and Schulze 2019b). Targeting ticks with topical application of fipronil on the primary reservoir host, the Materials and Methods white-footed mouse (Peromyscus leucopus Rafinesque), is typically met with minimal resistance from the public and this strategy has Study Site and Larger Study Design reduced abundances of both tick and tick-associated pathogens in The study took place throughout Guilford, Connecticut USA numerous studies (Dolan et al. 2004; Schulze et al. 2017; Williams (41.375055, –72.710818) as part of a larger ITM study. Guilford et al. 2018a, b; Little et al. 2020). is a relatively large town (129 km2), with a forested matrix of res- Fipronil-based rodent-targeted bait boxes are equipped with a idential and preserved open space with some agricultural lands to wick saturated with 0.7% fipronil that rodents are forced to contact the north. Lyme disease is endemic in Guilford with a reported 76
Journal of Medical Entomology, 2022, Vol. 59, No. 2 593 cases/100,000 population in 2018 (CTDPH 2021). As a part of the cardboard boxes. Boxes were then placed in a sealed, rodent-free larger study, seven neighborhoods adjacent to preserved open spaces greenhouse to dry for several weeks before their mass was recorded, were identified and residents’ participation solicited. Six of the neigh- after which time, they were disposed of. Care was taken to remove borhoods were randomly designated three treatment combinations, any visible soil or plant material within boxes likely from rodents’ resulting in two replicate neighborhoods/treatment combination and nesting behavior, but it proved difficult to remove in its totality. We one untreated control, which included nine properties/neighborhood determined the mean mass of several clean and empty bait boxes/ (n = 63 properties). The first treatment combination included distri- round and subtracted that mean from the recorded mass of indi- bution of 10 rodent-targeted bait boxes/property and activation of vidual used boxes to establish the mass of bait remaining within. 4-poster devices to treat adult I. scapularis parasitizing white-tailed The difference between an unused box and an empty box was 200 g; deer with permethrin during spring and fall (bait box/4-poster; n = 2 by subtracting the mass of remaining bait from 200, we were able to neighborhoods). The second treatment combination included distri- determine bait consumption/box. There was slight variation in mass bution of 10 rodent-targeted bait boxes/property and early spring (±~5 g) of empty bait boxes both within and between years, and treatment with Metarhizium anisopliae (Metschn.) Sorokin, 1883 some soil and plant material remained inside used boxes, as a result, (Hypocreales: Clavicipitaceae) (Met52 EC, Novozymes Biologicals, this process returned a general (rather than exact) measure of bait Inc., Salem, Virginia, USA; bait box/Met52; n = 2 neighborhoods). consumption but was more than adequate for comparison between Downloaded from https://academic.oup.com/jme/article/59/2/591/6462405 by guest on 04 July 2022 The third treatment combination consisted of all three; rodent- deployment configurations/treatments. targeted bait boxes, 4-poster devices, and Met52 (bait box/4-poster/ Met52; n = 2 neighborhoods). The control neighborhood contained Small Rodent Sampling no bait boxes and was subsequently excluded from this particular Small rodent sampling occurred at all properties. The larger ITM study as the focus was on impacts of bait box configuration rather study protocol dictated that 12 Sherman live traps (LFAHD folding than the larger ITM combination treatments on tick burdens (Table trap, H. B. Sherman Traps, Inc., Tallahassee, FL) containing a small 1). amount of peanut butter be set in a 2 x 6 grid starting at the lawn edge and headed into the wooded portion of the property or adjacent Bait Box Distribution open space. The Sherman trap grid was placed within or adjacent to Within each of the two replicate neighborhoods to receive the bait boxes and spacing varied somewhat based on property configu- same treatment combination, we randomly assigned one to place ration, landscaping, and proximity to neighboring private property, the 10 bait boxes ~ two m into the forest along the lawn periphery but was generally on 10-m spacing. We trapped June–August of all (manufacturer’s recommendation) at 10 m spacing (perimeter). The three years, when overnight low temperatures were warm enough to other replicate neighborhood we placed the 10 boxes in a 2 x 5 avoid stressing captured animals. Traps were placed out in the late grid configuration at 10 m spacing