Tick-borne diseases present an increasing threat in urban areas, where high human density can intensify human exposure to ticks given suitable habitat and host niches. We highlight considerable risk of tick exposure in residential yards on Staten Island, and demonstrate that the dynamics of three tick vector species in a highly fragmented urban environment are determined by both yard- and landscape-level features. In particular, we found that the distributions of the Lyme disease spirochetes vector, I. scapularis, and of A. americanum was largely determined by yard- and landscape- level factors, whereas H. longicornis was only impacted by yard-level features but not landscape level factors assessed in this study.
Host and habitat association may partially explain yard presence of the three tick species. Tick persistence depends on the local abiotic conditions being conducive to survival (4, 28, 34, 35). The finding that I. scapularis presence is most strongly associated with the amount of large, well connected patches of canopy cover in the surrounding landscape is in line with previous work linking the species to forest habitat and connectivity (43, 46, 70–74). Underlying this relationship is the sensitivity of I. scapularis to desiccation, which may constrain the tick to large, connected patches of canopy cover in urban areas, outside of which high impervious surface cover dramatically increases local temperatures and reduces saturation deficit (75, 76). Both A. americanum and H. longicornis are more tolerant to desiccation and heat stress (77–81), than I. scapularis, allowing them to persist in a range of habitats. In particular, H. longicornis can withstand temperatures up to 40˚C and severe dehydrating conditions under laboratory conditions (77, 82). Differences in the temperature and humidity tolerance of A. americanum and H. longicornis may explain the disparate distributions and landscape associations of the two tick species, despite exhibiting generalist host associations.
At the yard level, log and brush piles was consistently associated with the presence of all tick species. Log and brush piles may act as thermal refugia for ticks, allowing them to persist and to quest near open lawns where they would otherwise desiccate, and may also act as habitat for small-bodied hosts, such as mice, and dens for meso-mammals, such as raccoons (83, 84). Brush piles increase overwinter survival of white-footed mice (85), which act as important hosts for I. scapularis larvae, and the distribution of which may determine where fed larvae are deposited and emerge the following spring as nymphs. Landscaping tick control measures (e.g. clearing brush piles) have been found to increase risk of I. scapularis-associated disease (70) and to have no effect on Lyme disease cases (86). These different findings may reflect the discordant scales and metrics at which the two studies were conducted, the former being a meta-analysis of several studies that aggregated log and brush clearing into a property management risk category, and the latter being a neighborhood-matched case-control study. Our finding of higher probability of nymph presence with log and brush piles may or may not lead to increased human tick exposure and disease depending on human exposure behavior. Further work elucidating human behavior in similar urban settings would provide insights into the relative roles of the natural and human components of urban TBD risk.
As to host associations, adults of all tick species in the study are dependent on white-tailed deer as the primary reproductive stage host (10) and for movement through landscapes (43). However, A. americanum and particularly H. longicornis are also associated with mesomammal hosts, such as raccoons and opossums (21, 77, 87–89). Both nymphal stage A. americanum and H. longicornis have been found to exhibit generalist feeding behavior, feeding on a range of livestock, birds, and small mammal species (77, 90), which would allow them to feed on hosts less limited by landscape structure and fences than deer (e.g. squirrels and racoons; (91). The association between fencing and nymphal I. scapularis and A. americanum, but not H. longicornis, may thus reflect subtle differences in proportional host use between the three species. Differences in host use, and subsequently differences in the impact of the landscape on host movement (i.e. its functional connectivity (93)) may also explain the positive association between I. scapularis and A. americanum in residential yards and canopy cover and connectivity in surrounding yards, but not H. longicornis. Previous work in New York City found considerably greater burdens of immature stages of A. americanum and H. longicornis on raccoons than I. scapularis (89). Additionally, opossums were found to have highest infestation prevalence and intensity of immature H. longicornis than either I. scapularis or A. americanum, providing some support for differences in host use.
Finally, we identified an invasion front for H. longicornis, and potentially for A. americanum, which increased 9-fold and 3-fold, respectively, from 2018 to 2021. Whilst H. longicornis does not yet pose a significant public health risk in the Northeast US, its vector competence for several disease agents in its native range makes it a cause for concern. A. americanum was also more frequently observed over the sampling period, and is currently associated with several disease agents of humans (94, 95). Understanding the environmental factors associated with the distribution of these expanding tick populations, at appropriate spatial scales, is a critical first step towards guiding future policy regarding tick surveillance and management recommendations for individuals in high-risk areas.