Indirect Effects of Japanese Barberry Infestations on White-Footed Mice Exposure to Borrelia burgdorferi

Indirect Effects of Japanese Barberry Infestations on White-Footed Mice Exposure to Borrelia... Abstract Japanese barberry (Berberis thunbergii de Candolle; Ranunculales: Berberidaceae) is an exotic shrub that has invaded woodland understories in the northeastern United States. It forms dense thickets providing ideal structure and microclimate for questing blacklegged ticks (Ixodes scapularis Say; Acari: Ixodidae). While there have been studies on the favorable habitat barberry provides blacklegged ticks, little has been studied on the relationship between barberry, vectors (ticks), and reservoirs (white-footed mice; Peromyscus leucopus Rafinesque; Rodentia: Cricetidae); specifically, the influence Japanese barberry has on the abundance of blacklegged ticks and Borrelia burgdorferi infection (Johnson, Schmid, Hyde, Steigerwalt, and Brenner; Spirochaetales: Spirochaetaceae) in mice. We studied the impacts of barberry treatment over the course of 6 yr to determine influence on encounter abundance with white-footed mice, encounter abundance with B. burgdorferi-infected mice, and juvenile blacklegged ticks parasitizing mice. Results from our study suggest that while both white-footed mouse and B. burgdorferi-infected mouse encounters remained similar between barberry treatment areas, juvenile tick attachment to mice was significantly greater in intact barberry stands ( X¯ = 4.4 ticks per mouse ± 0.23 SEM) compared with managed ( X¯ = 2.8 ± 0.17; P < 0.001) or absent ( X¯ = 2.2 ± 0.16; P < 0.001) stands. Results of this study indicated that management of barberry stands reduced contact opportunities between blacklegged ticks and white-footed mice. Continued efforts to manage Japanese barberry will not only allow for reestablishment of native plant species, but will also reduce the number of B. burgdorferi-infected blacklegged ticks on the landscape. invasive plant management, serology, primary reservoir host, vector-borne disease Introduction Borrelia burgdorferi (Johnson, Schmid, Hyde, Steigerwalt, and Brenner; Spirochaetales: Spirochaetaceae) is the etiological agent of Lyme disease and has a wide range of hosts that can include various species of birds (Anderson et al. 1986, Townsend et al. 2003), mammals (Anderson and Magnarelli 1984, Donahue et al. 1987), and reptiles (Salkeld and Lane 2010, Swei et al. 2011). In the northeastern United States, its main vector is blacklegged ticks (Ixodes scapularis Say; Ixodida: Ixodidae), which are passive, obligate, ectoparasites that require two to three bloodmeals to successfully complete their life cycle, male and female, respectively. During these feedings, all stages of blacklegged ticks have the potential to ingest various pathogens from reservoir hosts; nymphs and adult females then have the potential to transmit pathogens to uninfected hosts, including humans, during their second, third, or both bloodmeal, respectively (Stafford 2007). However, hosts have varying degrees of reservoir competency, not all hosts are capable of pathogen transmission to ticks (Donahue et al. 1987, Telford et al. 1988, Mather et al. 1989, Hersh et al. 2012). Competent reservoirs are those that cannot only contract pathogens from infected vectors, but can also transfer pathogens to uninfected vectors. Conversely, incompetent reservoir hosts can contract pathogens, but have limited capacity to infect other vectors. White-tailed deer (Odocoileus virginianus Zimmermann; Artiodactyla: Cervidae) are a common example of an incompetent reservoir host (Telford et al. 1988), while white-footed mice (Peromyscus leucopus Rafinesque; Rodentia: Cricetidae) are a highly-competent reservoir host for numerous pathogens, including B. burgdorferi (Donahue et al. 1987, Stafford et al. 1999, Magnarelli et al. 2013, Stafford et al. 2014). White-footed mice are of particular importance in Lyme disease ecology as they are an abundant, small-bodied host for juvenile blacklegged ticks. The potential of white-footed mice to infect a large proportion of localized tick populations exists due to their competency in conjunction with their increased availability. White-footed mice have a proclivity for woodland habitats across their range, which includes Mexico and the contiguous United States east of the Rocky Mountains except for parts of the Southeast (Hoffmeister 1989, Barko et al. 2003). However, previous reports have indicated that Peromyscus exhibit ‘habitat generality’, meaning they can occupy a broad array of habitat types and sizes (Batzli 1977, Adler et al. 1984, Adler and Wilson 1987). Suitable habitat types can range from fragmented tracts in residential areas to larger, undisturbed woodland landscapes. Their ability to colonize and adapt to an array of niches allows this species to occupy mixed habitats and readily establish high population densities when conditions are favorable (MacArthur and Wilson 1967). Additionally, white-footed mice can have high spatial and temporal population size variability indicating that they do not have a demography affixed to particular habitat traits (Adler and Wilson 1987). Previous studies reported that fragmented patches with increased edge habitats, common in urban areas, have the potential for higher population densities (Nupp and Swihart 1996, Wolf and Batzli 2002, Barko et al. 2003). Conversely, larger patches were reported occupied by fewer mice in edges with greater interior densities (Anderson et al. 2003). In addition to patch size, the landscape dynamics involved in generalist species dispersion are often due to the capacity of the species to migrate between those patches in addition to the patch’s vegetation structure and complexity. The diversity of forest stand structure in southern New England forests has declined over the past century, and mature, closed-canopy stands are now predominant (Dickson and McAfee 1988, Butler 2016). The dense shade in these closed-canopy systems precludes development of complex shrub and ground cover communities necessary to support abundant and diverse wildlife species (Sterba 2012, Linske et al. 2018). In addition, the combination of excessive herbivory by overabundant white-tailed deer (Webb et al. 1956, Tierson et al. 1966, McShea et al. 1997, Horsley et al. 2003) and the aggressive growth of exotic invasive plants such as Japanese barberry (Berberis thunbergii de Candolle: Ranunculales: Berberidaceae), multiflora rose (Rosa multiflora Thunberg; Rosales: Rosaceae), and honeysuckle (Lonicera spp.; Dipsacales: Caprifoliaceae) (Cipollini et al. 2009, Eschtruth and Battles 2009, Relva et al. 2010, Duguay and Farfaras 2011, Ward et al. 2017) has further modified the landscape. Japanese barberry is an invasive shrub of particular concern due to its competitive superiority in shaded understories, which significantly inhibits native forest understory development (Ward et al. 2017). Its unique morphology can maintain high densities of ticks infected with pathogens (Williams et al. 2017). Japanese barberry is a highly invasive, nonnative ornamental plant species (Thompson and Robbins 1926, Silander and Klepeis 1999, Weber 2003). Shortly after its introduction to the northeastern United States in the late 1800s, Japanese barberry began to spread across the New England landscape and beyond. It is now documented in 32 states and 5 Canadian provinces (USDA, NRCS 2017). Previous studies determined that management of Japanese barberry was effective for at least 9–10 yr after initial treatment efforts (Williams et al. 2017, Ward et al. 2018). In Japanese barberry management studies, cover was initially reduced to levels comparable to plots where barberry was naturally absent (Williams et al. 2009, Williams and Ward 2010, Williams et al. 2017). Adult blacklegged tick abundances were significantly higher in intact Japanese barberry stands compared with managed stands or where the shrub was absent. While infection prevalence of adult ticks with B. burgdorferi was comparable between treatment types, intact barberry stands had significantly higher abundances of infected ticks (Williams et al. 2017). Japanese barberry’s unique umbrella-shaped morphology in conjunction with its ability to form dense thickets (Kourtev et al. 1998, Ehrenfeld 1999) creates an optimal microclimate for ticks. The growth pattern maintains high humidity levels that permit ticks to quest for hosts for longer durations of the day without having to retreat under the leaf litter to evade desiccation (Williams et al. 2009, Williams and Ward 2010, Williams et al. 2017). Additionally, the dense nature of its growth provides more surface area for questing ticks to attach to passing hosts, such as white-footed mice (Elias et al. 2006, Stafford 2007). While the positive correlation between Japanese barberry and tick abundances is clear, we further investigated the underlying causal mechanism for the increased abundance of B. burgdorferi-infected blacklegged ticks in Japanese barberry infestations. We implemented this study to determine whether there were additional interactions occurring between hosts and vectors within barberry stands, which may have caused increased tick abundances. We identified three objectives to determine the causal mechanism for increased tick densities with comparable B. burgdorferi infection in intact Japanese barberry stands compared to sites that were managed or where it was absent. The first objective was to determine whether there were significant differences in white-footed mouse abundances between treatments. The second was to examine differences in the abundance of feeding juvenile ticks on captured mice between treatments. The final objective was to determine whether B. burgdorferi infection prevalence in white-footed mice differed between treatments. Our overall intent of the study was to determine whether white-footed mice are the