cities-as-interfaces-zoonotic-hazard-emergence-development-new-york

Cities As Interfaces of Zoonotic Hazard Emergence: Development of the New York City Tick and Wildlife Urban Surveillance System

Tick-borne hazards in urban landscapes are increasing, yet critical gaps remain in understanding human tick-borne disease risk across urbanization ...

Severe fragmentation is a typical fate of native remnant habitats in cities, and urban wildlife with limited dispersal ability are predicted to lose genetic variation in isolated urban patches. However, little information exists on the characteristics of urban green spaces required to conserve genetic variation. In this study, we examine whether isolation in New York City (NYC) parks results in genetic bottlenecks in white-footed mice (Peromyscus leucopus), and test the hypotheses that park size and time since isolation are associated with genetic variability using nonlinear regression and information-theoretic model selection. White-footed mice have previously been documented to exhibit male-biased dispersal, which may create disparities in genetic variation between males and females in urban parks. We use genotypes of 18 neutral microsatellite data and four different statistical tests to assess this prediction. Given that sex-biased dispersal may create disparities between population genetic patterns inferred from bi- vs. uni-parentally inherited markers, we also sequenced a 324 bp segment of the mitochondrial D-loop for independent inferences of historical demography in urban P. leucopus. We report that isolation in urban parks does not necessarily result in genetic bottlenecks; only three out of 14 populations in NYC parks exhibited a signature of a recent bottleneck at 18 neutral microsatellite loci. Mouse populations in larger urban parks, or parks that have been isolated for shorter periods of time, also do not generally contain greater genetic variation than populations in smaller parks. These results suggest that even small networks of green spaces may be sufficient to maintain the evolutionary potential of native species with certain characteristics. We also found that isolation in urban parks results in weak to nonexistent sex-biased dispersal in a species known to exhibit male-biased dispersal in less fragmented environments. In contrast to nuclear loci, mitochondrial D-loop haplotypes exhibited a mutational pattern of demographic expansion after a recent bottleneck or selective sweep. Estimates of the timing of this expansion suggest that it occurred concurrent with urbanization of NYC over the last few dozens to hundreds of years. Given the general non-neutrality of mtDNA in many systems and evidence of selection on related coding sequences in urban P. leucopus, we argue that the P. leucopus mitochondrial genome experienced recent negative selection against haplotypes not favored in isolated urban parks. In general, rapid adaptive evolution driven by urbanization, global climate change, and other human-caused factors is underappreciated by evolutionary biologists, but many more cases will likely be documented in the near future.

Urban park characteristics, genetic variation, and historical demography of white-footed mouse (Peromyscus leucopus) populations in New York City.

With the accelerating pace of global change, it is imperative that we obtain rapid inventories of the status and distribution of wildlife for ecological inferences and conservation planning. To address this challenge, we launched the SNAPSHOT USA project, a collaborative survey of terrestrial wildlife populations using camera traps across the United States. For our first annual survey, we compiled data across all 50 states during a 14-week period (17 August-24 November of 2019). We sampled wildlife at 1,509 camera trap sites from 110 camera trap arrays covering 12 different ecoregions across four development zones. This effort resulted in 166,036 unique detections of 83 species of mammals and 17 species of birds. All images were processed through the Smithsonian's eMammal camera trap data repository and included an expert review phase to ensure taxonomic accuracy of data, resulting in each picture being reviewed at least twice. The results represent a timely and standardized camera trap survey of the United States. All of the 2019 survey data are made available herein. We are currently repeating surveys in fall 2020, opening up the opportunity to other institutions and cooperators to expand coverage of all the urban-wild gradients and ecophysiographic regions of the country. Future data will be available as the database is updated at eMammal.si.edu/snapshot-usa, as will future data paper submissions. These data will be useful for local and macroecological research including the examination of community assembly, effects of environmental and anthropogenic landscape variables, effects of fragmentation and extinction debt dynamics, as well as species-specific population dynamics and conservation action plans. There are no copyright restrictions; please cite this paper when using the data for publication.

SNAPSHOT USA 2019: a coordinated national camera trap survey of the United States.

