Association between tick density, park, site type and habitat. From 20 May to 12 August 2019, 432 drags were performed (Clove Lakes: n=168; Conference House: n=134; Willowbrook: n=132). All three habitats (maintained grass, leaf litter, and unmaintained herbaceous) were present in Clove Lakes and Willowbrook; however, no leaf litter habitat was present in Conference House sites (see Additional file 3).
A total of 10,036 ticks were collected across all parks and sites, including 7,133 H. longicornis (adults: n=489; nymphs: n=2,599; larvae: n=4,045), 1,972 A. americanum (adults: n=28; nymph: n=157; larvae: n=1,787) and 931 I. scapularis (adults: n=0; nymphs: n=85; larvae: n=846) (Additional file 7), with temporal variation by life stage (Additional file 8). Focusing on the nymphal data since we targeted the nymphal questing period, nymphs were mainly collected in transects along trails (n=2663), followed by open spaces (n=98), and at the edge of open spaces (n=80) (Additional file 9). Across habitat type, more total nymphs were collected in unmaintained herbaceous habitats (n=2770), followed by maintained grass (n=52), and leaf litter (n=19), though counts varied by species (Additional file 10).
The density (number of nymphs per 100 m2) of A. americanum was highest in Conference House and unmaintained herbaceous areas compared to maintained grass habitats (Table 1). After accounting for the drag habitat, the density of A. americanum nymphs in the strip of vegetation at the edge of open spaces was lower compared to trails (Table 1). For this species, the best model with the lowest AIC is presented, and no competing models were within 2 AIC. On the other hand, model averaging was conducted for H. longicornis and I. scapularis. Model results showed that the density of I. scapularis nymphs was best explained by park and drag habitat, where the density of I. scapularis per 100 m2 was greatest in Conference House, in leaf litter, and in unmaintained herbaceous locations (Table 1). The density of H. longicornis nymphs in Conference House was best described by site type and drag habitat, with densities per 100 m2 greatest in unmaintained herbaceous habitats compared to maintained grass and along trails (Table 1).
Table 1
Generalized linear model (negative binomial regression) summary for each species. Open spaces had either an edge (E) if the transect was at the limit of the area or no edge (NE) if the transect was in the interior of the open space. Relative abundance is the expected log count of nymphs for each unit of increase of the categorical variable compared to the reference variable.
Variable | Category | Relative abundance per 100 m2; 95% CI | p-value | Number of predicted ticks per 100 m2; 95% CI |
A. americanum |
Intercept | | 0.0004 (0, 0.001) | <0.001 | |
Park | Clove Lakes | 1 | | 1.13 (0.33, 3.83) |
Conference House | 33.09(8.12, 134.95) | <0.001 | 37.44 (17.93, 78.21) |
Willowbrook | 1.69 (0.36, 7.83) | 0.502 | 1.91 (0.66, 5.52) |
Site type | Trail | 1 | | 7.51 (3.38, 16.68) |
Open space NE | 0.87 (0.23, 3.36) | 0.840 | 6.54 (2.49, 17.18) |
Open space E | 0.22 (0.07, 0.72) | 0.012 | 1.65 (0.44, 6.22) |
| Unmaintained herbaceous | 1 | | 8.97 (3.94, 20.42) |
Habitat | Maintained grass | 0.17 (0.04, 0.78) | 0.023 | 1.50 (0.38, 5.96) |
Leaf litter | 0.67 (0.14, 3.13) | 0.611 | 6.01 (1.67, 21.68) |
H. longicornis |
Intercept | | 0.24 (0.17, 0.32) | <0.001 | |
Site type | Trails | 1 | | 762 (327.1, 1777) |
Open space NE | 0.43 (0.09, 1.84) | 0.258 | 380 (174.2, 827) |
Open space E | 0.26 (0.11, 0.63) | 0.003 | 254 (72.8, 885) |
Habitat | Unmaintained herbaceous | 1 | | 1435 (689.1, 2990) |
Maintained grass | 0.09 (0.02, 0.38) | 0.001 | 122 (41.7, 358) |
I. scapularis |
Intercept | | 0.002 (0, 0.014) | <0.001 | |
Park | Clove Lakes | 1 | | 7.96 (0.98, 64.7) |
Conference House | 4.43 (1.72,10.83) | 0.006 | 33.09 (4.04, 270.9) |