causal link between the increased prevalence of both blacklegged ticks and B. burgdorferi-infected blacklegged ticks in Japanese barberry stands and how its management may affect that ecological dynamic. Materials and Methods Study Areas In 2011, six replicate study sites, each subdivided into three treatment types, were established in geographically distinct locations throughout Connecticut. Two were located in south-central Connecticut on South Central Connecticut Regional Water Authority property in North Branford (Tommy Path and Tommy Top) and two were located in western Connecticut on Centennial Watershed State Forest land in Redding (Egypt and Greenbush). The fifth property was located in the northeastern corner of Connecticut at the University of Connecticut in Storrs (Storrs). The final site was in southeastern Connecticut in Lyme (Lord Cove). All study areas were previously agricultural fields or pastures with remnant stone walls. Details on forest stand compositions at the different study areas were reported previously in Williams et al. (2017). Plot Design and Japanese Barberry Control This study was a part of a larger Japanese barberry control project (see Ward et al. 2009) with three treatment plots established at each of the six sites. Plots included an intact barberry stand (full barberry), an area where barberry was managed (controlled barberry), and an area where barberry was absent (no barberry). No barberry plots were located in the immediate vicinity of the other two treatment plots in an area where barberry was naturally minimal or absent. Controlled barberry stands were managed using a combination of treatments in a two-step process. The first step was conducted in late winter to early spring followed by the secondary step in late spring through early summer. The entire treatment process occurred in the first year of site establishment. A hydraulically driven rotary wood shredder (model no. BH74FM, Bull Hog, Fecon Inc., Lebanon, OH) mounted on a compact track loader (model no. Bobcat Co., West Fargo, ND) was used for initial mechanical removal of barberry. Follow-up methods included directed flame with a 100,000 BTU backpack propane torch (model no. BP 223 C Weed Dragon, Flame Engineering, Inc., La Crosse, KS) and foliar application of glyphosate or triclopyr applied directly to new ramets of remaining plants. Combinations of methods were applied separately on subplots within treatment plots, but for the intent of this study, the combinations were considered equivalent among plots and therefore considered a single ‘managed’ plot. For more specific details pertaining to individual subplot treatments, refer to Ward et al. (2009). Japanese barberry management efforts were initiated at Egypt, Tommy Path, and Storrs in 2007; Greenbush and Tommy Top in 2008; and in Lord Cove in 2011. Due to variations in barberry management start times, varying levels of mouse trapping effort, and early substantial trap disturbance events by raccoons (Procyon lotor L.; Carnivora: Procyonidae), data were analyzed for the most recent 6 yr (2011–2016) for all six study sites contemporaneously. Data were analyzed for the impacts of the Japanese barberry treatment on encounter abundance with white-footed mice, the number of feeding juvenile blacklegged ticks per white-footed mouse encounter, and encounter abundance of white-footed mice infected with B. burgdorferi over time and within year. Japanese Barberry Cover Within each plot at each location for each year, Japanese barberry percent cover was estimated at 40 sample points. Percent cover was determined at each point using a 0.25-m2 sampling frame composed of 16 cell grids. Barberry cover was based on the presence or absence of at least one live Japanese barberry stem within each cell. This method, while biased to give a slightly higher estimate than traditional cover estimates, is reproducible and is applicable in both dormant and growing seasons (Ward and Williams 2011). To avoid pseudo-replication, estimated cover for each plot was averaged for all sample points. Resulting percentages were compared for all three treatment types. Small Mammal Trapping Small mammal live trapping was conducted posttreatment. White-footed mice were trapped using Sherman live traps (LFAHD folding trap, H. B. Sherman Traps, Inc., Tallahassee, FL) annually from June to September 2011–2016. Twenty traps were set in permanently marked locations at 15-m spacing in each of the three treatment plots at each study site and baited with peanut butter. Live trapping was used to determine the impact of treatment type on encounter abundance with white-footed mice, the number of feeding juvenile blacklegged ticks per captured white-footed mouse, and to determine the percentage of white-footed mice infected with B. burgdorferi. Encounter abundance was defined as the occasion in which a mouse was collected within one trap night. Attached ticks were identified as blacklegged ticks based on location, season, and morphological characteristics such as dorsal scutum pattern. Captured white-footed mice were temporarily sedated using the inhalant anesthetic isoflurane (Piramal Critical Care, Inc., Bethlehem, PA). White-footed mice were then fitted with a uniquely numbered ear tag (National Band and Tag Co., Newport, KY), blood-sampled, and the number of feeding juvenile blacklegged ticks was recorded. Blood samples were obtained via cardiac puncture using a 1-ml syringe (BD Insulin Syringe, Becton, Dickinson, and Company, Franklin Lakes, NJ) with a 16-mm, 27-gauge needle. A sample of 100–200 µl was taken from each mouse and stored in a 500-µl microcentrifuge tube. Within a few hours of sampling, whole blood samples were transported from the field site to the laboratory with freezer packs in an insulated container and centrifuged to separate serum from whole blood. Both sera and whole blood were individually stored at −80°C for serological analysis. Following recovery from the effects of isoflurane, mice were released where they were originally captured. Capture and handling protocols for the mice were approved by the Wildlife Division of the Connecticut Department of Energy and Environmental Protection (#819005), The Connecticut Agricultural Experiment Station’s Institutional Animal Care and Use Committee (IACUC; P18-13), and a reciprocal agreement with the University of Connecticut’s IACUC (R16-002) in accordance with the American Society of Mammologist’s guidelines for the use of wild animals in research (Sikes and Gannon 2011). Both the number of mouse captures and feeding juvenile blacklegged ticks per mouse were standardized per trap night for each location within each treatment type for each year. White-Footed Mouse Exposure to B. burgdorferi Antibody response to B. burgdorferi in mouse sera was determined using an enzyme-linked immunosorbent assay (ELISA) whose methodology was previously described in Magnarelli et al. (1991, 1997, 2006). Positive cutoff values were derived from the mean plus three standard deviations of net absorbance values of sera from 13 B. burgdorferi-naïve, laboratory-reared white-footed mice. Readings for mouse sera were deemed positive if net optical densities exceeded 0.18, 0.15, and 0.11 for the respective serum dilutions 1:160, 1:320, and ≥1:640. These values were standardized by determining the number of B. burgdorferi-positive, white-footed mice captured per trap night per treatment per location per year. Data Analyses Using a balanced design, analyses were conducted using Sigmaplot statistical software (Sigmaplot 13.0, Systat Software Inc., San Jose, CA). Shapiro–Wilk Normality and Brown–Forsythe Equal Variance tests were conducted on each data set. All variables that were not normally distributed were transformed using a square-root transformation. Transformed barberry cover data were subjected to a two-way (treatment type and year) repeated-measures analysis of variance (ANOVA). Repeated-measures ANOVA was selected to detect overall differences between related means over time after initial treatment. The subject was the study area, with the two factors being year and treatment type. The effect of treatment over time on encounter abundance with white-footed mice, the number of feeding juvenile blacklegged ticks per white-footed mouse encounter, and encounter abundance of unique white-footed mice infected with B. burgdorferi were also analyzed using two-way (treatment type and year) repeated-measures ANOVA. Tukey HSD test was used as a multiple comparison test to determine differences between treatment types and year for each variable. Results Japanese Barberry Cover Barberry percent cover differed among treatment types (F = 94.89; df = 2, 50; P < 0.001). There was also a significant difference in the interaction between treatment type and year (F = 3.16; df = 10, 50; P = 0.003). However, no differences were detected between years (F = 1.59; df = 5, 50; P = 0.20). For all 6 yr, Japanese barberry cover was always highest in full barberry. Cover in no barberry and controlled barberry did not differ from 2011 to 2014, but controlled barberry cover was higher than no barberry areas in both 2015 and 2016 (Fig. 1). Fig. 1. View largeDownload slide Comparison of square root–transformed percent Japanese barberry cover over 6 yr and within year comparisons. Within each year, treatments with the same letter were not significantly different using Tukey HSD multiple comparison with P < 0.05. Treatments include an intact barberry stand (Full Barberry), a stand where barberry was removed (Controlled Barberry), and an area where barberry was naturally absent (No Barberry). Standard error included. Fig. 1. View largeDownload slide Comparison of square root–transformed percent Japanese barberry cover over 6 yr and within year comparisons. Within each year, treatments with the same letter were not significantly different using Tukey HSD multiple comparison with P < 0.05. Treatments