TY - JOUR
AU - Duchamp, Joseph E
AB - Abstract The blacklegged tick (Ixodes scapularis Say) vectors several bacterial, protozoan, and viral human pathogens. The known distribution, abundance, and phenology of I. scapularis within its estimated range are incomplete. This gap in knowledge is problematic because these factors are important for determining acarological risk of exposure to infected ticks. Consequently, enhanced surveillance of I. scapularis is being promoted and supported in the United States. Although the most common method for collecting I. scapularis is by dragging a sturdy cloth along the ground, there are no published empirical data showing which drag fabric is most effective. We used a randomized block design to directly compare the relative efficiencies of canvas, corduroy, and flannel drags for the collection of larval, nymphal, and adult I. scapularis. Overall, flannel was the most effective fabric and canvas was the least effective. Significantly more adults were collected on flannel than on canvas or corduroy, and the same number of nymphs was collected on flannel and corduroy. Significantly more larvae were collected on flannel than on canvas, but one-third of larvae could not be removed from the former fabric by lint-rolling, and handpicking was difficult. Our findings support the use of flannel drags to maximize sampling effort for collection of I. scapularis, especially adults to determine the presence of ticks and tick-borne pathogens when density and infection prevalence are low, with the caveat that detection and removal of larvae are time-consuming. Ixodes scapularis, blacklegged tick, collection, drag, efficiency The blacklegged tick (Ixodes scapularis Say) is a vector of seven bacterial, protozoan, and viral human pathogens causing anaplasmosis, babesiosis, Borrelia miyamotoi disease, ehrlichiosis, Lyme disease, and Powassan virus disease (Nelder et al. 2016, Eisen and Eisen 2018). Over the last two decades, the geographic range of I. scapularis and number of associated disease cases reported to the National Notifiable Diseases Surveillance System have markedly increased in the United States (Kugeler et al. 2015; Eisen et al. 2016, 2017; Rosenberg et al. 2018). Mathematical modeling based on suitability of habitat and environmental conditions predicts the range of I. scapularis will continue to expand (Hahn et al. 2016). Across the estimated range of I. scapularis, data on the distribution of reported or established populations at the county level are incomplete (Eisen et al. 2016, Centers for Disease Control and Prevention [CDC] 2020a), and comparable data on the density of ticks and infection prevalence of pathogens in these populations are limited (Eisen and Paddock 2020). Because the occurrence and abundance of pathogen-infected host-seeking ticks are important determinants of disease risk (Eisen and Eisen 2016), the CDC responded to this deficiency of data by establishing a national tick and tick-borne pathogen surveillance and reporting program (Eisen and Paddock 2020). The objectives of the program are to identify counties with reported or established tick populations, characterize phenology, quantify density, determine the presence or prevalence of pathogens, and estimate density of infected ticks. In support of this program, the CDC (2018) developed standard guidelines for the collection of I. scapularis and testing for pathogens. Although there are a variety of methods to collect ticks that include dragging, flagging, walking, CO2 trapping, and removing ticks from wild animals, pets, and people, dragging or flagging are the only methods generally acceptable for all the objectives and specifically for quantification of tick density (CDC 2018, Eisen and Paddock 2020). Dragging or flagging involves pulling or sweeping a sturdy piece of light-colored cloth along the ground through and over vegetation and periodically checking for ticks. For both methods, the cloth is attached on its leading edge to a dowel, but drags are pulled using a cord and flags are swept using a handle. Beyond these generalities, drag materials and dragging techniques vary considerably due to a lack of widely accepted standard methods (Eisen and Paddock 2020). For its blanket-style drag, the CDC (2018) standard guidelines specify a 45 in wide and 1-1/2 yd long (1.1 × 1.4 m) piece of rubberized cotton flannel weighted on the back end with lead sinkers and recommends checking the cloth every 10–20 m for adults and 10–15 m for nymphs. Building on the CDC (2018) guidelines, Salomon et al. (2020) described a standard tick dragging protocol including construction of drags using heavy cotton flannel fabric. They also considered corduroy but felt that the wales increased the actual surface area of the cloth, which would be problematic for density estimates and also provided crevices in which larvae could hide and be overlooked. The National