starting just inside the lawn pe- afternoon, left overnight, and retrieved the following morning. Each riphery in the middle of the backyard heading into the wooded por- property was trapped on four occasions in 2018 and 2019 and on tion of the property or adjacent preserved open space (grid). Bait five occasions in 2020. boxes were outfitted with EPA-mandated metal shrouds to prevent For the purposes of this study, captured P. leucopus were trans- species such as eastern gray squirrels (Sciurus carolinensis Gmelin ferred to a plastic bag with a cotton ball containing a small amount (Rodentia: Sciuridae)) from damaging the plastic, exposing the of the inhalant anesthetic isoflurane (Piramal Critical Care, Inc., fipronil wick within (Schulze et al. 2007). Once fitted with metal Bethlehem, PA) for temporary sedation using the open drop method. shrouds, all 540 bait boxes were staked to the ground, and first Once sedated, mice were removed from the bag, the number of para- distributed in early May 2018, 2019, and 2020 ahead of the pre- sitizing ticks on the ears and face was recorded, and unique, metal sumed nymphal I. scapularis activity peak. All 540 bait boxes were ear tag (#1005-1, National Band and Tag Co., Newport, KY) at- removed in mid-July (after ~ nine weeks of deployment) of all three tached. Mice were then returned to Sherman traps until alert and years and replaced with new boxes in preparation for the August then released to the location from which they were originally cap- larval I. scapularis hatch. All bait boxes and metal shrouds were tured. Nontarget trapped species were recorded and immediately re- then removed in late September for the season, after an additional leased without handling. While we realize that 4-posters and Met52 ~nine-week deployment. treatment likely had an impact on overall tick abundances, our study design permitted us to compare differences in parasitizing tick Bait Box Usage burdens between replicates as the result of differences in bait box Used bait boxes were labeled with their assigned property address configuration only. and location within the grid or perimeter array and placed in open Capture and handling protocols were approved by the Wildlife Division of the Connecticut Department of Energy and Environmental Protection (#1320001) and The Connecticut Table 1. Bait box deployment configuration and larger ITM Agricultural Experiment Station’s Institutional Animal Care and treatment assignments based on neighborhood Use Committee (P27-16) in accordance with the American Society Neighborhood 4-poster Bait box Met52 Properties of Mammologist’s guidelines for the use of wild animals in research (Sikes 2016). 1 No Yes (perimeter) Yes 9 2 Yes Yes (perimeter) No 9 3 Yes Yes (grid) Yes 9 Data Analyses 4 Yes Yes (grid) No 9 Standardized Data 5 (control) No No No 9 Bait consumption data were highly variable and needed to be con- 6 Yes Yes (perimeter) Yes 9 solidated for analysis. As a result, we determined a single, mean 7 No Yes (grid) Yes 9 consumption value for all 20 boxes distributed at each property for Total 63 each year (n = 162). However, due to the sale of one property and
594 Journal of Medical Entomology, 2022, Vol. 59, No. 2 the substitution of a previously untreated property midway through the larger ITM study. Of those, I. scapularis larvae (n = 343) and the study, we chose to omit those three values from the analysis. nymphs (n = 15) comprised 86.3% of the subsample. American dog Additionally, we didn’t capture any mice at one property one year, tick (Dermacentor variabilis Say (Ixodida: Ixodidae)) larvae (n = 32) resulting in n = 158 values used in the model. We also determined and nymphs (n = 24), as well as a single lone star tick (Amblyomma the number of total mouse captures (including recaptures), as well americanum L. (Ixodida: Ixodidae)) larva, comprised 13.5% and as the mean number of parasitizing ticks, on all mouse captures for 0.2% of total, respectively. We presumed this distribution, which each property for each year. Because we trapped on 4 occasions in was vast majority I. scapularis, was reflective of unengorged para- 2018 and 2019 and 5 in 2020, we could not directly compare mouse sitizing ticks that were not sampled as well. For the purposes of this capture data. As a result, we standardized data by determining the study, neither species nor stage were of serious significance because number of mouse captures/trap night for each property for each year. all were susceptible to topical fipronil treatment delivery via bait boxes. Mean tick burdens/captured P. leucopus can be found in Regression