include an intact barberry stand (Full Barberry), a stand where barberry was removed (Controlled Barberry), and an area where barberry was naturally absent (No Barberry). Standard error included. Small Mammal Trapping Mouse encounter abundance was not significantly different between treatment types across years (F = 0.264; df = 2, 50; P = 0.773). Within years, 2016 controlled barberry was statistically similar to both full (P = 0.517) and no barberry stands (P = 0.141), whereas full and no barberry were significantly different (P = 0.012). Furthermore, the interaction between year and treatment type was also not significantly different between treatments (F = 2.00; df = 10, 50; P = 0.053). However, there was a significant difference between years (F = 15.04; df = 5, 50; P < 0.001). Mean mouse encounter abundance for 2013 was significantly less than 2011 (P < 0.001), 2012 (P = 0.002), 2014 (P = 0.002), and 2016 (P < 0.001). Mean mouse encounter abundance for 2015 was also significantly less than 2011 (P < 0.001) and 2016 (P = 0.001; Fig. 2). Fig. 2. View largeDownload slide Comparison of square root–transformed mouse encounter abundances per trap night over 6 yr. Years with the same letter were not significantly different using Tukey HSD multiple comparison with P < 0.05. Standard error included. Fig. 2. View largeDownload slide Comparison of square root–transformed mouse encounter abundances per trap night over 6 yr. Years with the same letter were not significantly different using Tukey HSD multiple comparison with P < 0.05. Standard error included. Feeding Juvenile Ticks per Mouse The number of feeding juvenile ticks per mouse differed between treatment types (F = 26.85; df = 2, 50; P < 0.001) and years (F = 4.31; df = 5, 50; P < 0.01; Fig. 3). However, there was no detectable interaction between year and treatment type (F = 1.76; df = 10, 50; P = 0.09). Across all years, mean number of feeding juvenile ticks per mouse was significantly greater in full barberry stands ( X¯ = 4.4 ticks per mouse ± 0.23 SEM) compared with both no barberry ( X¯= 2.2 ± 0.16; P < 0.001) and controlled barberry stands ( X¯= 2.8 ± 0.17; P < 0.001). However, number of feeding ticks per mouse did not differ between no barberry and controlled barberry (P = 0.38). Mean values were greater in 2013 compared with that in 2011 (P < 0.04) and 2016 (P = 0.04). Fig. 3. View largeDownload slide Comparison of square root–transformed feeding juvenile ticks per mouse per trap night over 6 yr with within year comparisons. Within each year, treatments with the same letter were not significantly different using Tukey HSD multiple comparison with p < 0.05. Treatments include an intact barberry stand (Full Barberry), a stand where barberry was removed (Controlled Barberry), and an area where barberry was naturally absent (No Barberry). Standard error included. Fig. 3. View largeDownload slide Comparison of square root–transformed feeding juvenile ticks per mouse per trap night over 6 yr with within year comparisons. Within each year, treatments with the same letter were not significantly different using Tukey HSD multiple comparison with p < 0.05. Treatments include an intact barberry stand (Full Barberry), a stand where barberry was removed (Controlled Barberry), and an area where barberry was naturally absent (No Barberry). Standard error included. B. burgdorferi Exposure in White-Footed Mice We found that B. burgdorferi-infected mouse encounter did not differ between treatment types (F = 0.72; df = 2, 50; P = 0.51) across years. However, 2016 controlled barberry was statistically similar to both full (P = 0.682) and no barberry stands (P = 0.093), whereas full and no barberry were significantly different (P = 0.013). However, there was a significant difference between years (F = 11.77; df = 5, 50; P < 0.001) and interaction between year and treatment type (F = 2.03; df = 10, 50; P = 0.05). The mean infected mouse encounter abundance was less in 2013 compared with that in 2011 (P < 0.001), 2012 (P < 0.03), 2014 (P < 0.01), and 2016 (P < 0.001). Likewise, 2015 values were less than those in 2011 (P < 0.01) and 2016 (P < 0.01). Additionally, 2011 was significantly greater than 2012 (P = 0.04; Fig. 4). Fig. 4. View largeDownload slide Comparison of square root–transformed Borrelia burgdorferi-exposed mouse encounter abundances per trap night over 6 yr. Years with the same letter are not significantly different using Tukey HSD multiple comparison with P < 0.05. Standard error included. Fig. 4. View largeDownload slide Comparison of square root–transformed Borrelia burgdorferi-exposed mouse encounter abundances per trap night over 6 yr. Years with the same letter are not significantly different using Tukey HSD multiple comparison with P < 0.05. Standard error included. The percent encountered mice exposed to B. burgdorferi for each year based on treatment type is summarized in Table 1. Percentage was determined from the number of infected mouse encounters out of total mouse encounter abundance in each treatment type for each year. Table 1. Total Borrelia burgdorferi-exposed white-footed mice encounters and percent-infected mouse encounters by treatment type within each year Year  Treatment type  Positive mouse encounters  Percent positive encounters (%)  2011  CB  158  88  FB  138  81  NB  117  72  2012  CB  71  63  FB  62  67  NB  68  64  2013  CB  27  77  FB  14  74  NB  18  72  2014  CB  59  71  FB  61  72  NB  65  76  2015  CB  34  72  FB  38  83  NB  40  74  2016  CB  102  81  FB  117  77  NB  67  75  Year  Treatment type  Positive mouse encounters  Percent positive encounters (%)  2011  CB  158  88  FB  138  81  NB  117  72  2012  CB  71  63  FB  62  67  NB  68  64  2013  CB  27  77  FB  14  74  NB  18  72  2014  CB  59  71  FB  61  72  NB  65  76  2015  CB  34  72  FB  38  83  NB  40  74  2016  CB  102  81  FB  117  77  NB  67  75  Treatments include an intact barberry stand (FB), a stand where barberry was removed (CB), and where barberry was naturally absent (NB). View Large Table 1. Total Borrelia burgdorferi-exposed white-footed mice encounters and percent-infected mouse encounters by treatment type within each year Year  Treatment type  Positive mouse encounters  Percent positive encounters (%)  2011  CB  158  88  FB  138  81  NB  117  72  2012  CB  71  63  FB  62  67  NB  68  64  2013  CB  27  77  FB  14  74  NB  18  72  2014  CB  59  71  FB  61  72  NB  65  76  2015  CB  34  72  FB  38  83  NB  40  74  2016  CB  102  81  FB  117  77  NB  67  75  Year  Treatment type  Positive mouse encounters  Percent positive encounters (%)  2011  CB  158  88  FB  138  81  NB  117  72  2012  CB  71  63  FB  62  67  NB  68  64  2013  CB  27  77  FB  14  74  NB  18  72  2014  CB  59  71  FB  61  72  NB  65  76  2015  CB  34  72  FB  38  83  NB  40  74  2016  CB  102  81  FB  117  77  NB  67  75  Treatments include an intact barberry stand (FB), a stand where barberry was removed (CB), and where barberry was naturally absent (NB). View Large Discussion Numerous research studies have shown an increased abundance of blacklegged ticks in unhealthy forests infested with invasive plants including Amur honeysuckle (Lonicera maackii (Rupr.) Herder; Allan et al. 2010), multiflora rose (Adalsteinsson et al. 2016, 2018), as well as Japanese barberry (Williams et al. 2009, Williams and Ward 2010, Williams et al. 2017). Our previous work documented a positive correlation between adult blacklegged tick abundances and barberry presence (Williams et al. 2017) with the possible causal mechanism that Japanese barberry stands improved questing habitat. The increased interface between ticks and mice was a function of Japanese barberry’s unique physical structure. This structure maintained an optimal microclimate with increased duration of humidity above critical thresholds, which permitted ticks to quest for longer periods of time, and its dense growth pattern created more surface area for the passive vector to quest for host species (Elias et al. 2006, Williams et al. 2009, Williams et al. 2017). Our initial hypothesis was that increased tick densities were caused by increased white-footed mouse abundances within barberry stands. However, this study found that white-footed mouse encounter abundances did not differ between the three treatment types across all 6 yr. Additionally, we found no difference in the abundance of B. burgdorferi-infected mouse encounters between treatment types across all years. However, number of feeding juvenile blacklegged ticks per captured mouse did differ between treatment types; there was a greater number of juvenile feeding ticks on mice captured in full Japanese barberry stands compared with both controlled sites and those areas where barberry was naturally absent. The increase in juvenile blacklegged tick attachment on mice from intact barberry stands further supports the concept that Japanese barberry increases opportunities for questing ticks to successfully find a host (Williams et al. 2009, Williams and Ward 2010). The morphology of the invasive plant in conjunction with localized host availability provided by a reservoir-competent generalist host (Adler and Wilson 1987) created improved circumstances for blacklegged tick populations to increase in abundance. The decline in juvenile tick attachment success upon removal of barberry suggests that reduction in cover in controlled barberry stands created a more hostile environment resulting in an increase in desiccation-induced mortality of juvenile ticks. After initial barberry management, successful attachment of juvenile ticks in controlled barberry stands declined to that of no barberry stands. The drop in attachment should result in reduced abundances of mature stages of ticks over time (Bertrand and Wilson 1996, Stafford 2007, Williams et al. 2017) in addition to reducing pathogen presence. Juvenile blacklegged tick reliance on white-footed mice for bloodmeals (Stafford et al. 