Willowbrook | 0.89 (0.34, 2.32) | 0.806 | 7.06 (0.87, 57.4) |
Site type | Trails | 1 | | 12.5 (1.67, 9.41) |
Open space NE | 1.15 (0.35, 3.84) | 0.927 | 12.8 (1.69, 97.3) |
Open space E | 0.62 (0.20, 1.88) | 0.79 | 11.6 (1.45, 92.6) |
Habitat | Unmaintained herbaceous | 1 | | 31.71 (4.58, 219.7) |
Maintained grass | 0.04 (0.01, 0.34) | 0.003 | 1.39 (0.09, 22.2) |
Leaf litter | 1.33 (0.48, 3.71) | 0.583 | 42.25 (5.46, 326.9) |
Park, site type, and habitat usage by park visitors. From 20 May to 19 August, a total of 5,910 individuals were observed entering the parks (Clove Lakes: n=2,773; Conference House: n=1,162; Willowbrook: n=1,975). Fewer people visited Conference House compared to Clove Lakes and Willowbrook, and more people visited Clove Lakes compared to Willowbrook (P < 0.001 for all comparisons). Across all parks, 3,214 visitors were men and 2,632 were women (P < 0.001), when observed gender could be determined, and more adults visited the parks compared to children, teens, and seniors (P < 0.0001 for all comparisons); however, adults made up the largest age range group (ages 20-60) (Table 2). More children were in Conference House compared to Clove Lakes (P = 0.0043) followed Willowbrook (P = 0.009), while more children were in Willowbrook compared to Clove Lakes (P < 0.0001). Teen counts were the same for all parks (P > 0.1). Clove Lakes had higher adult and senior counts compared to Conference House and Willowbrook (P < 0.0001 for all comparisons); however, more adults visited Willowbrook than Conference House (P < 0.0001), and Conference and Willowbrook had equal counts of seniors (P = 0.3685). Regarding gender, female and male counts were higher in Clove Lakes compared to Conference House and Willowbrook parks. Counts for both genders were higher in Willowbrook compared to Conference House (P < 0.0001 for all comparisons) (see Table 2).
Table 2
Counts of park visitors by age group and gender. The total number (n) and percent of total visitors (%) in each park within each group.
Park | Gender n (%) | Age group n (%) |
| Male | Female | Child | Teen | Adult | Senior |
Clove Lakes | 1,583 (56.8) | 1,194 (43.2) | 200 (7.2) | 207 (7.4) | 1,877 (67.7) | 490 (17.7) |
Conference House | 649 (55) | 529 (44.9) | 288 (24.3) | 151 (12.7) | 582 (49) | 166 (14) |
Willowbrook | 1,032 (52.4) | 945 (47.6) | 402 (20.3) | 174 (8.8) | 1,187 (60) | 214 (10.8) |
Visitor counts in each site type and habitat varied and were influenced by gender and age group in each park (see Additional file 11). Generally, open spaces were used more than trails, and impervious surfaces were used more than habitats with vegetation. In Clove Lakes, age group counts varied by habitat but not site (P < 0.0001 and P = 0.6794, respectively), with adults visiting impervious, impervious-maintained grass, maintained grass, and unmaintained herbaceous habitats more than other groups. Gender counts were the same across site and habitat (P = 0.0958 and P = 0.056, respectively). In Conference House, gender and age group counts differed by both site and habitat type (P < 0.0001 for all comparisons), with more males visiting trails and unmaintained herbaceous habitats compared to females. Adults visited trails and open spaces most often, and adults went into impervious-maintained grass, maintained grass, and unmaintained herbaceous habitats more than other groups. In Willowbrook, age group counts differed across habitat and site type (P < 0.0001 for both comparisons), with adults visiting trails, open spaces, impervious, impervious-maintained grass, leaf litter, maintained grass, and unmaintained herbaceous most often. Gender counts only differed across habitat, not site (P = 0.0027 and P = 0.7048, respectively) with men visiting impervious, leaf litter, and maintained grass-leaf litter environments more than females.