Analysis Table 3. A backward stepwise regression was conducted using Sigmaplot (Version 14.0, Systat Software, Inc., San Jose, CA) to determine sig- Bait Consumption nificant predictors for the mean number of parasitizing ticks/cap- Both early and later summer bait box deployments were approxi- Downloaded from https://academic.oup.com/jme/article/59/2/591/6462405 by guest on 04 July 2022 tured mouse (dependent variable). The maximum model included mately nine weeks in duration. Additionally, due to highly variable bait box configuration, year, larger ITM treatment combination, differences, we consolidated bait consumption data for all 20 boxes mean bait consumption, and total mouse captures/trap night as in- for each year to a single mean value/property, fully describing the dependent variables. Bait box deployment configuration was listed 18-week deployment window for each year. In 2018, mean bait con- as a nominal variable with 0 for perimeter and 1 for grid. The ITM sumption ranged from 27.4 g to 93.3 g in the grid orientation and treatment combinations were assigned 0 for bait box/4-poster, 1 for 39.0 g to 69.9 g for perimeter. The 2019 mean values ranged from bait box/Met52, and 2 for bait box/4-poster/Met52. The resulting 35.8 g to 94.7 g and from 35.9 g to 106.8 g in grid and perimeter minimum model was used to determine which predictors or com- orientations, respectively. Finally, in 2020, mean bait consumption bination thereof were significantly impacting tick burdens on mice. values ranged from 105.5 g to 130.2 g and 95.6 g to 137.0 g in grid and perimeter orientations, respectively (Table 4). Results Multiple Linear Regression Animal Capture and Tick Sampling The final minimum model was statistically significant (F2, 155 = 6.419; The trapping effort resulted in a total of 8,424 trap nights and P = 0.002). The backward stepwise regression determined that bait 1,454 successful captures, of which 1,190 (81.8% of total) were box deployment configuration (P = 0.017) and total mouse captures/ P. leucopus comprising 840 unique individuals (Table 2). Tamias trap night (P = 0.002) were significant predictors of the number of striatus (n = 224) and northern short-tailed shrew (Blarina juvenile I. scapularis parasitizing P. leucopus while larger ITM treat- brevicauda Say (Eulipotyphla: Soricidae); n = 23) comprised ment assignment, year, and mean bait consumption/property/year 15.4% and 1.6% of total captures, respectively, and likely also were not. The final minimum model produced: included numerous repeat captures. Other nontarget species Ticks/Mouse = 0.640 + (0.428 * Bait Box deployment configura- such as eastern gray squirrel (n = 5), house wren (Troglodytes tion) – (3.123 * Mouse Captures/Trap Night) aedon Vieillot (Passeriformes: Troglodytidae); n = 4), southern Therefore, when bait boxes were oriented in a perimeter config- flying squirrel (Glaucomys volans L. (Rodentia: Sciuridae); n = uration, there was no change in parasitizing tick values, but there 2), ermine (Mustela erminea L. (Carnivora: Mustelidae); n = 2), was a 0.428 unit increase in ticks/mouse when placed in a grid pat- Virginia opossum (Didelphis virginiana Kerr (Didelphimorphia: tern. Additionally, with each unit increase in mouse captures per trap Didelphidae); n = 1), wood frog (Lithobates sylvaticus LeConte night, there was a 3.123 unit decrease in tick burdens parasitizing (Anura: Ranidae); n = 1), eastern cottontail (Sylvilagus floridanus P. leucopus. (Lagomorpha: Leporidae); J. A. Allen; n = 1), and common garter snake (Thamnophis sirtalis L. (Squamata: Colubridae); n = 1) Discussion combined for the remaining 1.2% of captures. Additionally, 310 parasitizing ticks were recorded on captured The findings from this study indicated that two factors primarily P. leucopus resulting in a mean of 0.26 ticks/captured individual influenced the effectiveness of bait box deployment in reducing tick (Table 2). A subsample of engorged ticks, including those from burdens: bait box deployment configuration and total P. leucopus the control/untreated properties (n = 415), was sampled as part of abundance. Given the two different configurations tested, we Table 2. Total number of unique mice, mouse captures (including recaptures), and total number of parasitizing juvenile ticks counted for all three years across sites Year Trap nights Unique mice Total mouse captures Total ticks Ticks/mouse capture 2018 2,592 209 261 132 0.51 2019 2,592 176 258 131 0.51 2020 3,240 455 671 47 0.07 Total 8,424 840 1,190 310 0.26 Also included are total number of parasitizing ticks per captured mouse for each year.