1999, Goodwin et al. 2001) may be the predominant cause for the higher densities of feeding juvenile tick densities in full barberry stands compared with stands where it was controlled or absent. While the presence of this invasive shrub increased the likelihood of questing ticks finding a host (Silander and Klepeis 1999, Lubelczyk et al. 2004, Williams and Ward 2010), barberry itself does not directly increase tick abundances, but functions indirectly by retaining daily relative humidity (Williams and Ward 2010). The presence of host species like white-footed mice is essential for the blacklegged tick and pathogen life cycles. This reservoir species has become the key host in the tick life cycle in woodland habitats because alternative host diversity and abundance have declined in the current mature forests of Connecticut (Butler 2016, Linske et al. 2018). In the absence of other available hosts, ticks obtain bloodmeals on available white-footed mice, thus increasing opportunities for exposure to B. burgdorferi. In Connecticut, there was a greater diversity and abundance of reservoir hosts in residential compared with woodland settings; mean serologically B. burgdorferi-positive white-footed mice in woodland settings was 81% compared with 59% in residential areas (Linske et al. 2018). If our study sites are representative of Connecticut’s woodlands, then increased attachment of early-stage ticks on white-footed mice may result in increased infection due to the absence of other available dilution hosts. Our increased B. burgdorferi-exposed white-footed mouse encounter abundance in sites where Japanese barberry stands were intact may be indicative of this landscape dynamic. A favorable microclimate, a lack of host diversity, and the presence of a reservoir-competent host such as the white-footed mouse that is capable of thriving in various habitat types (Adler et al. 1984, Nupp and Swihart 1996, Anderson et al. 2003) may be the reason why the ticks survive and reach greater densities within Japanese barberry stands (Williams et al. 2009, Williams and Ward 2010, Williams et al. 2017). Due to environmental variables, mouse abundances across all treatment types declined significantly in 2013 (Fig. 2), and consequently juvenile blacklegged tick attachment on mice significantly increased (Fig. 3). Regardless of treatment type and barberry stand composition, this inverse relationship further suggests that juvenile ticks are heavily reliant on white-footed mice for their first, second, or both bloodmeal. While the addition of alternative host species may not have displaced mouse populations, ticks could have parasitized other hosts instead of being concentrated primarily on mice (Linske et al. 2018). If there had been an adequate abundance of alternative hosts, we would assume that the juvenile tick cohort in 2013 would have parasitized them rather than increase their level of attachment on white-footed mice, as speculated in other studies (Ostfeld and Keesing 2000, LoGiudice et al. 2008, Ogden and Tsao 2009). Instead, this inverse relationship was evidence of a lack of host diversity and abundance in Connecticut’s mature forested ecosystems (Butler 2016, Linske et al. 2018), as well as reliance on white-footed mice as the primary reservoir host for juvenile blacklegged ticks. We presumed that mice trapped from full barberry stands with significantly higher abundances of successfully feeding juvenile ticks would have had higher exposure rates to B. burgdorferi, yet infected mouse encounters remained similar between treatments. This would explain why percent infection of adult blacklegged ticks did not differ among treatments as observed in Williams et al. (2017), despite greater adult tick densities in full barberry stands. While overall feeding ticks per mouse densities were greater in intact barberry stands, the chances of ticks successfully feeding on a B. burgdorferi-infected mouse were the same between treatment types. The increased potential for questing ticks to encounter white-footed mice with uniform pathogen transmission capabilities may have caused the number of infected black-legged ticks to be greater overall without a significantly greater infection percentage (Williams et al. 2017). This dynamic between habitat, host, and disease prevalence is an area of increased interest. Comparable instances occur in which vegetation facilitates the opportunity for pathogens and associated diseases to spread. The corn mouse (Calomys musculinus Thomas: Rodentia: Cricetidae), the reservoir for Junín virus, is known as a crop field specialist (de Villafañe et al. 1977) that aids in aerial virus transmission to farmers working in their fields (Carballal et al. 1988). However, studies concluded that the viral interaction between workers and rodent was facilitated by the adjacent, weedy borders that provided ideal reservoir host habitat, not necessarily the crop fields (de Villafañe et al. 1977, Carballal et al. 1988, Mills and Childs 1998). These studies concluded that by removing bordering vegetation, rodents would reduce transmission of the virus to workers. Sudden aspen (Populus tremuloides Michx: Malpighiales: Salicaceae) decline (SAD) elicited a similar response in which vegetation structure altered small mammal density and diversity (Lehmer et al. 2012). In return, the alteration to the host community for Sin Nombre virus (SNV) caused an increase in pathogen presence; areas with high levels of SAD had significantly greater SNV occurrences compared with lower levels. Areas with higher SAD had greater abundance of deer mice (Peromyscus maniculatus Wagner; Rodentia: Cricetidae), the major reservoir host for SNV, thereby enabling the virus to spread (Lehmer et al. 2012). However, these habitat–host relationships primarily relate to inhalant viruses that do not require a vector. The relationship between the host community and vegetation in addition to the presence of the vector, in this case the blacklegged tick, was what made our study both unique and significant. Lowered vegetative diversity in conjunction with invasive plant establishment in northeastern woodlands has had an impact on overall wildlife diversity without displacing white-footed mice. While the elimination of Japanese barberry may reduce tick abundances as well as opportunities for tick attachment, the lack of overall plant diversity in the forest understory has the potential to primarily, and to some extent exclusively, support generalist species such as white-footed mice. This is a public health concern because this species is a highly competent reservoir host, whereas the reestablishment of a greater proportion of incompetent species would help dilute pathogen presence (Linske et al. 2018). Appropriate management strategies for recruiting native shrub stratum in our woodland landscape is becoming increasingly necessary as diversity of both flora and fauna have become reduced over time as forests mature (McKinney 2002, Fahrig 2003, Butler 2016, Linske et al. 2018). Japanese barberry management conducted for this study reduced invasive cover and subsequently reduced juvenile tick attachment to mice. Invasive plant management can also momentarily reduce vegetative competition and in so doing allow native plant species to regenerate (Ward et al. 2013, Ward et al. 2017). Reestablishment of a native understory may aid in restructuring the vertebrate composition of our woodlands by providing habitats capable of supporting and attracting more host diversity. Not only would this aid the health of the forests, but also the increased proportion of incompetent host species would likely dilute the presence of B. burgdorferi. Our study investigated the effects of a single season of treatment on long-term management of an invasive shrub. These treatments not only sustained reduced Japanese barberry cover, but also reduced juvenile tick attachment on white-footed mice comparable to sites where barberry was naturally absent. While mouse populations and percent infection with B. burgdorferi remained the same between treatment types, the reduction in tick attachment and overall population presence supports Japanese barberry control as an effective, long-term management strategy (Williams et al. 2017). However, further research needs to be conducted on reestablishment of woodland diversity to enhance the overall health of forests and people alike. We have shown that management of Japanese barberry is a proven effective strategy in successfully reducing the interface between blacklegged ticks and their primary competent reservoir host. Acknowledgments We would like to thank Aquarion Water Company, Connecticut Chapter—The Nature Conservancy, South Central Connecticut Regional Water Authority, Connecticut Department of Energy and Environmental Protection-Division of Forestry, The University of Connecticut, and Lord Creek Farm for providing study locations. We would also like to thank Weed-It-Now Program—The Nature Conservancy, the Propane Education and Research Council, USDA-National Institute of Food and Agriculture (Hatch), and State of Connecticut general fund for providing valued funding. The late Dr L. A. Magnarelli provided guidance on entomological sampling, terminology, and laboratory techniques. M. R. Short, J. P. Barsky, R. M. Cecarelli, R. J. Hannan, Jr, G. M. Picard, D. V. Tompkins, R. A. Wilcox, E. A. Kiesewetter, T. M. Blevins, H. Stuber, C. Ariori, K. Drennan, and F. Pacyna assisted with plot establishment, treatments, data collection, and mouse blood and tick processing. Monoclonal antibody H5332 was generously provided by Dr Alan Barbour of the Department of Microbiology and Molecular Genetics at the University of California, Irvine’s School of Medicine. References Adalsteinsson, S. A., V. D’Amico, W. G. Shriver, D. Brisson, and J. J. Buler. 2016. 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Indirect Effects of Japanese Barberry Infestations on White-Footed Mice Exposure to Borrelia burgdorferi