Across all parks, visitors were exposed to maintained grass habitats for the longest time duration (Additional file 12). In Clove Lakes, exposure time to different habitats was also influenced by age but not gender (P < 0.0001 and P = 0.2927, respectively) with children in the grass longer than teens, adults, and seniors (P < 0.0001 for all comparisons). In Conference House, exposure time varied by age and gender (P=0.0049 and P=0.002, respectively) with children exposed longer than teens and adults (P = 0.0258 and P = 0.0049, respectively) and females exposed longer than men (P = 0.002). Age and gender did not impact habitat exposure times in Willowbrook (P = 0.2930 and P = 0.9723, respectively).
Picnicking (average range across all parks: 16-25 mins), socializing (28 mins), exercising (2-29 mins), sitting (13-14 mins), tanning (8-20 mins), and engaging in arts and photography (4- 25 mins) were long-stay activities that occurred in maintained grass habitats, potentially exposing many individuals to low levels of ticks, especially if occurring near a forested edge with leaf litter. Activities in more hazardous habitats such as walking (average duration across all parks:<1-3 mins), jogging (<1 min), biking (<1-1 min), and working (3 mins) were more short-stay activities that exposed fewer visitors to hazardous habitats for less time (Additional file 13).
Tick hazard.
When combining the tick density estimated at each location with the human exposure time estimated over a period of 30 min through observations, we found that both the probability of finding a tick during that period based on the density and time spent in the area was higher in trails compared to open areas for all species (see Figure 2). During a 30 min period, individuals had a small probability (median =0.1%; IQR: 0-0.2%) of encountering an I. scapularis nymph when transiting trails, but the probability of encountering an I. scapularis nymph in open areas was almost zero (median probability: 0% IQR: 0-0%, Q99: 0.7%). A similar pattern was observed for A. americanum, with a median 0.02% (IQR: 0-0.08%) probability of finding a nymph in trails and an almost zero probability of encountering them in open areas (median probability: 0% IQR: 0-0%, Q99: 1.4%). For both species, the highest probability of finding a nymph was found at Conference House Park (Figure 2). H. longicornis was only found at Conference House Park, and the probability of finding a nymph was also higher in trails compared to open areas (median probability: 7.7%, IQR: 0-15.0% in trails and median probability: 0%, IQR: 0-0%, Q99: 40.3% in open spaces). Although the probability of finding a tick in open areas was almost zero for all species, the estimated individual probabilities was highly variable and non-zero probabilities were estimated for all open spaces (Figure 2).
When we measure the risk of exposure per person during the period analyzed, we estimated an overall risk of 0.03 I. scapularis nymphs per min/m2 (IQR: 0-0.06) in trails but almost zero in open spaces (0 I. scapularis nymphs per min/m2, IQR: 0-0, Q99: 0.07). In comparison, we found a lower overall risk of encountering A. americanum (0.01 A. americanum nymph per min/m2, IQR: 0-0.03 in trails and 0 A. americanum nymphs per min/m2, IQR: 0-0, Q99: 0.42 in open spaces); and a higher risk of encountering H. longicornis (2.36 H. longicornis nymphs per min/m2, IQR: 2.36-7.10 in trails, and 0 H. longicornis nymphs per min/m2, IQR: 0-0, Q99: 3.10 in open spaces). The highest risk of exposure occurred at Conference House Park for all three species.
Survey response rate, demographics, and tick experience. One hundred and ninety surveys were administered across all parks (Clove Lakes: n=65; Willowbrook: n=61, Conference House: n=64). Of the 232 park visitors who were asked to participate in the survey, 42 refused, resulting in an 18% refusal rate. Among the refusals, 52% were male, and 46% of the refusals were observed to be between 50-70 years old. Respondents who agreed to participate were predominately residents of Staten Island (n=176; 93%), male (n=109; 57.4%), white/Caucasian (n=112; 58.9%), and non-Hispanic/Latino (n=153; 80.5%). The age range of respondents was from 18-82 with a median age of 50. Education ranged from having a high school degree or less (n=41; 21.6%) to having a graduate degree (n=24; 12.6%); however, most attended some college or received 2-year college (associates) degree (n=71; 37.4%). The two main sources for acquiring information about ticks and tick-borne diseases were the internet (n=77; 41.4%) and TV/radio (n=37; 19.9%) (Additional file 14).