Ecological Observatory Network (NEON) also developed standard guidelines for the collection of ixodid hard ticks, including I. scapularis, for regional monitoring of tick-borne pathogen risk across the United States (Springer et al. 2016). The NEON specifies a 1 × 1 m piece of white cotton flannel and recommends checking the cloth every 5–10 m. The distance intervals ranging from 5 to 20 m as recommended by Springer et al. (2016) and CDC (2018) are supported by drop-off studies that measured the rate of detachment by Schulze and Jordan (2001) for adult I. scapularis and Borgmann-Winter and Allen (2020) for adult and nymphal I. scapularis. In contrast to these optimal distance intervals, the choice of ~1 m2 cotton flannel appears to be based on experience or convention, and not empirical data. However, there are well-established tick research laboratories (e.g., Carey Institute of Ecosystem Studies and The Louis Calder Center in New York State) that have used and continue to use corduroy (Fischhoff et al. 2019, Piedmonte et al. 2020). We searched the literature and only found two studies calculating absolute collection efficiency (i.e., percent of actual population collected on a drag after one pass) of drags for I. scapularis (Daniels et al. 2000, Simmons et al. 2015) and one study comparing relative collection efficiency of two drag fabrics for ticks including I. scapularis (Newman et al. 2019). Daniels et al. (2000) conducted removal and mark–recapture experiments and calculated collection efficiencies of 8.6% for larvae, 6.7% for nymphs, and 3.6% for adults using 1 × 1 m corduroy drags in a mixed deciduous hardwood forest in southeastern New York. Simmons et al. (2015) conducted similar experiments and calculated collection efficiencies of 24.5% for larvae, 9.9% for nymphs, and 4.5% for adults using 1 × 1 m cotton sailcloth canvas drags in a mixed hardwood forest in midwestern Pennsylvania. The results of these two studies suggest that corduroy and canvas drags are comparable for collecting nymphs and adults, while canvas is more effective for collecting larvae. However, even though Simmons et al. (2015) replicated the study design of Daniels et al. (2000) as closely as possible, these fabrics were not directly compared with one another at the same place or time, so geography, habitat, and environmental conditions differed and are confounding factors. Newman et al. (2019) proposed a standard method for constructing 1 × 1 m drags and compared the relative effectiveness of collecting ticks using cotton muslin or cotton flannel fabric in a mixed pine hardwood forest in northwestern Alabama. Unfortunately, only 1.1% of the ticks collected were I. scapularis, so their numbers could not be analyzed separately from other species. Given the low collection efficiency of dragging for I. scapularis, possible differences in collection efficiency of drag fabrics should be considered to maximize surveillance efforts and to compare research studies and surveillance activities that used or are using different drag fabrics. The goal of our study was to directly compare the relative collection efficiency of canvas, corduroy, and flannel made from cotton of similar weight and color following standard dragging techniques. These are commonly used fabrics representing a wide range of textures (Newman et al. 2019). Materials and Methods Study Site Our study was conducted in Blue Spruce County Park in Indiana, PA, the site of a previous study where phenology and density of I. scapularis were characterized (Simmons et al. 2015). The terrain and composition of trees in the park were described by Simmons et al. (2015). Briefly, the closed canopy overstory is dominated by deciduous hardwood trees, and the understory is sparse due to heavy browsing by deer. For each life stage (i.e., larva, nymph, or adult), we selected a forested plot in the same location where Simmons et al. (2015) previously observed the highest density for that specific stage. The plots were large enough to accommodate a statistically adequate number of 100-m transects based on power analyses and were draggable throughout with no steep embankments, dense understory, or surface water. Drag Construction All drags were constructed by BioQuip Products, Inc. (Rancho Dominguez, CA). Their standard drag is a 0.6 × 1.1 m light tan-colored 100% cotton sailcloth canvas with a weight of 271 g/m2. The leading edge of the canvas is sewn into a Dacron sail hem, which is wrapped around and secured to a 2.5-cm dowel. A polypropylene cord for pulling the drag is attached to the ends of the dowel. Simmons et al. (2015, 2020) used a 1 × 1 m version of this drag, which was also employed in the present study (Fig. 1). In addition, we supplied BioQuip with corduroy and flannel fabrics of similar color and weight to make matching 1 × 1 m drags (Fig. 2). Kaufman off-white-colored 100% cotton 14-wale (14 cords per 2.54 