Journal of Medical Entomology, 2022, Vol. 59, No. 2 595 Table 3. Mean tick burdens on each Peromyscus leucopus capture distributed equally across all replicates. The multitude of variables for each bait box deployment configuration by year surrounding bait box deployment in the field make it difficult to as- certain whether it is one individual utilizing bait boxes repeatedly or Year Ticks/P. leucopus (SEM) multiple individuals using them evenly through consumption data Grid Perimeter alone. Anecdotally, we found that if a bait box was placed near a 2018 0.54 (0.15) 0.47 (0.21) burrow or similar den construct, the bait was depleted quickly and 2019 0.80 (0.20) 0.18 (0.10) entirely, most likely due to one or two individuals. In such an in- 2020 0.03 (0.01) 0.13 (0.05) stance, resulting consumption data would be a misrepresentation of Mean 0.30 (0.06) 0.21 (0.06) the overall utilization of bait boxes and presumed distribution of fipronil across the larger population. The minimum model produced with the stepwise selection proce- Table 4. Mean bait consumption for both grid and perimeter dure documented that mean bait consumption was not a significant configuration of bait boxes for all three of the larger ITM predictor of treatment effectiveness on tick burdens. As a result, we treatment types/year suggest that future ITM research efforts using fipronil-based rodent- Year Treatment Mean bait consumption (SEM) targeted bait boxes be wary of reporting consumption results only Downloaded from https://academic.oup.com/jme/article/59/2/591/6462405 by guest on 04 July 2022 as an oversimplified measure of bait box use by the rodent popula- Grid Perimeter tion as a whole. The results from our work show that effectiveness 2018 4Poster&Box 93.3 (12.0) 69.9 (15.5) in reducing tick burdens was dictated by the increased availability Met52&Box 27.4 (8.3) 44.2 (9.5) of hosts to be attracted to bait and treated with fipronil, resulting in Met52,Box,4Poster 72.5 (11.7) 39.0 (13.2) the likely treatment of an increased proportion of the reservoir base 2019 4Poster&Box 61.6 (6.4) 106.8 (14.9) Met52&Box 35.8 (8.0) 35.9 (5.9) instead of repeated treatments of the same individuals. Realizing that Met52,Box,4Poster 94.7 (16.5) 61.1 (11.4) private applicators hired to distribute boxes across private proper- 2020 4Poster&Box 130.2 (8.9) 137.0 (15.3) ties are unlikely to perform rodent population assays, there are de- Met52&Box 105.5 (15.4) 95.9 (15.9) ployment strategies that can be used to increase effectiveness. Met52,Box,4Poster 126.1 (15.7) 95.6 (16.4) Ecotonal zones have already been identified as preferred habitat for P. leucopus, but additional attributes such as structural composi- tion of the understory (Anderson et al. 2003) can also be indicative hypothesized that the grid pattern would intercept more P. leucopus of greater abundances. Dense vegetation like the invasive multiflora due to bait boxes extending deeper into the adjacent woodlands, per- rose (Rosa multiflora Thunb. (Rosales: Rosaceae)) (Drickamer 1970), mitting access to bait boxes and help avoid detection by predators. overall high-density ground cover (M’Closkey and Lajoie 1975), However, the perimeter configuration (and current manufacturer’s oak (Quercus spp.) stands (McShea and Gilles 1992), and structures recommendation) continues to be the most effective for targeting aiding in travel, as well as shelter such as fallen trees (Barnum et al. P. leucopus and thus reducing the number of parasitizing ticks. This 1992) and stone walls (Sinclair et al. 1967, Fergus 2010), are all most likely correlates with the increased usage of ecotonal areas, readily identifiable as preferred mouse habitat. Fragmentation and identifiable edges between major vegetation types (Clements 1905, increased habitat heterogeneity caused by smaller patch sizes charac- Leopold 1933, Odum 1971, Despommier et al. 2006), by P. leucopus teristic of residential properties have been correlated with increased as well as other reservoir species. In this case, the hard edge de- mouse abundance as well (Yahner, 1992, Nupp and Swihart 1996, scribed is the landscaped backyards of residential properties abutting Krohne and Hoch 1999, Mossman and Waser 2001, Anderson et al. woodland habitats. Populations of P. leucopus have been known 2003). The combination of preferable habitat, increased abundance to preferentially inhabit such zones (LoGiudice et al. 2003, of the primary reservoir host, and accessibility make woodland- Despommier et al. 2006) and subsequently, make for an ideal bait adjacent residential areas the ideal location for bait box applications box deployment location. within an ITM framework. Overall P. leucopus abundance was measured in terms of number Bait boxes are commonly used within most ITM strategies for of successful captures/trap night within the vicinity of deployed bait targeting parasitizing ticks (Schulze et al 2008; Williams et al. 2018a, boxes. Peromyscus leucopus are habitat generalists and, therefore, b; Little et al. 2020). Integrated tick management studies continue to are present in most habitat types, including residential developments be conducted to optimize the