Most respondents (60%; n=114) had some level of past tick exposure (Additional file 14). Sixty percent of visitors (n=114) reported seeing a tick before. Of those who had seen a tick, 53.5% (n=61) reported finding ticks on either themselves or a household member, and 54.4% (n=61) had found ticks on a pet. Forty-four percent of respondents (n=84) knew someone with Lyme disease, of which 30.9% (n=58) knew one individual and 12.4% (n=23) knew two people. Eighteen percent (n=19) reported having someone in the household with Lyme disease. Prior experience with ticks was not associated with park, visitation frequency, knowledge of tick habitat, knowledge of tick phenotype, perceived probability of tick encounter, knowledge of tick prevention methods, number of prevention methods used, perceived severity, gender, age, education, or owning a dog (P > 0.05).
Knowledge and attitudes. Park visitors were moderately to highly knowledgeable about which specimens were ticks and which were other arthropods but less knowledgeable about disease biology (Additional file 14). Of those who claimed to have seen a tick before, most could distinguish ticks from non-ticks from a sample of eight arthropods (Additional file 6). When asked to recognize the ticks in the sample, 64% (n=72) correctly identified the Dermacentor variabilis adult as a tick, while this fraction decreased to 38.1% (n=43) for A. americanum adults, and 26.5% (n=30) for I. scapularis adult. However, only 3.5% (n=4) were able to tell that the I. scapularis nymph was a tick. Knowledge of tick phenotype was not affected by park, visitation frequency, knowledge of tick habitat, perceived probability of tick encounter, knowledge of tick prevention methods, number of prevention methods used, perceived severity, prior experience with ticks, gender, age, education, or owning a dog (P > 0.05). Additionally, most did not know how ticks become infected with the Lyme bacterium (n=78; 63.7%), and 22.6% (n=24) incorrectly assumed infection was from feeding on deer. Only 8.4% (n=16) knew that infection was caused by feeding on infected mice or on infected animals in general (8.9%, n=17).
Regarding tick habitat, most identified parks as the main source for tick exposure (n=82; 43.2%), followed by woods (n=52; 27.4%) and grass (n=32; 16.8%), and 12.6% (n=24) connected tick presence to the presence of deer (Additional file 14). Knowledge of tick habitat was not affected by park, visitation frequency, knowledge of tick phenotype, perceived probability of tick encounter, perceived severity of ticks, number of known prevention methods, number of used prevention methods, prior experience with ticks, education, gender, age, or owning a dog (P > 0.05).
There were varying responses regarding the reduction of Lyme disease on Staten Island, and visitors could respond with multiple answers (Additional file 14). Most believed that spraying pesticides (n=63; 34.9%), educating the public (n=55; 29.6%), and reducing or controlling deer (n=33; 17.7%) would control the disease. Fewer people reported personal protection measures (n=15; 8.1%), vegetation management (n=12; 6.5%), mice control (n=6; 3.2%) and general tick reduction (n=6; 3.2%). A small proportion (n=19; 10.2%) did not know what could be done, and 4.3% (n=8) said that nothing could reduce Lyme disease.
Knowledge of tick prevention measures was limited (Additional file 14); thirty-three individuals (17.4%) did not know any prevention measures. Of the respondents who were aware of prevention methods, they knew a median of two measures. Sixty-two percent (n=117) knew about insect repellent, 40% (n=76) about wearing long sleeves, 35.8% (n=68) mentioned avoiding tick habitat as a preventative measure, 24.7% (n=47) were familiar with tick checks, and 23.2% (n=44) reported knowing about tucking pants into socks or wearing long socks. Fewer people reported knowing about wearing light colored clothing to spot ticks easily (n=15; 7.9%) and showering after being outdoors (n=10; 5.3%). The number of known preventative measures was not influenced by park, visitation frequency, knowledge of tick phenotype, knowledge of tick habitat, perceived probability of tick encounter, perceived severity of ticks, prior experience with ticks, age, gender, or owning a dog (P > 0.05). However, individuals who practiced more tick prevention methods also knew more tick prevention methods (P < 0.0001).