cm) corduroy with a weight of 275 g/m2 was purchased from fabric.com (https://www.fabric.com/), and light tan-colored 100% cotton flannel with a weight of 271 g/m2 from Organic Cotton Plus (https://organiccottonplus.com/). The corduroy was mounted with wales running parallel to the dowel. Fig. 1. Open in new tabDownload slide Flannel (closest), canvas (middle), and corduroy (furthest) 1 × 1 m drags being pulled side-by-side in unison along forest floor in adult Ixodes scapularis plot. Fig. 1. Open in new tabDownload slide Flannel (closest), canvas (middle), and corduroy (furthest) 1 × 1 m drags being pulled side-by-side in unison along forest floor in adult Ixodes scapularis plot. Fig. 2. Open in new tabDownload slide Canvas (upper), corduroy (middle), and flannel (lower) drag fabrics with Ixodes scapularis adult females, males, nymphs, and larvae (from left to right). Fig. 2. Open in new tabDownload slide Canvas (upper), corduroy (middle), and flannel (lower) drag fabrics with Ixodes scapularis adult females, males, nymphs, and larvae (from left to right). Tick Sampling Each tick stage was sampled on multiple days, partly based on number of transects prescribed by power analysis, during its expected peak of seasonal activity as determined by Simmons et al. (2015). Adults were sampled from late March to mid-April, nymphs in mid-July, and larvae in early August of 2018. To account for possible changes in tick activity due to air temperature and humidity (Vail and Smith 1998, Schulze et al. 2001, Berger et al. 2014, Burtis et al. 2016), we monitored ground temperature and relative humidity at the beginning and end of each sampling day using a Testo 605 H-1 Hygrometer Humidity stick (Testo North America, West Chester, PA). Ticks were only sampled when temperatures were above 10.0°C, which is just above the uncoordinated activity threshold temperature of 9.2°C for female I. scapularis determined by Clark (1995), and not during wet conditions due to rain that would have moistened the drag cloths or windy conditions that would have lifted or flapped the cloths. We divided plots into adjacent 100 × 5 m transects using pin flags spaced 10 m apart to delineate edges between them. Each transect was visually (i.e., no pin flags) divided into three lanes, one for each drag fabric, allowing 0.5 m of buffer space between lanes and between lanes and transect edges. We used a randomized block design to minimize temporal, spatial, and person effects between drag fabrics. At the start of each sampling day, persons and drag fabrics were randomly assigned independent of one another to lanes within a previously unsampled transect. At the beginning of each subsequent transect, drag fabrics were systematically rotated from lane to lane while persons remained in the same lane, they were assigned at the start of the sampling day. For each transect, new drags were used. The drags were pulled side-by-side in unison at a pace between 0.13 and 0.22 m/s (approximately 1 min/10 m; Fig. 1) and no faster than 0.3 m/s as specified by Springer et al. (2016) to allow adequate contact time for ticks to attach. The drags were checked every 10 m for ticks as recommended by Schulze and Jordan (2001), Estrada-Peña et al. (2013), and Springer et al. (2016) to minimize dislodgement of ticks after they attach. For adults and nymphs, each drag fabric was examined by each person for a total of three times to ensure that all ticks were counted and removed by-hand with entomological forceps (BioQuip Products, Rancho Dominguez, CA). Only ticks on the underside of drags were considered attached to exclude from analyses those that fell onto the top of drags from disturbed vegetation or coarse woody debris. For larvae, which are too small and numerous to handpick in the field, drag fabrics were draped over 1.2 × 1.2 m sheets of 2.5-cm polystyrene insulation board (Kingspan, Atlanta, GA) for backing and support, and larvae were removed by lint-rolling three times using new sheets for each roll (Scotch-Brite, 3M, St. Paul, MN). The first lint-roll removed larvae from the leading Dacron sail hem edge, and these larvae were excluded from analyses because the hem was identical on all drags. The second and third lint-rolls removed larvae from the underside of drag fabrics by first rolling horizontally and then vertically, respectively. After each rolling direction, sheets were placed in plastic slider zipper quart storage bags (Great Value, WalMart, Bentonville, AR), and after each transect, drags were placed into 2 mil industrial poly bag poster sleeves (Uline, Pleasant Prairie, WI) and stored at 1.6°C until examination in the laboratory. Laboratory Analysis Larvae on lint roller sheets were enumerated in the laboratory by placing transparent acetate counting grids with 1 × 1 cm cells on the sheets and examining under a stereomicroscope. Larvae on tick drags were enumerated by placing transparent