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Abstract

Abstract Japanese barberry (Berberis thunbergii de Candolle; Ranunculales: Berberidaceae) is an exotic shrub that has invaded woodland understories in the northeastern United States. It forms dense thickets providing ideal structure and microclimate for questing blacklegged ticks (Ixodes scapularis Say; Acari: Ixodidae). While there have been studies on the favorable habitat barberry provides blacklegged ticks, little has been studied on the relationship between barberry, vectors (ticks), and reservoirs (white-footed mice; Peromyscus leucopus Rafinesque; Rodentia: Cricetidae); specifically, the influence Japanese barberry has on the abundance of blacklegged ticks and Borrelia burgdorferi infection (Johnson, Schmid, Hyde, Steigerwalt, and Brenner; Spirochaetales: Spirochaetaceae) in mice. We studied the impacts of barberry treatment over the course of 6 yr to determine influence on encounter abundance with white-footed mice, encounter abundance with B. burgdorferi-infected mice, and juvenile blacklegged ticks parasitizing mice. Results from our study suggest that while both white-footed mouse and B. burgdorferi-infected mouse encounters remained similar between barberry treatment areas, juvenile tick attachment to mice was significantly greater in intact barberry stands ( X¯ = 4.4 ticks per mouse ± 0.23 SEM) compared with managed ( X¯ = 2.8 ± 0.17; P < 0.001) or absent ( X¯ = 2.2 ± 0.16; P < 0.001) stands. Results of this study indicated that management of barberry stands reduced contact opportunities between blacklegged ticks and white-footed mice. Continued efforts to manage Japanese barberry will not only allow for reestablishment of native plant species, but will also reduce the number of B. burgdorferi-infected blacklegged ticks on the landscape. invasive plant management, serology, primary reservoir host, vector-borne disease Introduction Borrelia burgdorferi (Johnson, Schmid, Hyde, Steigerwalt, and Brenner; Spirochaetales: Spirochaetaceae) is the etiological agent of Lyme disease and has a wide range of hosts that can include various species of birds (Anderson et al. 1986, Townsend et al. 2003), mammals (Anderson and Magnarelli 1984, Donahue et al. 1987), and reptiles (Salkeld and Lane 2010, Swei et al. 2011). In the northeastern United States, its main vector is blacklegged ticks (Ixodes scapularis Say; Ixodida: Ixodidae), which are passive, obligate, ectoparasites that require two to three bloodmeals to successfully complete their life cycle, male and female, respectively. During these feedings, all stages of blacklegged ticks have the potential to ingest various pathogens from reservoir hosts; nymphs and adult females then have the potential to transmit pathogens to uninfected hosts, including humans, during their second, third, or both bloodmeal, respectively (Stafford 2007). However, hosts have varying degrees of reservoir competency, not all hosts are capable of pathogen transmission to ticks (Donahue et al. 1987, Telford et al. 1988, Mather et al. 1989, Hersh et al. 2012). Competent reservoirs are those that cannot only contract pathogens from infected vectors, but can also transfer pathogens to uninfected vectors. Conversely, incompetent reservoir hosts can contract pathogens, but have limited capacity to infect other vectors. White-tailed deer (Odocoileus virginianus Zimmermann; Artiodactyla: Cervidae) are a common example of an incompetent reservoir host (Telford et al. 1988), while white-footed mice (Peromyscus leucopus Rafinesque; Rodentia: Cricetidae) are a highly-competent reservoir host for numerous pathogens, including B. burgdorferi (Donahue et al. 1987, Stafford et al. 1999, Magnarelli et al. 2013, Stafford et al. 2014). White-footed mice are of particular importance in Lyme disease ecology as they are an abundant, small-bodied host for juvenile blacklegged ticks. The potential of white-footed mice to infect a large proportion of localized tick populations exists due to their competency in conjunction with their increased availability. White-footed mice have a proclivity for woodland habitats across their range, which includes Mexico and the contiguous United States east of the Rocky Mountains except for parts of the Southeast (Hoffmeister 1989, Barko et al. 2003). However, previous reports have indicated that Peromyscus exhibit ‘habitat generality’, meaning they can occupy a broad array of habitat types and sizes (Batzli 1977, Adler et al. 1984, Adler and Wilson 1987). Suitable habitat types can range from fragmented tracts in residential areas to larger, undisturbed woodland landscapes. Their ability to colonize and adapt to an array of niches allows this species to occupy mixed habitats and readily establish high population densities when conditions are favorable (MacArthur and Wilson 1967). Additionally, white-footed mice can have high spatial and temporal population size variability indicating that they do not have a demography affixed to particular habitat traits (Adler and Wilson 1987). Previous studies reported that fragmented patches with increased edge habitats, common in urban areas, have the potential for higher population densities (Nupp and Swihart 1996, Wolf and Batzli 2002, Barko et al. 2003). Conversely, larger patches were reported occupied by fewer mice in edges with greater interior densities (Anderson et al. 2003). In addition to patch size, the landscape dynamics involved in generalist species dispersion are often due to the capacity of the species to migrate between those patches in addition to the patch’s vegetation structure and complexity. The diversity of forest stand structure in southern New England forests has declined over the past century, and mature, closed-canopy stands are now predominant (Dickson and McAfee 1988, Butler 2016). The dense shade in these closed-canopy systems precludes development of complex shrub and ground cover communities necessary to support abundant and diverse wildlife species (Sterba 2012, Linske et al. 2018). In addition, the combination of excessive herbivory by overabundant white-tailed deer (Webb et al. 1956, Tierson et al. 1966, McShea et al. 1997, Horsley et al. 2003) and the aggressive growth of exotic invasive plants such as Japanese barberry (Berberis thunbergii de Candolle: Ranunculales: Berberidaceae), multiflora rose (Rosa multiflora Thunberg; Rosales: Rosaceae), and honeysuckle (Lonicera spp.; Dipsacales: Caprifoliaceae) (Cipollini et al. 2009, Eschtruth and Battles 2009, Relva et al. 2010, Duguay and Farfaras 2011, Ward et al. 2017) has further modified the landscape. Japanese barberry is an invasive shrub of particular concern due to its competitive superiority in shaded understories, which significantly inhibits native forest understory development (Ward et al. 2017). Its unique morphology can maintain high densities of ticks infected with pathogens (Williams et al. 2017). Japanese barberry is a highly invasive, nonnative ornamental plant species (Thompson and Robbins 1926, Silander and Klepeis 1999, Weber 2003). Shortly after its introduction to the northeastern United States in the late 1800s, Japanese barberry began to spread across the New England landscape and beyond. It is now documented in 32 states and 5 Canadian provinces (USDA, NRCS 2017). Previous studies determined that management of Japanese barberry was effective for at least 9–10 yr after initial treatment efforts (Williams et al. 2017, Ward et al. 2018). In Japanese barberry management studies, cover was initially reduced to levels comparable to plots where barberry was naturally absent (Williams et al. 2009, Williams and Ward 2010, Williams et al. 2017). Adult blacklegged tick abundances were significantly higher in intact Japanese barberry stands compared with managed stands or where the shrub was absent. While infection prevalence of adult ticks with B. burgdorferi was comparable between treatment types, intact barberry stands had significantly higher abundances of infected ticks (Williams et al. 2017). Japanese barberry’s unique umbrella-shaped morphology in conjunction with its ability to form dense thickets (Kourtev et al. 1998, Ehrenfeld 1999) creates an optimal microclimate for ticks. The growth pattern maintains high humidity levels that permit ticks to quest for hosts for longer durations of the day without having to retreat under the leaf litter to evade desiccation (Williams et al. 2009, Williams and Ward 2010, Williams et al. 2017). Additionally, the dense nature of its growth provides more surface area for questing ticks to attach to passing hosts, such as white-footed mice (Elias et al. 2006, Stafford 2007). While the positive correlation between Japanese barberry and tick abundances is clear, we further investigated the underlying causal mechanism for the increased abundance of B. burgdorferi-infected blacklegged ticks in Japanese barberry infestations. We implemented this study to determine whether there were additional interactions occurring between hosts and vectors within barberry stands, which may have caused increased tick abundances. We identified three objectives to determine the causal mechanism for increased tick densities with comparable B. burgdorferi infection in intact Japanese barberry stands compared to sites that were managed or where it was absent. The first objective was to determine whether there were significant differences in white-footed mouse abundances between treatments. The second was to examine differences in the abundance of feeding juvenile ticks on captured mice between treatments. The final objective was to determine whether B. burgdorferi infection prevalence in white-footed mice differed between treatments. Our overall intent of the study was to determine whether white-footed mice are the causal link between the increased prevalence of both blacklegged ticks and