Discussion
Host movement is a missing component in predicting vector-borne disease emergence, spread, and transmission (Hartemink et al. 2015; Dougherty et al. 2018) and has mainly been explored through mathematical models (Hartfield et al. 2011; Sumner et al.2017; Tardy et al. 2021). However, individual movement is often not accounted for when modeling the transmission process (Fofana & Hurford 2017). Our results demonstrate individual resource selection of development intensity is modified by deer’s sex, tendency to utilize habitat at the human interface, and their location in the urban matrix. This finding suggests modeling individual-scale movement is essential when assessing hosts’ distribution of ticks and tick-borne pathogens into residential areas.
We observed seasonal sex-based movement differences important for vector dispersal in urban deer. Males moved faster and selected developed habitats more frequently than females, that instead maintained smaller HRs with more forested habitat than developed landcover. This suggests male deer may disproportionately distribute ticks outside of natural areas while females maintain ‘source’ tick populations in urban green spaces through providing bloodmeals and short-distance dispersal opportunities. Further, because male movement was slowest through urban areas during the pre-breeding and females during the breeding season, male movements could drive the distribution of feeding nymphs, while females could propagate feeding adult ticks to human interfaces.
Our analysis identified predictable responses in deer use of specific landcover classes at the individual scale, highlighting the potential to understand deer response under different urban development scenarios. Deer use of wetland and herbaceous habitats, low-intensity development, and highly vegetated residential areas scaled alongside the availability of these habitats. In contrast, highly developed public and residential landcovers were used less than the amount available, indicating a threshold may exist for urban deer’s tolerance of impervious surfaces and high human activity. This finding is consistent with studies that found deer use declines with increasing housing density (Urbanek & Nielsen 2013). However, larger HRs were associated with increased use of highly developed areas, suggesting development may be more utilized as natural resources become limited. Finally, deer used developed landcovers more at night compared to daytime hours. This diel activity pattern supports global meta-analyses showing increased wildlife nocturnality in response to human activity (Gaynor et al. 2018) and provides evidence of anthropogenic-driven alteration of deer space use.
Our results indicate urban deer have an immediate response to landscape-dependent fragmentation and strongly avoid development at the spatial scale of 100m when establishing their HRs. In our study, deer avoided the urban environment and depended on natural habitats when establishing their HR but were more tolerant of urban features within the HR, using those resources according to their availability or, for some individuals, selecting them. Our findings on the spatial scale of second order selection to human impact may differ from other work that observed second order selection over a larger distance (Nagy-Reiset al. 2019) because SI’s urban landscape presents extreme spatial heterogeneity over short distances (Band et al. 2005), forcing deer to respond to the surrounding environment more imminently than in more natural environments.
We identified block level characteristics important for deer resource use that were associated with tick presence – suggesting residential attributes may increase or decrease the likelihood of tick introduction and survival in ecotones that directly interface with humans. This finding provides evidence to LIF influencing deer’s perception and use of the landscape as observed through their movement. Although our models showed deer overall preferred forested habitat, there was high variation in use of non-forested landcover types and stronger avoidance as development intensity of non-forested habitats increased. While residential block-1 was selected for by few individuals, 30% of models using fine thematic landcover resulted in a neutral response, indicating that some deer may not use residential landcover more or less than expected by chance and that there is not strong aversion of this habitat. In comparison, over 90% of models showed deer select against block-2 and only 3% of models resulted in a neutral response towards block-2. This contrast between the two residential landcover types indicates that deer prioritize more accessible concentrated resources in block-1.
Critically, our findings provide further evidence to support the need for a landscape lens of tick-borne disease (Diuk-Wasser et al.2021). We observed individual movement responses that can directly impact the risk landscape for urban tick-borne disease. Deer that maintained smaller HRs occupied more natural habitats where they may amplify vectors if habitat is suitable for I. scapularis survival (e.g. deciduous forest). The diversity and percentage of more developed landcover types within HRs increased with HR size. Individuals with larger HRs may functionally connect selected habitat types resulting in conduits of movement. The juxtaposition of these patterns of deer space use may jointly contribute to the amplification and dispersal of ticks, two components at the core of increasing tick-borne disease incidence and spread. As observed in models examining the role of landscape connectivity for deer on tick-borne disease risk (VanAcker et al.2019; Tardy et al. 2021), higher functional connectivity for deer can enhance the spread of ticks between isolated habitat patches. Home ranges of male (30-1049 ha; average: 170 ha) and female (24-79 ha; average: 50 ha) deer far exceed the spatial extent of most forest patches sampled in studies that laid the foundation for the dilution effect theory (0.3 to 19 ha) (Allan et al. 2003; LoGiudiceet al. 2008), indicating that patches where nymphal tick density and infection prevalence were estimated and treated independent from one another were likely functionally connected through deer (and potentially other host) movement. Thus, we recommend using the scale of the animal’s space use to examine the spatial unit of influence that wildlife hosts have on tick-borne disease dynamics (Bolzoni et al. 2012). This study addresses this by leveraging tools and analytical approaches from movement and disease ecology to reconcile the hierarchical structure of resource selection with variation in spatial behaviors exhibited by individual animals, rarely attempted before in an urban setting where the outcome of habitat selection impacts zoonotic hazard. With increased attention on translating movement mechanisms to spatial epidemiological modeling (Manlove et al. 2022), we hope this work provides a foundation to formalize integrating movement and epidemiological datasets.
The individual based hierarchical approach employed in this study increased our ability to identify movement behaviors that would have otherwise been missed with a single-scale mean-population approach. Examining the response of deer to development across spatial scales provided insight into how urban deer differ from those in more natural landscapes in their response to human activity during second-order selection. By examining space use in a hierarchical manner, we gained a nuanced understanding of how deer both avoid and exploit anthropogenic development and resources in human-dominated environments, effectively shedding light on how ecological relationships emerge at the human-wildlife interface altering the state of zoonotic hazards. The individual-based modeling framework allowed us to see consistency in movement behaviors across individuals (ie. patterns across sexes) and important movement anomalies (ie. high variation in HR size and use of high intensity development). Finally, translating deer’s observed movement behaviors to an area with unobserved space-use through simulation revealed how resource selection can determine an animal’s use of the human interface, modulating transmission risk. We observed how simulations based on deer that selected highly forested, connected residential blocks resulted in high dispersal probability into the urban matrix than the simulation based on the individual which showed neutral selection to non-forested landcovers. Simulating future space use from individual movement models advances our understanding of how host-environment interactions through movement connects to the spatial spread or concentration of vectors and pathogens across landscapes and at human interfaces and improves the use of static risk-maps to display infectious disease risk.