Lexan counting grids with 10 × 10 cm cells on the drags and examining with the aid of a flashlight and magnifying glass. Habitat Analysis Because habitat structure can affect retention of I. scapularis adults on drags (Schulze and Jordan 2001), we characterized groundcover vegetation and soil surface substrate composition for each plot by adapting standard protocols developed and refined by the Virginia Department of Conservation and Recreation Natural Heritage Program (DCR-DNH) over the last 25 yr. (Fleming et al. 2006). For each 10-m length of transect, a 1 m2 sampling square, constructed of PVC pipes on the edges and elbow fittings at the corners, was placed on the ground in the middle lane at a randomly determined distance. The PVC pipes were marked at 0.25 m (i.e., 1/4) intervals to visually subdivide the sampling square into 16 subsquares. Percent groundcover vegetation and soil surface substrate types were visually estimated within each square with the aid of the subsquares to focus the estimation on smaller more manageable areas (Table 1). Soil surface substrates consisting of abiotic components, leaf litter, and coarse woody debris summed to 100%. The percent cover of nonvascular plants and herbaceous and woody plants of <0.5 m tall was in addition to the 100% cover by soil surface substrates. Table 1. Groundcover vegetation and surface cover composition of plots used for sampling different blacklegged tick life stages . Percent composition . . Adult plot (n = 200) . Nymphal plot (n = 130) . Larval plot (n = 120) . Surface substrate  Boulder/stone 32.0 ± 2.1 (0–98) 0.06 ± 0.05 (0–6) 0.28 ± 0.19 (0–20)  Gravel/cobble 0 0 0  Mineral soil/sand 0.53 ± 0.14 (0–15) 2.94 ± 0.40 (0–20) 3.93 ± 0.76 (0–70)  Leaf litter/organic matter 55.7 ± 2.0 (0–97) 85.0 ± 1.1 (15–100) 85.4 ± 1.3 (20–98)  Coarse woody debris 11.8 ± 1.1 (0–95) 12.0 ± 1.1 (0–80) 11.5 ± 1.6 (0–80)  Total 100 100 100 Groundcover vegetation  Woody plants 1.55 ± 0.30 (0–30) 9.61 ± 0.93 (0–70) 5.28 ± 0.89 (0–80)  Herbaceous plants 1.24 ± 0.23 (0–25) 9.02 ± 0.80 (0–50) 6.90 ± 0.90 (0–65)  Ferns 4.36 ± 0.42 (0–50) 2.19 ± 0.97 (0–80) 5.67 ± 1.33 (0–90)  Club mosses 0 17.5 ± 1.8 (0–90) 0  Mosses 21.5 ± 1.4 (0–90) 0.28 ± 0.08 (0–5) 0.36 ± 0.16 (0–15)  Total 28.6 ± 1.5 (0–95) 38.6 ± 2.1 (3–100) 18.2 ± 1.8 (0–100) . Percent composition . . Adult plot (n = 200) . Nymphal plot (n = 130) . Larval plot (n = 120) . Surface substrate  Boulder/stone 32.0 ± 2.1 (0–98) 0.06 ± 0.05 (0–6) 0.28 ± 0.19 (0–20)  Gravel/cobble 0 0 0  Mineral soil/sand 0.53 ± 0.14 (0–15) 2.94 ± 0.40 (0–20) 3.93 ± 0.76 (0–70)  Leaf litter/organic matter 55.7 ± 2.0 (0–97) 85.0 ± 1.1 (15–100) 85.4 ± 1.3 (20–98)  Coarse woody debris 11.8 ± 1.1 (0–95) 12.0 ± 1.1 (0–80) 11.5 ± 1.6 (0–80)  Total 100 100 100 Groundcover vegetation  Woody plants 1.55 ± 0.30 (0–30) 9.61 ± 0.93 (0–70) 5.28 ± 0.89 (0–80)  Herbaceous plants 1.24 ± 0.23 (0–25) 9.02 ± 0.80 (0–50) 6.90 ± 0.90 (0–65)  Ferns 4.36 ± 0.42 (0–50) 2.19 ± 0.97 (0–80) 5.67 ± 1.33 (0–90)  Club mosses 0 17.5 ± 1.8 (0–90) 0  Mosses 21.5 ± 1.4 (0–90) 0.28 ± 0.08 (0–5) 0.36 ± 0.16 (0–15)  Total 28.6 ± 1.5 (0–95) 38.6 ± 2.1 (3–100) 18.2 ± 1.8 (0–100) Values are presented as mean ± SEM (range) for 1 m2 sampling squares. Open in new tab Table 1. Groundcover vegetation and surface cover composition of plots used for sampling different blacklegged tick life stages . Percent composition . . Adult plot (n = 200) . Nymphal plot (n = 130) . Larval plot (n = 120) . Surface substrate  Boulder/stone 32.0 ± 2.1 (0–98) 0.06 ± 0.05 (0–6) 0.28 ± 0.19 (0–20)  Gravel/cobble 0 0 0  Mineral soil/sand 0.53 ± 0.14 (0–15) 2.94 ± 0.40 (0–20) 3.93 ± 0.76 (0–70)  Leaf litter/organic matter 55.7 ± 2.0 (0–97) 85.0 ± 1.1 (15–100) 85.4 ± 1.3 (20–98)  Coarse woody debris 11.8 ± 1.1 (0–95) 12.0 ± 1.1 (0–80) 11.5 ± 1.6 (0–80)  Total 100 100 100 Groundcover vegetation  Woody plants 1.55 ± 0.30 (0–30) 9.61 ± 0.93 (0–70) 5.28 ± 0.89 (0–80)  Herbaceous plants 1.24 ± 0.23 (0–25) 9.02 ± 0.80 (0–50) 6.90 ± 0.90 (0–65)  Ferns 4.36 ± 0.42 (0–50) 2.19 ± 0.97 (0–80) 5.67 ± 1.33 (0–90)  Club mosses 0 17.5 ± 1.8 (0–90) 0  Mosses 21.5 ± 1.4 (0–90) 0.28 ± 0.08 (0–5) 0.36 ± 0.16 (0–15)  Total 28.6 ± 1.5 (0–95) 38.6 ± 2.1 (3–100) 18.2 ± 1.8 (0–100) . Percent composition . . Adult plot (n = 200) . Nymphal plot (n = 130) . Larval plot (n = 120) . Surface substrate  Boulder/stone 32.0 ± 2.1 (0–98) 0.06 ± 0.05 (0–6) 0.28 ± 0.19 (0–20)  Gravel/cobble 0 0 0  Mineral soil/sand 0.53 ± 0.14 (0–15) 2.94 ± 0.40 (0–20) 3.93 ± 0.76 (0–70)  Leaf litter/organic matter 55.7 ± 2.0 (0–97) 85.0 ± 1.1 (15–100) 85.4 ± 1.3 (20–98)  Coarse woody debris 11.8 ± 1.1 (0–95) 12.0 ± 1.1 (0–80) 11.5 ± 1.6 (0–80)  Total 100 100 100 Groundcover vegetation  Woody plants 1.55 ± 0.30 (0–30) 9.61 ± 0.93 (0–70) 5.28 ± 0.89 (0–80)  Herbaceous plants 1.24 ± 0.23 (0–25) 9.02 ± 0.80 (0–50) 6.90 ± 0.90 (0–65)  Ferns 4.36 ± 0.42 (0–50) 2.19 ± 0.97 (0–80) 5.67 ± 1.33 (0–90)  