B. burgdorferi-infected blacklegged ticks in Japanese barberry stands and how its management may affect that ecological dynamic. Materials and Methods Study Areas In 2011, six replicate study sites, each subdivided into three treatment types, were established in geographically distinct locations throughout Connecticut. Two were located in south-central Connecticut on South Central Connecticut Regional Water Authority property in North Branford (Tommy Path and Tommy Top) and two were located in western Connecticut on Centennial Watershed State Forest land in Redding (Egypt and Greenbush). The fifth property was located in the northeastern corner of Connecticut at the University of Connecticut in Storrs (Storrs). The final site was in southeastern Connecticut in Lyme (Lord Cove). All study areas were previously agricultural fields or pastures with remnant stone walls. Details on forest stand compositions at the different study areas were reported previously in Williams et al. (2017). Plot Design and Japanese Barberry Control This study was a part of a larger Japanese barberry control project (see Ward et al. 2009) with three treatment plots established at each of the six sites. Plots included an intact barberry stand (full barberry), an area where barberry was managed (controlled barberry), and an area where barberry was absent (no barberry). No barberry plots were located in the immediate vicinity of the other two treatment plots in an area where barberry was naturally minimal or absent. Controlled barberry stands were managed using a combination of treatments in a two-step process. The first step was conducted in late winter to early spring followed by the secondary step in late spring through early summer. The entire treatment process occurred in the first year of site establishment. A hydraulically driven rotary wood shredder (model no. BH74FM, Bull Hog, Fecon Inc., Lebanon, OH) mounted on a compact track loader (model no. Bobcat Co., West Fargo, ND) was used for initial mechanical removal of barberry. Follow-up methods included directed flame with a 100,000 BTU backpack propane torch (model no. BP 223 C Weed Dragon, Flame Engineering, Inc., La Crosse, KS) and foliar application of glyphosate or triclopyr applied directly to new ramets of remaining plants. Combinations of methods were applied separately on subplots within treatment plots, but for the intent of this study, the combinations were considered equivalent among plots and therefore considered a single ‘managed’ plot. For more specific details pertaining to individual subplot treatments, refer to Ward et al. (2009). Japanese barberry management efforts were initiated at Egypt, Tommy Path, and Storrs in 2007; Greenbush and Tommy Top in 2008; and in Lord Cove in 2011. Due to variations in barberry management start times, varying levels of mouse trapping effort, and early substantial trap disturbance events by raccoons (Procyon lotor L.; Carnivora: Procyonidae), data were analyzed for the most recent 6 yr (2011–2016) for all six study sites contemporaneously. Data were analyzed for the impacts of the Japanese barberry treatment on encounter abundance with white-footed mice, the number of feeding juvenile blacklegged ticks per white-footed mouse encounter, and encounter abundance of white-footed mice infected with B. burgdorferi over time and within year. Japanese Barberry Cover Within each plot at each location for each year, Japanese barberry percent cover was estimated at 40 sample points. Percent cover was determined at each point using a 0.25-m2 sampling frame composed of 16 cell grids. Barberry cover was based on the presence or absence of at least one live Japanese barberry stem within each cell. This method, while biased to give a slightly higher estimate than traditional cover estimates, is reproducible and is applicable in both dormant and growing seasons (Ward and Williams 2011). To avoid pseudo-replication, estimated cover for each plot was averaged for all sample points. Resulting percentages were compared for all three treatment types. Small Mammal Trapping Small mammal live trapping was conducted posttreatment. White-footed mice were trapped using Sherman live traps (LFAHD folding trap, H. B. Sherman Traps, Inc., Tallahassee, FL) annually from June to September 2011–2016. Twenty traps were set in permanently marked locations at 15-m spacing in each of the three treatment plots at each study site and baited with peanut butter. Live trapping was used to determine the impact of treatment type on encounter abundance with white-footed mice, the number of feeding juvenile blacklegged ticks per captured white-footed mouse, and to determine the percentage of white-footed mice infected with B. burgdorferi. Encounter abundance was defined as the occasion in which a mouse was collected within one trap night. Attached ticks were identified as blacklegged ticks based on location, season, and morphological characteristics such as dorsal scutum pattern. Captured white-footed mice were temporarily sedated using the inhalant anesthetic isoflurane (Piramal Critical Care, Inc., Bethlehem, PA). White-footed mice were then fitted with a uniquely numbered ear tag (National Band and Tag Co., Newport, KY), blood-sampled, and the number of feeding juvenile blacklegged ticks was recorded. Blood samples were obtained via cardiac puncture using a 1-ml syringe (BD Insulin Syringe, Becton, Dickinson, and Company, Franklin Lakes, NJ) with a 16-mm, 27-gauge needle. A sample of 100–200 µl was taken from each mouse and stored in a 500-µl microcentrifuge tube. Within a few hours of sampling, whole blood samples were transported from the field site to the laboratory with freezer packs in an insulated container and centrifuged to separate serum from whole blood. Both sera and whole blood were individually stored at −80°C for serological analysis. Following recovery from the effects of isoflurane, mice were released where they were originally captured. Capture and handling protocols for the mice were approved by the Wildlife Division of the Connecticut Department of Energy and Environmental Protection (#819005), The Connecticut Agricultural Experiment Station’s Institutional Animal Care and Use Committee (IACUC; P18-13), and a reciprocal agreement with the University of Connecticut’s IACUC (R16-002) in accordance with the American Society of Mammologist’s guidelines for the use of wild animals in research (Sikes and Gannon 2011). Both the number of mouse captures and feeding juvenile blacklegged ticks per mouse were standardized per trap night for each location within each treatment type for each year. White-Footed Mouse Exposure to B. burgdorferi Antibody response to B. burgdorferi in mouse sera was determined using an enzyme-linked immunosorbent assay (ELISA) whose methodology was previously described in Magnarelli et al. (1991, 1997, 2006). Positive cutoff values were derived from the mean plus three standard deviations of net absorbance values of sera from 13 B. burgdorferi-naïve, laboratory-reared white-footed mice. Readings for mouse sera were deemed positive if net optical densities exceeded 0.18, 0.15, and 0.11 for the respective serum dilutions 1:160, 1:320, and ≥1:640. These values were standardized by determining the number of B. burgdorferi-positive, white-footed mice captured per trap night per treatment per location per year. Data Analyses Using a balanced design, analyses were conducted using Sigmaplot statistical software (Sigmaplot 13.0, Systat Software Inc., San Jose, CA). Shapiro–Wilk Normality and Brown–Forsythe Equal Variance tests were conducted on each data set. All variables that were not normally distributed were transformed using a square-root transformation. Transformed barberry cover data were subjected to a two-way (treatment type and year) repeated-measures analysis of variance (ANOVA). Repeated-measures ANOVA was selected to detect overall differences between related means over time after initial treatment. The subject was the study area, with the two factors being year and treatment type. The effect of treatment over time on encounter abundance with white-footed mice, the number of feeding juvenile blacklegged ticks per white-footed mouse encounter, and encounter abundance of unique white-footed mice infected with B. burgdorferi were also analyzed using two-way (treatment type and year) repeated-measures ANOVA. Tukey HSD test was used as a multiple comparison test to determine differences between treatment types and year for each variable. Results Japanese Barberry Cover Barberry percent cover differed among treatment types (F = 94.89; df = 2, 50; P < 0.001). There was also a significant difference in the interaction between treatment type and year (F = 3.16; df = 10, 50; P = 0.003). However, no differences were detected between years (F = 1.59; df = 5, 50; P = 0.20). For all 6 yr, Japanese barberry cover was always highest in full barberry. Cover in no barberry and controlled barberry did not differ from 2011 to 2014, but controlled barberry cover was higher than no barberry areas in both 2015 and 2016 (Fig. 1). Fig. 1. View largeDownload slide Comparison of square root–transformed percent Japanese barberry cover over 6 yr and within year comparisons. Within each year, treatments with the same letter were not significantly different using Tukey HSD multiple comparison with P < 0.05. Treatments include an intact barberry stand (Full Barberry), a stand where barberry was removed (Controlled Barberry), and an area where barberry was naturally absent (No Barberry). Standard error included. Fig. 1. View largeDownload slide Comparison of square root–transformed percent Japanese barberry cover over 6 yr and within year comparisons. Within each year, treatments with the same letter were not significantly different using Tukey HSD multiple comparison with P < 0.05. Treatments include an intact barberry stand (Full Barberry), a stand where barberry was