Perceptions of tick-borne disease severity were moderate to high (Additional file 14). Most respondents believed tick-borne diseases were either extremely serious or very serious (n=80; 42.1%), 15.8% (n=30) believed they were not at all serious or slightly serious, and 20% were unsure about the status of tick-borne diseases on Staten Island (n=38). Individuals who had a higher perceived probability of tick encounter had a higher perception of severity (P = 0.01). Perceived level of severity was not influenced by park, visitation frequency, knowledge of tick phenotype, knowledge of tick habitat, knowledge of tick prevention methods, number of tick prevention methods used, prior experience with ticks, age, gender, education, or owning a dog (P > 0.05).
Practices. While most visitors attended the parks regularly, few and inconsistent personal protective measures were used to prevent tick exposure (Additional file 14). Thirty-six percent (n=69) of respondents reported visiting the parks daily, 18.4% (n=35) several times a week, 10% (n=19) once a week, 10.5% (n=20) once a month, 16.3% (n=31) once a year, and 6.8% (n=13) visited for the park for the first time. Walking/running (n=102; 53.7%), dog walking (n=39; 20.5%), and relaxing (n=28; 14.7%) were the top activities enjoyed by respondents. Respondents who practiced tick prevention methods practiced a median of two methods. Most practiced no methods (32.8%; n=62), while 30.7% practiced one (n=58; 30.7%) and 19% practiced two (n=36) (Table 3). The most used prevention methods were avoiding tick habitat (n=58; 30.7%), using repellent (n=54; 28.5%), wearing long sleeves (n=49; 25.9%), and conducting tick checks (n=34; 18%). Fewer people reported tucking pants into socks or wearing long socks (n=26; 13.8%), wearing light colored clothing (n=7; 3.7%), or showering after being outdoors (n=8; 4%).
Table 3
The number of tick-preventative methods practiced by park visitors. This shows the count and percentage of people who practiced a certain number of methods, with most practicing none.
Number of methods practiced | Number of individuals n (%) |
None | 62 (32.8) |
One | 58 (30.7) |
Two | 36 (19) |
Three | 20 (10.6) |
Four | 10 (5.3) |
Five | 2 (1.1) |
Six | 0 |
Seven | 1 (0.5) |
Most people (n=99; 58%) reported checking for ticks either sometimes or always, while 42% (n=79) reported never checking for ticks (Additional file 14). Those who never checked for ticks believed they were not in an area with ticks (24%; n=46), they reported laziness (12%; n=23), forgot to check (12%, n=22), never had experience with ticks (10%, n=19), or did not think about it at the time (10%; n=19).
Results from the generalized linear model (Table 4) showed that tick check behavior could be best predicted by the number of tick prevention methods known, the perceived probability of tick encounter, and knowledge of tick habitat. With each unit increase in the known number of prevention methods, the odds of checking for ticks increased almost two-fold. The odds of practicing tick checks were 3.7 times more when increasing knowing no prevention methods to knowing two methods. Likewise, with each unit increase in the perceived probability of encountering a tick, the odds of checking for ticks increased 1.6 times. The odds of a park visitor checking for ticks who perceived their risk for tick encounter as “extremely likely” was 6.9 times higher than a person who perceived their risk for tick encounter as “very unlikely”. Knowing tick habitat was not associated with performing tick checks.
Table 4
An additive generalized linear regression model for predicting tick checks. The odds of checking for ticks were obtained by exponentiating the estimate.
Predictor | Estimate | SE | p-value | Odds ratio |
Intercept | -0.7419 | 0.5881 | 0.2712 | NA |
Number of prevention methods known | 0.6605 | 0.2235 | 0.00312 | 1.9 |
Perceived probability of tick encounter | 0.4845 | 0.1711 | 0.00464 | 1.6 |
Knowledge of tick habitat | -0.6434 | 0.3508 | 0.06664 | 0.5 |