Club mosses 0 17.5 ± 1.8 (0–90) 0  Mosses 21.5 ± 1.4 (0–90) 0.28 ± 0.08 (0–5) 0.36 ± 0.16 (0–15)  Total 28.6 ± 1.5 (0–95) 38.6 ± 2.1 (3–100) 18.2 ± 1.8 (0–100) Values are presented as mean ± SEM (range) for 1 m2 sampling squares. Open in new tab Statistical Analyses All data were analyzed using R-3.5.2 for Windows (https://www.r-project.org/) and are presented as mean ± SEM. A power analysis was conducted for each life stage to determine sample size as number of transects needed to detect a significant difference in number of ticks collected between drag fabrics based on sample variation reported by Simmons et al. (2015) (α = 0.05, power = 0.80, effect size = 0.25). These analyses showed minimum sample sizes of 25 transects for adults, 10 for nymphs, and 33 for larvae. The sample size for the larval life stage was limited to 12 because all larvae could not be removed from drags after each transect and a new drag was needed for each sample. We examined the assumptions of normality of data for all life stages using a Shapiro–Wilk test, and as a result, nymph data were log-transformed to meet the normality assumption. For each life stage, a number of ticks collected per transect were compared across fabrics using a mixed-effect analysis of variance (ANOVA), treating fabrics as fixed effects and observers and transects as separate random effects (R packages lme4 v.1.1–25 and lmerTest v.3.1-3, Bates et al. 2015, Kuznetsova et al. 2017). We then followed the ANOVA with pairwise comparisons between our fixed effects using a Tukey’s test post hoc analysis (R package emmeans v.1.5.2-1; Lenth 2020). For larvae, we also compared the proportion of ticks remaining on drags at the end of the transects after collection with lint rollers, using the same approach. Habitat was not included in the analyses because drags were pulled side-by-side in unison to minimize differences in surface substrate and groundcover vegetation between fabrics. Furthermore, although we characterized surface substrate and groundcover vegetation for each of the 10-m drag segments, these habitat measures varied considerably between segments and were therefore not combined for transect-level analyses. In addition, we only recorded nymph and adult numbers at the transect and not the segment level due to their low densities. Results Although all of the plots were heterogeneous with sparsely and heavily vegetated patches ranging from 0 or 3% to 95 or 100% groundcover (Table 1), overall the adult plot habitat had the most uneven terrain due to boulders interspersed with coarse woody debris and ferns (Fig. 3A), whereas the nymphal plot habitat was mostly club mosses covering leaf litter (Fig. 3B), and the larval plot habitat was mostly exposed leaf litter (Fig. 3C). The lowest temperature at which any ticks were sampled was 18.3°C for adults, well above the uncoordinated activity threshold of 9.2°C (Clark 1995), and the midrange sampling day temperature and relative humidity for adults (n = 5) were 19.2 ± 2.6°C and 35.3 ± 5.8%, nymphs (n = 3) were 23.4 ± 2.8°C and 79.5 ± 1.4%, and larvae (n = 2) were 19.8 ± 1.0°C and 84.0 ± 2.3%, respectively. Fig. 3. Open in new tabDownload slide Representative habitat in plots for sampling of (A) adults, (B) nymphs, and (C) larvae. Fig. 3. Open in new tabDownload slide Representative habitat in plots for sampling of (A) adults, (B) nymphs, and (C) larvae. For each life stage, there was a significant difference in number of ticks collected across drag fabrics (Table 2). The number of adults collected on flannel was 76.9% greater than on canvas (P < 0.001) and 58.6% greater than on corduroy (P = 0.004), and there was no difference between canvas and corduroy (P = 0.825). The number of nymphs collected on flannel and corduroy were 47.2% (P = 0.002) and 55.5% (P = 0.003) greater than on canvas, respectively, and flannel and corduroy did not differ from one another (P = 0.996). The total number of larvae collected on flannel was 74.9% greater than on canvas (P = 0.005), and the number of larvae collected on corduroy was intermediate between these fabrics, but not significantly different from either flannel (P = 0.117) or canvas (P = 0.320). There was also a significant difference across fabrics in the proportion of ticks remaining on drags after lint-rolling (F = 88.39; df = 2, 20; P < 0.001). The proportion left on flannel (31.1 ± 3.3%) was 13.4-fold greater than on canvas (2.32 ± 0.53%; P < 0.001) and 10.37-fold greater than on corduroy (3.0 ± 0.6%; P < 0.001), and there was no difference between canvas and corduroy (P = 0.956). Table 2. Number of blacklegged ticks collected per 100 × 1 m linear transect using different drag fabrics . Number of ticks per transect . . Life stage . Canvas . Corduroy . Flannel . ANOVA . Adult (n = 25) 2.08 ± 0.43a 2.32 ± 0.42b 3.68 ± 0.34a,b F = 9.08; df = 2, 46.15; P < 0.001 Nymph (n = 13) 6.23 ± 1.97c,d 9.69 ± 1.43c 9.17 ± 