combination of treatments for reducing (Hoffmeister 1989, Nupp 1997, Linske et al. 2018). However, the ticks and tick-borne pathogens. Therein was the primary objective of mere presence of this reservoir host does not necessarily result in sig- this study: to enhance prior bait box deployment methodology to nificant contact with bait boxes and subsequent reduction in para- increase efficacy in reducing tick burdens on the primary reservoir sitizing ticks. There needs to be a large proportion of the population host, P. leucopus. Successful reduction of ticks parasitizing compe- consistently utilizing bait boxes to cause a substantial, sustained re- tent host species via bait boxes can be achieved and can be improved duction in parasitizing tick abundances. Prior studies used bait con- upon based on the results of this study. Treatment and management sumption as one measure of effectiveness (Dolan et al. 2004, 2011, of ticks, even focusing specifically on parasitizing ticks on mice is 2017; Schulze et al. 2007, 2017), which can be useful, but may not multifaceted. There are many variables, both biotic and abiotic, that necessarily reflect true rodent density, distribution, or bait box usage impact the density of ticks and subsequent tick burdens on mice such by multiple individuals. Once bait boxes are deployed, there are fac- as overwintering success, questing conditions, and both annual and tors that can influence consumption that may not be correlated with seasonal fluctuations in density of both hosts and vectors. What this mouse/rodent abundance, such as the presence of alternative, pre- study provided was an update to treatment applications, such as ferred food sources such as acorns (Dolan et al. 2011). In addition, determining the most effective configuration and placement of bait in the case of this study, the use of boxes and consumption of bait boxes regardless of these conditions. Such updates will only further by T. striatus, which likely had minimal impact on our results as ITM practices and their ability to make direct and sustained impacts they comprised only 15% of captures and their influence was likely on local tick populations. Studies such as these only serve to increase
596 Journal of Medical Entomology, 2022, Vol. 59, No. 2 information available to homeowners, applicators, and other rele- box to control Ixodes scapularis (Acari: Ixodidae) and reduce Borrelia vant stakeholders to amplify ITM efficacy and will only continue to burgdorferi and Anaplasma phagocytophilum infection in small mammal benefit current practices as well as public health. reservoirs and host-seeking ticks. J. Med. Entomol. 54: 403–410. Drickamer, L. C. 1970. Seed preferences in wild caught Peromyscus maniculatus bairdii and Peromyscus leucopus noveboracensis. J. Mammal. 51: 191–194. Acknowledgments Ebel, G. D., E. N. Campbell, H. K. Goethert, A. Spielman, and S. R. Telford, We are grateful to the Town of Guilford’s Health Department for their support 3rd. 2000. Enzootic transmission of deer tick virus in New England and and assistance as well as the collaborating homeowners who allowed us access Wisconsin sites. Am. J. Trop. Med. Hyg. 63: 36–42. to their properties. We would also like to recognize Michael Short, Heidi Stuber, Eisen, L., and M. C. Dolan. 2016. Evidence for personal protective measures and Jamie Cantoni of The Connecticut Agricultural Experiment Station and to reduce human contact with blacklegged ticks and for environmentally seasonal research assistants Sarah Hemstock, Daniel Duque, Hunter Badey, based control methods to suppress host-seeking blacklegged ticks and re- Meagen Denicolo, and Bailey Willett for their technical assistance. This study duce infection with Lyme disease spirochetes in tick vectors and rodent was funded as part of the Areawide Tick Management Project by the United reservoirs. J. Med. Entomol. 53: 1063–1092. States Department of Agriculture through a Non-Assistance Cooperative Eisen, L., and K. C. Stafford. 2021. Barriers to effective tick management Agreement (# 58-8042-6-079) with support from Hatch Act funds. This ar- and tick-bite prevention in the United States (Acari: Ixodidae). J. Med. Entomol. 58: 1588–1600. Downloaded from https://academic.oup.com/jme/article/59/2/591/6462405 by guest on 04 July 2022 ticle reports the results of research only. Mention of a proprietary product does not constitute an endorsement or a recommendation by the Connecticut Fergus, C. 2010. Mice and voles. Wildlife Notes. 41: 1–4. Agricultural Experiment Station (CAES) or the USDA for its use. The CAES Flor-Weiller, L. B., R. W. Behle, and K. C. Stafford III. 2011. Susceptibility and USDA are equal opportunity providers and employers. of four tick species, Amblyomma americanum, Dermacentor variabilis, Ixodes scapularis, and Rhipicephalus sanguineus (Acari: Ixodidae) to nootkatone from essential oil of grapefruit. J. Med. Entomol. 48: 322–326. References Cited Ghosh, S., P. Azhahianambi, and M. P. Yadav. 2007. Upcoming and future Anderson, J. F., and L. A. Magnarelli. 1984. Avian and mammalian hosts strategies of tick control: a review. J. 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