removed (Controlled Barberry), and an area where barberry was naturally absent (No Barberry). Standard error included. Small Mammal Trapping Mouse encounter abundance was not significantly different between treatment types across years (F = 0.264; df = 2, 50; P = 0.773). Within years, 2016 controlled barberry was statistically similar to both full (P = 0.517) and no barberry stands (P = 0.141), whereas full and no barberry were significantly different (P = 0.012). Furthermore, the interaction between year and treatment type was also not significantly different between treatments (F = 2.00; df = 10, 50; P = 0.053). However, there was a significant difference between years (F = 15.04; df = 5, 50; P < 0.001). Mean mouse encounter abundance for 2013 was significantly less than 2011 (P < 0.001), 2012 (P = 0.002), 2014 (P = 0.002), and 2016 (P < 0.001). Mean mouse encounter abundance for 2015 was also significantly less than 2011 (P < 0.001) and 2016 (P = 0.001; Fig. 2). Fig. 2. View largeDownload slide Comparison of square root–transformed mouse encounter abundances per trap night over 6 yr. Years with the same letter were not significantly different using Tukey HSD multiple comparison with P < 0.05. Standard error included. Fig. 2. View largeDownload slide Comparison of square root–transformed mouse encounter abundances per trap night over 6 yr. Years with the same letter were not significantly different using Tukey HSD multiple comparison with P < 0.05. Standard error included. Feeding Juvenile Ticks per Mouse The number of feeding juvenile ticks per mouse differed between treatment types (F = 26.85; df = 2, 50; P < 0.001) and years (F = 4.31; df = 5, 50; P < 0.01; Fig. 3). However, there was no detectable interaction between year and treatment type (F = 1.76; df = 10, 50; P = 0.09). Across all years, mean number of feeding juvenile ticks per mouse was significantly greater in full barberry stands ( X¯ = 4.4 ticks per mouse ± 0.23 SEM) compared with both no barberry ( X¯= 2.2 ± 0.16; P < 0.001) and controlled barberry stands ( X¯= 2.8 ± 0.17; P < 0.001). However, number of feeding ticks per mouse did not differ between no barberry and controlled barberry (P = 0.38). Mean values were greater in 2013 compared with that in 2011 (P < 0.04) and 2016 (P = 0.04). Fig. 3. View largeDownload slide Comparison of square root–transformed feeding juvenile ticks per mouse per trap night over 6 yr with within year comparisons. Within each year, treatments with the same letter were not significantly different using Tukey HSD multiple comparison with p < 0.05. Treatments include an intact barberry stand (Full Barberry), a stand where barberry was removed (Controlled Barberry), and an area where barberry was naturally absent (No Barberry). Standard error included. Fig. 3. View largeDownload slide Comparison of square root–transformed feeding juvenile ticks per mouse per trap night over 6 yr with within year comparisons. Within each year, treatments with the same letter were not significantly different using Tukey HSD multiple comparison with p < 0.05. Treatments include an intact barberry stand (Full Barberry), a stand where barberry was removed (Controlled Barberry), and an area where barberry was naturally absent (No Barberry). Standard error included. B. burgdorferi Exposure in White-Footed Mice We found that B. burgdorferi-infected mouse encounter did not differ between treatment types (F = 0.72; df = 2, 50; P = 0.51) across years. However, 2016 controlled barberry was statistically similar to both full (P = 0.682) and no barberry stands (P = 0.093), whereas full and no barberry were significantly different (P = 0.013). However, there was a significant difference between years (F = 11.77; df = 5, 50; P < 0.001) and interaction between year and treatment type (F = 2.03; df = 10, 50; P = 0.05). The mean infected mouse encounter abundance was less in 2013 compared with that in 2011 (P < 0.001), 2012 (P < 0.03), 2014 (P < 0.01), and 2016 (P < 0.001). Likewise, 2015 values were less than those in 2011 (P < 0.01) and 2016 (P < 0.01). Additionally, 2011 was significantly greater than 2012 (P = 0.04; Fig. 4). Fig. 4. View largeDownload slide Comparison of square root–transformed Borrelia burgdorferi-exposed mouse encounter abundances per trap night over 6 yr. Years with the same letter are not significantly different using Tukey HSD multiple comparison with P < 0.05. Standard error included. Fig. 4. View largeDownload slide Comparison of square root–transformed Borrelia burgdorferi-exposed mouse encounter abundances per trap night over 6 yr. Years with the same letter are not significantly different using Tukey HSD multiple comparison with P < 0.05. Standard error included. The percent encountered mice exposed to B. burgdorferi for each year based on treatment type is summarized in Table 1. Percentage was determined from the number of infected mouse encounters out of total mouse encounter abundance in each treatment type for each year. Table 1. Total Borrelia burgdorferi-exposed white-footed mice encounters and percent-infected mouse encounters by treatment type within each year Year  Treatment type  Positive mouse encounters  Percent positive encounters (%)  2011  CB  158  88  FB  138  81  NB  117  72  2012  CB  71  63  FB  62  67  NB  68  64  2013  CB  27  77  FB  14  74  NB  18  72  2014  CB  59  71  FB  61  72  NB  65  76  2015  CB  34  72  FB  38  83  NB  40  74  2016  CB  102  81  FB  117  77  NB  67  75  Year  Treatment type  Positive mouse encounters  Percent positive encounters (%)  2011  CB  158  88  FB  138  81  NB  117  72  2012  CB  71  63  FB  62  67  NB  68  64  2013  CB  27  77  FB  14  74  NB  18  72  2014  CB  59  71  FB  61  72  NB  65  76  2015  CB  34  72  FB  38  83  NB  40  74  2016  CB  102  81  FB  117  77  NB  67  75  Treatments include an intact barberry stand (FB), a stand where barberry was removed (CB), and where barberry was naturally absent (NB). View Large Table 1. Total Borrelia burgdorferi-exposed white-footed mice encounters and percent-infected mouse encounters by treatment type within each year Year  Treatment type  Positive mouse encounters  Percent positive encounters (%)  2011  CB  158  88  FB  138  81  NB  117  72  2012  CB  71  63  FB  62  67  NB  68  64  2013  CB  27  77  FB  14  74  NB  18  72  2014  CB  59  71  FB  61  72  NB  65  76  2015  CB  34  72  FB  38  83  NB  40  74  2016  CB  102  81  FB  117  77  NB  67  75  Year  Treatment type  Positive mouse encounters  Percent positive encounters (%)  2011  CB  158  88  FB  138  81  NB  117  72  2012  CB  71  63  FB  62  67  NB  68  64  2013  CB  27  77  FB  14  74  NB  18  72  2014  CB  59  71  FB  61  72  NB  65  76  2015  CB  34  72  FB  38  83  NB  40  74  2016  CB  102  81  FB  117  77  NB  67  75  Treatments include an intact barberry stand (FB), a stand where barberry was removed (CB), and where barberry was naturally absent (NB). View Large Discussion Numerous research studies have shown an increased abundance of blacklegged ticks in unhealthy forests infested with invasive plants including Amur honeysuckle (Lonicera maackii (Rupr.) Herder; Allan et al. 2010), multiflora rose (Adalsteinsson et al. 2016, 2018), as well as Japanese barberry (Williams et al. 2009, Williams and Ward 2010, Williams et al. 2017). Our previous work documented a positive correlation between adult blacklegged tick abundances and barberry presence (Williams et al. 2017) with the possible causal mechanism that Japanese barberry stands improved questing habitat. The increased interface between ticks and mice was a function of Japanese barberry’s unique physical structure. This structure maintained an optimal microclimate with increased duration of humidity above critical thresholds, which permitted ticks to quest for longer periods of time, and its dense growth pattern created more surface area for the passive vector to quest for host species (Elias et al. 2006, Williams et al. 2009, Williams et al. 2017). Our initial hypothesis was that increased tick densities were caused by increased white-footed mouse abundances within barberry stands. However, this study found that white-footed mouse encounter abundances did not differ between the three treatment types across all 6 yr. Additionally, we found no difference in the abundance of B. burgdorferi-infected mouse encounters between treatment types across all years. However, number of feeding juvenile blacklegged ticks per captured mouse did differ between treatment types; there was a greater number of juvenile feeding ticks on mice captured in full Japanese barberry stands compared with both controlled sites and those areas where barberry was naturally absent. The increase in juvenile blacklegged tick attachment on mice from intact barberry stands further supports the concept that Japanese barberry increases opportunities for questing ticks to successfully find a host (Williams et al. 2009, Williams and Ward 2010). The morphology of the invasive plant in conjunction with localized host availability provided by a reservoir-competent generalist host (Adler and Wilson 1987) created improved circumstances for blacklegged tick populations to increase in abundance. The decline in juvenile tick attachment success upon removal of barberry suggests that reduction in cover in controlled barberry stands created a more hostile environment resulting in an increase in desiccation-induced mortality of juvenile ticks. After initial barberry management, successful attachment of juvenile ticks in controlled barberry stands declined to that of no barberry stands. The drop in attachment should result in reduced abundances of mature stages of ticks over time (Bertrand and Wilson 1996, Stafford 2007, Williams et al. 2017) in addition to reducing pathogen presence. Juvenile blacklegged tick reliance on white-footed mice for bloodmeals (Stafford et al. 1999, Goodwin et al. 2001) may be the predominant cause for the higher densities