0.87d F = 9.80; df = 2, 22.8; P < 0.001 Larva (n = 12) 241.4 ± 41.2e 316.4 ± 38.7 422.3 ± 59.6e F = 6.46; df = 2, 20; P = 0.007 . Number of ticks per transect . . Life stage . Canvas . Corduroy . Flannel . ANOVA . Adult (n = 25) 2.08 ± 0.43a 2.32 ± 0.42b 3.68 ± 0.34a,b F = 9.08; df = 2, 46.15; P < 0.001 Nymph (n = 13) 6.23 ± 1.97c,d 9.69 ± 1.43c 9.17 ± 0.87d F = 9.80; df = 2, 22.8; P < 0.001 Larva (n = 12) 241.4 ± 41.2e 316.4 ± 38.7 422.3 ± 59.6e F = 6.46; df = 2, 20; P = 0.007 Values are presented as mean ± SEM. For each life stage means sharing superscripts are significantly different from one another at P < 0.05 using a Tukey’s test. Open in new tab Table 2. Number of blacklegged ticks collected per 100 × 1 m linear transect using different drag fabrics . Number of ticks per transect . . Life stage . Canvas . Corduroy . Flannel . ANOVA . Adult (n = 25) 2.08 ± 0.43a 2.32 ± 0.42b 3.68 ± 0.34a,b F = 9.08; df = 2, 46.15; P < 0.001 Nymph (n = 13) 6.23 ± 1.97c,d 9.69 ± 1.43c 9.17 ± 0.87d F = 9.80; df = 2, 22.8; P < 0.001 Larva (n = 12) 241.4 ± 41.2e 316.4 ± 38.7 422.3 ± 59.6e F = 6.46; df = 2, 20; P = 0.007 . Number of ticks per transect . . Life stage . Canvas . Corduroy . Flannel . ANOVA . Adult (n = 25) 2.08 ± 0.43a 2.32 ± 0.42b 3.68 ± 0.34a,b F = 9.08; df = 2, 46.15; P < 0.001 Nymph (n = 13) 6.23 ± 1.97c,d 9.69 ± 1.43c 9.17 ± 0.87d F = 9.80; df = 2, 22.8; P < 0.001 Larva (n = 12) 241.4 ± 41.2e 316.4 ± 38.7 422.3 ± 59.6e F = 6.46; df = 2, 20; P = 0.007 Values are presented as mean ± SEM. For each life stage means sharing superscripts are significantly different from one another at P < 0.05 using a Tukey’s test. Open in new tab Discussion For all life stages, flannel performed as well or better than the other fabrics, supporting its recommended use in the recently published standard tick collection methods developed specifically for I. scapularis (CDC 2018) and generally for ixodid species including I. scapularis (Springer et al. 2016, Newman et al. 2019). For nymphs, corduroy and flannel performed equally well, indicating that assessments of acarological risk based on the density of pathogen-infected nymphs using either fabric are comparable to one another (Mather et al. 1996, Eisen and Eisen 2016). One explanation for the greater overall efficacy of flannel is that the fabric’s nap made it easier for ticks to attach and stay attached compared with canvas or corduroy. This explanation is most reasonable for adults because they have a more difficult time clinging to drags than do nymphs, especially considering the more uneven terrain where adults were sampled in our study. Ixodes scapularis adults have been shown to drop-off brushed bull denim drags at 1.8-fold higher rates than nymphs (0.083/m vs 0.047/m) collected on open forest floor with limited vegetation (Borgmann-Winter and Allen 2020). Furthermore, I. scapularis adults have been shown to drop-off corduroy drags in one-third of the distance in densely compared with sparsely vegetated habitats (mean distances of 11.5 m vs 38.0 m; Schulze and Jordan 2001). In contrast to adults, in our study, there was no difference in relative collection efficiency between corduroy and flannel for nymphs suggesting they were able to grip the wales on corduroy as well as the nap on flannel or find protection between the wales. Another explanation for the overall greater efficiency of flannel is that the fabric caught the leaf litter and vegetation to a greater extent than canvas or corduroy causing more disturbance and allowing more attachment time, although we are unaware of studies providing insight into the possible contribution of fabric catch. Significantly more larvae were collected on flannel compared with canvas, and the number of larvae on corduroy was intermediate, but not significantly different from either. The greater efficacy of flannel for collecting larvae may be outweighed by the difficulty of removing them from the nap. Only two-thirds of larvae could be removed from flannel by lint-rolling twice, whereas 97% could be removed from canvas and corduroy. Also, in contrast to the concerns of Salomon et al. (2020) that larvae could hide in the crevices between corduroy wales and be overlooked, we had more difficultly seeing and handpicking larvae burrowed in flannel nap than on canvas weave or between corduroy wales. The substantial residual sample can be problematic because as many as 166 and 731 larvae were collected in a 10-m interval and 100-m transect, respectively. An advantage of using corduroy to collect larvae is that most can be easily removed by lint-rolling so there is minimal carryover between collection sites when using the same drag. Our findings apply to collecting I. scapularis using drags constructed with single pieces of unweighted sturdy cloth during peak activity levels under late spring and summer environmental conditions representative of the mid-Atlantic region of the