Introduction
Anthropogenic environmental changes continue to drive the increasing frequency of zoonotic disease emergence – diseases transmitted between wildlife and human populations (Allen et al. 2017; Gibb et al. 2020). Zoonotic diseases emerge from a suite of processes that require spatio-temporal overlap between humans and infected hosts or vectors for spillover occurrence. Urban ecosystems are a hotbed for emerging zoonoses due to opportunistic species adapted to anthropic landscapes that serve as zoonotic hosts and the existence of interfaces between humans, wildlife, and/or vectors where contact and pathogen spillover can occur (Alirol et al. 2011; Hassell et al.2017). Through movement, wildlife hosts influence contact rates between vectors, pathogens, and other hosts, ultimately shaping the distribution of zoonotic hazards in complex multi-host-pathogen systems.
Urban wildlife movement patterns are driven by landscape-dependent and independent fragmentation. Landscape-dependent fragmentation (LDF) alters the physical configuration of habitat patches, preventing species from moving freely across the landscape as patches become increasingly isolated (Magle et al. 2014; Berger-Tal & Saltz 2019). As natural land is converted to impervious surface, wildlife hosts aggregate in remaining habitat fragments leading to increased contact rates and spatial hotspots of transmission and spillover (Wilkinsonet al. 2018). Landscape-independent fragmentation (LIF) results from anthropogenic disturbances which change animals’ perception and use of their environment (Berger-Tal & Saltz 2019). For example, resource subsidies lead to LIF whereby fertilized vegetation, gardens, or waste byproducts (Becker et al. 2015; Langley et al. 2021) provide stable, often predictable, resources which influence wildlife host movement (Ossi et al. 2020; Ranc et al. 2020) and contact patterns at the human interface, where zoonotic hazard becomes risk.
Tick-borne disease emergence is intertwined with land use change and habitat fragmentation (Diuk-Wasser et al. 2021) and tick-borne diseases are the most common vector-borne zoonoses in temperate North America, Europe, and Asia. In the United States, Lyme disease (LD), a bacterial infection caused by Borrelia burgdorferi sensu stricto , affects 400,000 people annually (Kugeler et al. 2021; Schwartz et al. 2021). Historically, LD was associated with the incursion of suburban and exurban development into rural areas (Barbour & Fish 1993). More recently, ticks expanded their geographic range with climate change (Sonenshine 2018; Ogden et al. 2021) and by occupying diverse and novel landscapes such as cities (VanAcker et al. 2019). The urban expansion of LD occurs through two pathways increasing human risk of exposure to the LD hazard: (1) vegetation increases in cities undergoing de-urbanization linked with population decline and land abandonment (Eskew & Olival 2018; Richards & Belcher 2019), or through cities adopting urban greening strategies (Yanget al. 2014; Halsey et al. 2022); and (2) expanding urban matrix into surrounding natural habitats. Both pathways increase tick habitat and the prevalence of wildland-urban interfaces where species richness is dominated by synanthropic wildlife species, often tick hosts or pathogen reservoirs (Gibb et al. 2020), and human exposure to ticks is high (Diuk-Wasser et al. 2021).
In the eastern and midwestern US, the establishment and persistence of the LD vector Ixodes scapularis ticks is supported by large mammal hosts. For adult I. scapularis , white-tailed deer (Odocoileus virginianus , hereafter deer) are the primary reproductive stage host (Barbour & Fish 1993; Rand et al. 2004; Ostfeld et al. 2018). Importantly, while deer amplify the vector for LD (Carpi et al. 2008; Cagnacci et al. 2012), deer are not susceptible to B. burgdorferi infection and do not supportB. burgdorferi transmission (Telford III et al. 1988). Studies predicting the distribution of I. scapularis ticks and LD over large geographic areas typically utilize broad-scale climatic and landcover variables (Estrada-Peña 1998; Diuk-Wasser et al. 2006; Soucy et al. 2018). This approach, however, lacks power to predict the zoonotic hazard at fine-spatial scales because it ignores local LD ecology and the modulating role of host movement in fragmented environments at different spatial (home range, fine scale movements) and temporal (seasonal, diel) scales.
Available niches for parasites are shaped by movement and resource selection of wildlife hosts (Ezenwa et al. 2016). Thus, the probability of tick population establishment is affected by the hosts’ scale of response to the landscape – for example, the scale at which deer select and establish their home range. Wildlife resource selection spans multiple spatial scales and is hierarchically nested (Johnson 1980), where broad-scale selection constrains fine-scale selection (Senft et al. 1987). Multi-scale selection is integral to consider in urban landscapes where deer often display urban-adapted behavior such as foraging close to households (Swihart et al.1995; Kilpatrick et al. 2000; Grund et al. 2002) while resting in forest patches. If deer habitat selection encompasses anthropogenic resources, residential areas may experience enhanced exposure to infected ticks. Because ticks passively fall from hosts upon engorgement, host movement speed and directionality through varying landcovers affect tick spatial clustering and ticks’ likelihood of survival post-feeding. Further, the burden of I. scapularis ’ life stages on deer varies with tick phenology such that seasonal movement patterns exhibited by deer may differentially affect which life stages are dispersed, when, and to where.
This study examines fine-scale deer movement in an urban, fragmented borough of New York City (NYC) to determine how deer movement links to local distributions of I. scapularis ticks and heightened LD hazard. We employ a multi-scale hierarchical resource selection framework to (i) examine deer’s scale of response to anthropogenic landscape features when establishing their home-range (i.e., responses to LDF in 2nd order selection), (ii) determine fine-scale spatiotemporal effects of the urban landscape on within-home range habitat selection and avoidance (i.e., responses to LIF in 3rd order selection), and (iii) assess the spatial congruence between deer seasonal habitat selection and LD hazard. We expect high intensity development will restrict deer home range selection at fine-spatial scales through limiting available natural habitat and creating movement barriers. We expect deer to exhibit diel variation when selecting for features within the home range and to avoid highly anthropic areas during periods of heightened human activity. We further hypothesize that vegetated neighborhoods nested within areas connected to natural habitats will attract deer to fine-scale foraging resources and support the microclimate for tick survival, leading to higher tick occupancy compared to neighborhoods that are less accessible to deer and/or present more hostile microclimates for I. scapularis.
With the majority of the human population residing in cities (United Nations, Department of Economic and Social Affairs 2018) and the recent increase of tick-borne diseases in urban areas globally (Hamer et al. 2012; Rizzoli et al. 2014; Hansford et al. 2017, 2021; Heylen et al. 2019; VanAcker et al. 2019; Simmonset al. 2020; Sormunen et al. 2020), there is an urgent need to understand the urban ecology of tick-borne disease emergence and the determinants of heterogeneity in tick-borne disease hazard. Here, we pair deer movement and tick surveillance data to provide the first study that links deer movement behavior to tick distribution across a highly urban landscape. We conclude that resource selection at different spatial scales enables urban deer to navigate fragmented habitat and that sex and individual-based responses to human activity characterize differences in tick distribution capacity.