of feeding juvenile tick densities in full barberry stands compared with stands where it was controlled or absent. While the presence of this invasive shrub increased the likelihood of questing ticks finding a host (Silander and Klepeis 1999, Lubelczyk et al. 2004, Williams and Ward 2010), barberry itself does not directly increase tick abundances, but functions indirectly by retaining daily relative humidity (Williams and Ward 2010). The presence of host species like white-footed mice is essential for the blacklegged tick and pathogen life cycles. This reservoir species has become the key host in the tick life cycle in woodland habitats because alternative host diversity and abundance have declined in the current mature forests of Connecticut (Butler 2016, Linske et al. 2018). In the absence of other available hosts, ticks obtain bloodmeals on available white-footed mice, thus increasing opportunities for exposure to B. burgdorferi. In Connecticut, there was a greater diversity and abundance of reservoir hosts in residential compared with woodland settings; mean serologically B. burgdorferi-positive white-footed mice in woodland settings was 81% compared with 59% in residential areas (Linske et al. 2018). If our study sites are representative of Connecticut’s woodlands, then increased attachment of early-stage ticks on white-footed mice may result in increased infection due to the absence of other available dilution hosts. Our increased B. burgdorferi-exposed white-footed mouse encounter abundance in sites where Japanese barberry stands were intact may be indicative of this landscape dynamic. A favorable microclimate, a lack of host diversity, and the presence of a reservoir-competent host such as the white-footed mouse that is capable of thriving in various habitat types (Adler et al. 1984, Nupp and Swihart 1996, Anderson et al. 2003) may be the reason why the ticks survive and reach greater densities within Japanese barberry stands (Williams et al. 2009, Williams and Ward 2010, Williams et al. 2017). Due to environmental variables, mouse abundances across all treatment types declined significantly in 2013 (Fig. 2), and consequently juvenile blacklegged tick attachment on mice significantly increased (Fig. 3). Regardless of treatment type and barberry stand composition, this inverse relationship further suggests that juvenile ticks are heavily reliant on white-footed mice for their first, second, or both bloodmeal. While the addition of alternative host species may not have displaced mouse populations, ticks could have parasitized other hosts instead of being concentrated primarily on mice (Linske et al. 2018). If there had been an adequate abundance of alternative hosts, we would assume that the juvenile tick cohort in 2013 would have parasitized them rather than increase their level of attachment on white-footed mice, as speculated in other studies (Ostfeld and Keesing 2000, LoGiudice et al. 2008, Ogden and Tsao 2009). Instead, this inverse relationship was evidence of a lack of host diversity and abundance in Connecticut’s mature forested ecosystems (Butler 2016, Linske et al. 2018), as well as reliance on white-footed mice as the primary reservoir host for juvenile blacklegged ticks. We presumed that mice trapped from full barberry stands with significantly higher abundances of successfully feeding juvenile ticks would have had higher exposure rates to B. burgdorferi, yet infected mouse encounters remained similar between treatments. This would explain why percent infection of adult blacklegged ticks did not differ among treatments as observed in Williams et al. (2017), despite greater adult tick densities in full barberry stands. While overall feeding ticks per mouse densities were greater in intact barberry stands, the chances of ticks successfully feeding on a B. burgdorferi-infected mouse were the same between treatment types. The increased potential for questing ticks to encounter white-footed mice with uniform pathogen transmission capabilities may have caused the number of infected black-legged ticks to be greater overall without a significantly greater infection percentage (Williams et al. 2017). This dynamic between habitat, host, and disease prevalence is an area of increased interest. Comparable instances occur in which vegetation facilitates the opportunity for pathogens and associated diseases to spread. The corn mouse (Calomys musculinus Thomas: Rodentia: Cricetidae), the reservoir for Junín virus, is known as a crop field specialist (de Villafañe et al. 1977) that aids in aerial virus transmission to farmers working in their fields (Carballal et al. 1988). However, studies concluded that the viral interaction between workers and rodent was facilitated by the adjacent, weedy borders that provided ideal reservoir host habitat, not necessarily the crop fields (de Villafañe et al. 1977, Carballal et al. 1988, Mills and Childs 1998). These studies concluded that by removing bordering vegetation, rodents would reduce transmission of the virus to workers. Sudden aspen (Populus tremuloides Michx: Malpighiales: Salicaceae) decline (SAD) elicited a similar response in which vegetation structure altered small mammal density and diversity (Lehmer et al. 2012). In return, the alteration to the host community for Sin Nombre virus (SNV) caused an increase in pathogen presence; areas with high levels of SAD had significantly greater SNV occurrences compared with lower levels. Areas with higher SAD had greater abundance of deer mice (Peromyscus maniculatus Wagner; Rodentia: Cricetidae), the major reservoir host for SNV, thereby enabling the virus to spread (Lehmer et al. 2012). However, these habitat–host relationships primarily relate to inhalant viruses that do not require a vector. The relationship between the host community and vegetation in addition to the presence of the vector, in this case the blacklegged tick, was what made our study both unique and significant. Lowered vegetative diversity in conjunction with invasive plant establishment in northeastern woodlands has had an impact on overall wildlife diversity without displacing white-footed mice. While the elimination of Japanese barberry may reduce tick abundances as well as opportunities for tick attachment, the lack of overall plant diversity in the forest understory has the potential to primarily, and to some extent exclusively, support generalist species such as white-footed mice. This is a public health concern because this species is a highly competent reservoir host, whereas the reestablishment of a greater proportion of incompetent species would help dilute pathogen presence (Linske et al. 2018). Appropriate management strategies for recruiting native shrub stratum in our woodland landscape is becoming increasingly necessary as diversity of both flora and fauna have become reduced over time as forests mature (McKinney 2002, Fahrig 2003, Butler 2016, Linske et al. 2018). Japanese barberry management conducted for this study reduced invasive cover and subsequently reduced juvenile tick attachment to mice. Invasive plant management can also momentarily reduce vegetative competition and in so doing allow native plant species to regenerate (Ward et al. 2013, Ward et al. 2017). Reestablishment of a native understory may aid in restructuring the vertebrate composition of our woodlands by providing habitats capable of supporting and attracting more host diversity. Not only would this aid the health of the forests, but also the increased proportion of incompetent host species would likely dilute the presence of B. burgdorferi. Our study investigated the effects of a single season of treatment on long-term management of an invasive shrub. These treatments not only sustained reduced Japanese barberry cover, but also reduced juvenile tick attachment on white-footed mice comparable to sites where barberry was naturally absent. While mouse populations and percent infection with B. burgdorferi remained the same between treatment types, the reduction in tick attachment and overall population presence supports Japanese barberry control as an effective, long-term management strategy (Williams et al. 2017). However, further research needs to be conducted on reestablishment of woodland diversity to enhance the overall health of forests and people alike. We have shown that management of Japanese barberry is a proven effective strategy in successfully reducing the interface between blacklegged ticks and their primary competent reservoir host. Acknowledgments We would like to thank Aquarion Water Company, Connecticut Chapter—The Nature Conservancy, South Central Connecticut Regional Water Authority, Connecticut Department of Energy and Environmental Protection-Division of Forestry, The University of Connecticut, and Lord Creek Farm for providing study locations. We would also like to thank Weed-It-Now Program—The Nature Conservancy, the Propane Education and Research Council, USDA-National Institute of Food and Agriculture (Hatch), and State of Connecticut general fund for providing valued funding. The late Dr L. A. Magnarelli provided guidance on entomological sampling, terminology, and laboratory techniques. M. R. Short, J. P. Barsky, R. M. Cecarelli, R. J. Hannan, Jr, G. M. Picard, D. V. Tompkins, R. A. Wilcox, E. A. Kiesewetter, T. M. Blevins, H. Stuber, C. Ariori, K. Drennan, and F. Pacyna assisted with plot establishment, treatments, data collection, and mouse blood and tick processing. Monoclonal antibody H5332 was generously provided by Dr Alan Barbour of the Department of Microbiology and Molecular Genetics at the University of California, Irvine’s School of Medicine. References Adalsteinsson, S. A., V. D’Amico, W. G. Shriver, D. Brisson, and J. J. Buler. 2016. 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Environmental EntomologyOxford University Press

Published: May 30, 2018

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