United States. The wider application of our findings using differently designed drags, under various environmental conditions, in other regions of the United States and Canada, and for other members of the Ixodes ricinus species complex should be taken into consideration. Drag cloths have been modified to increase contact with substrate by weighting the trailing edge, adding a second dowel midway between the leading and trailing edges, or dividing into strips; they have been augmented with CO2 from portable gas cylinders (Eisen and Eisen 2016, CDC 2018). Although the performance of drags with unweighted or weighted corduroy, felt, flannel, or muslin one-piece cloths have been compared with other techniques using flags, dry-ice traps, walking humans, small mammal hosts, and CO2 augmentation for collection of I. scapularis (Ginsberg and Ewing 1989, Falco and Fish 1992, Solberg et al. 1992, Schulze et al. 1997, Rulison et al. 2013, Mays et al. 2016), the different drag cloth modifications and fabrics have not been compared with one another. Although the effect of temperature on attachment and dislodgement of Ixodes scapularis from drags has not been directly investigated, in our phenology study (Simmons et al. 2015), we had to take extra care not to lose adults falling-off canvas drags while being examined for ticks in the late fall and early spring at temperatures near a collection threshold of 4°C because they moved slowly and clung weakly to the fabric (personal observation). We had chosen a collection threshold temperature of 4°C because Duffy and Campbell (1994) had observed a dramatic decrease in number of drag-collected I. scapularis adults at temperatures below this threshold, and Clark (1995) estimated uncoordinated activity and activity threshold temperatures of 9.2 and 6.2°C for females and 11.2 and 8.5°C for males, respectively. The effect of temperature has been investigated for the closely related Eurasian species Ixodes ricinus (L.) (Acari: Ixodidae) and Ixodes persulcatus (Schulze) (Acari: Ixodidae) (Uspensky 1993). Consistent with our observation, 52% fewer I. ricinus attached to flannel drags pulled over 25-m transects, and 60% fewer I. ricinus and 28% fewer I. persulcatus remained attached at cooler (6–10°C) compared with warmer (17–22°C) temperatures. Information on collection efficiency of drags for I. scapularis beyond the mid-Atlantic region of the United States (Daniels et al. 2000, Simmons et al. 2015), and for members of the I. ricinus complex species, other than I. scapularis is very limited. In the southeastern United States, collection of I. scapularis nymphs using drags is much less effective than in the upper Midwest and northeast due to differences in questing behavior, with nymphs in the southeast remaining under leaf litter and rarely contacting drags (Arsnoe et al. 2019). The absolute collection efficiency of flannel blankets for nymphs of the western United States species Ixodes pacificus (Cooley & Kohls) (Acari: Ixodidae) was estimated to be 5.9% in a study conducted in California by Tälleklint-Eisen and Lane (2000). The similarity of this value to the absolute collection efficiencies of 6.7 and 9.9% calculated for I. scapularis nymphs by Daniels et al. (2000) in a New York study and Simmons et al. (2015) in a Pennsylvania study, respectively, suggest that the two species exhibit similar drag attachment and dislodgement characteristics. Vassallo et al. (2000) compared the relative efficiencies of drags made from the clothes cotton, woolen flannel, ‘molleton’ (soft thick cotton), or toweling (a towel, sponge cloth) for collection of I. ricinus nymphs. They found that toweling was the most optimal cloth but did not distinguish between the other cloths. In addition, they used 0.25 × 1 m strips of cloth that were pulled at a speed of 0.5 m/s (20 s/10 m), so the results are not comparable to ours because their cloths were one-quarter of the area and pulled three times faster than our methods. More recently, Gil de Mendonça (2018) compared the relative efficiency of 1 × 1 m flags made from thin flannel or ‘heavier and thicker fabric with complex structure’ (in our opinion burlap-like material based on the published SEM and photograph figures) to collect I. ricinus larvae, nymphs, and adults. There were no differences between the fabrics for the number of nymphs and adults collected, whereas nearly five times more larvae were collected on the flannel flags. As observed in our study, Gil de Mendonça (2018) noted that larvae were difficult to detect and remove from flannel and concluded that these problems made this fabric unsuitable for quantitative sampling of the larval stage. The most relevant difference we observed was the 77 and 59% greater collection of adults using flannel compared with canvas or corduroy, respectively. Based on studies by Daniels et al. (2000) using corduroy and Simmons et al. (2015) using canvas, this would increase the absolute collection efficiency (i.e., percent of actual population collected on a drag after one pass) of adults from approximately 4 to 5% or 6%. Although this increase may be insignificant when calculating the density of infected ticks as a measure of acarological risk or comparing studies done under different environmental conditions that could have more of an effect than fabrics on collection efficiencies, it could be significant when determining the presence of I. scapularis and I. scapularis-borne pathogens. For example, the county-level establishment criteria for ‘reported’ populations of I. scapularis is less than six ticks of a single stage collected within a 12-mo period and for ‘established’ populations greater than or equal to six ticks of a single stage or greater than one life stage collected within a 12-mo period (Dennis et al. 1998, Eisen et al. 2016, CDC 2018). Therefore, a couple more collected adults when the population density is low could make the difference between ‘no records’, ‘reported’, or ‘established’ county status classification. Furthermore, adult I. scapularis are often used to monitor populations for pathogens because infection prevalence is typically greater that found in nymphs (Eisen and Paddock 2020), and the CDC (2018) recommends that at least 50 ticks and not less than 25 of a given life stage be tested within a county to calculate infection prevalence with reasonable confidence. Therefore, a few more collected adults when infection prevalence is low could make the difference between documenting presence or calculating acceptable infection prevalence estimates of a pathogen. Although our study focused on I. scapularis because it is responsible for most cases of vector-borne diseases in the United States (Rosenberg et al. 2018), other tick species of particular concern include Amblyomma americanum (Linnaeus) (Acari: Ixodidae), Amblyomma maculatum Koch (Acari: Ixodidae), Dermacentor andersoni Stiles (Acari: Ixodidae), Dermacentor occidentalis Marx (Acari: Ixodidae), Dermacentor variabilis (Say) (Acari: Ixodidae), and Rhipicephalus sanguineus (Latreille) (Acari: Ixodidae) (CDC 2020b). For surveillance of these species, the CDC (2020b) also recommends using drags constructed with rubberized cotton flannel sheeting like its recommendation for I. scapularis. However, we are likewise aware of only a couple studies comparing the relative collection efficiencies of different fabrics for drag or flag-collection of these species. Newman et al. (2019) found muslin to be more effective than flannel for surveying ticks when all active stages of A. americanum, D. variabilis, and I. scapularis were analyzed together. However, they could not attribute the difference to any one species or stage. Espada et al. (2020) found corduroy to more effective than denim for collecting A. americanum nymphs, but caution that this difference may have been due to a statistical artifact. Coincidentally, they propose that in the future denim and corduroy be compared with CDCs recommended rubberized cotton flannel sheeting. Studies on these species to estimate the absolute collection efficiency of drags or flags are also scarce. Sonenshine et al. (1966) calculated that ≤8% of D. variabilis adults were collected with muslin, Lane et al. (1985) calculated that 7% of D. occidentalis were collected with white flannel, and Carroll et al. (1991) calculated that 20% of D. variabilis adults were collected with flannel sheeting. Given that these collection efficiencies are low, surveillance for tick species of concern could benefit from experiments similar to our study of I. scapularis. In conclusion, although drag construction, environmental, geographic, and I. ricinus complex species-specific biological factors may affect the collection efficiency of drags and possibly increase or decrease the relative differences that we observed in our study, our findings indicate it is unlikely flannel would not perform at least as well as other fabrics because of its nap. Moreover, they support the use of flannel to maximize the number of ticks collected with the caveat that larvae will take extra effort to detect and remove from the fabric. Acknowledgments We thank Dr. Michael Tyree for his valuable input on the study design. This work was partially supported by a graduate student research award to E.N.W. from the Indiana University of Pennsylvania School of Graduate Studies and Research. 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TI - Relative Efficiency of Drag Fabrics for Collection of Blacklegged Tick (Acari: Ixodidae) Larvae, Nymphs, and Adults
JF - Journal of Medical Entomology
DO - 10.1093/jme/tjab002
DA - 2021-01-28
UR - https://www.deepdyve.com/lp/oxford-university-press/relative-efficiency-of-drag-fabrics-for-collection-of-blacklegged-tick-TLbRSC9nPK
SP - 1
EP - 1
VL - Advance Article
IS - 
DP - DeepDyve
ER -