Managing wildlife populations in the face of global change requires regular data on the abundance and distribution of wild animals, but acquiring these over appropriate spatial scales in a sustainable way has proven challenging. Here we present the data from Snapshot USA 2020, a second annual national mammal survey of the USA. This project involved 152 scientists setting camera traps in a standardized protocol at 1485 locations across 103 arrays in 43 states for a total of 52,710 trap-nights of survey effort. Most (58) of these arrays were also sampled during the same months (September and October) in 2019, providing a direct comparison of animal populations in 2 years that includes data from both during and before the COVID-19 pandemic. All data were managed by the eMammal system, with all species identifications checked by at least two reviewers. In total, we recorded 117,415 detections of 78 species of wild mammals, 9236 detections of at least 43 species of birds, 15,851 detections of six domestic animals and 23,825 detections of humans or their vehicles. Spatial differences across arrays explained more variation in the relative abundance than temporal variation across years for all 38 species modeled, although there are examples of significant site-level differences among years for many species. Temporal results show how species allocate their time and can be used to study species interactions, including between humans and wildlife. These data provide a snapshot of the mammal community of the USA for 2020 and will be useful for exploring the drivers of spatial and temporal changes in relative abundance and distribution, and the impacts of species interactions on daily activity patterns. There are no copyright restrictions, and please cite this paper when using these data, or a subset of these data, for publication.

SNAPSHOT USA 2020: A second coordinated national camera trap survey of the United States during the COVID-19 pandemic.

Coyotes are ubiquitous on the North American landscape as a result of their recent expansion across the continent. They have been documented in the heart of some of the most urbanized cities, such as Chicago, Los Angeles, and New York City. Here, we explored the genomic composition of 16 coyotes in the New York metropolitan area to investigate genomic demography and admixture for urban-dwelling canids in Queens County, New York. We identified moderate-to-high estimates of relatedness among coyotes living in Queens (r = 0.0-0.5) and adjacent neighborhoods, suggestive of a relatively small population. Although we found low background levels of domestic-dog ancestry across most coyotes in our sample (5%), we identified a male suspected to be a first-generation coyote-dog hybrid with 46% dog ancestry, as well as his two putative backcrossed offspring that carried approximately 25% dog ancestry. The male coyote-dog hybrid and one backcrossed offspring each carried two transposable element insertions that are associated with human-directed hypersociability in dogs and gray wolves. An additional, unrelated coyote with little dog ancestry also carried two of these insertions. These genetic patterns suggest that gene flow from domestic dogs may become an increasingly important consideration as coyotes continue to inhabit metropolitan regions.

Coyotes in New York City Carry Variable Genomic Dog Ancestry and Influence Their Interactions with Humans.

Carnivores are currently colonizing cities where they were previously absent. These urban environments are novel ecosystems characterized by habitat degradation and fragmentation, availability of human food, and different prey assemblages than surrounding areas. Coyotes () established a breeding population in New York City (NYC) over the last few decades, but their ecology within NYC is poorly understood. In this study, we used non-invasive scat sampling and DNA metabarcoding to profile vertebrate, invertebrate, and plant dietary items with the goal to compare the diets of urban coyotes to those inhabiting non-urban areas. We found that both urban and non-urban coyotes consumed a variety of plants and animals as well as human food. Raccoons () were an important food item for coyotes within and outside NYC. In contrast, white-tailed deer () were mainly eaten by coyotes inhabiting non-urban areas. Domestic chicken () was the human food item found in most scats from both urban and non-urban coyotes. Domestic cats () were consumed by urban coyotes but were detected in only a small proportion of the scats (<5%), which differs markedly from high rates of cat depredation in some other cities. In addition, we compared our genetic metabarcoding analysis to a morphological analysis of the same scat samples. We found that the detection similarity between the two methods was low and it varied depending on the type of diet item.

DNA metabarcoding reveals that coyotes in New York City consume wide variety of native prey species and human food.

Skin microbial communities are an essential part of host health and can play a role in mitigating disease. Host and environmental factors can shape and alter these microbial communities and, therefore, we need to understand to what extent these factors influence microbial communities and how this can impact disease dynamics. Microbial communities have been studied in amphibian systems due to skin microbial communities providing some resistance to the amphibian chytrid fungus, . However, we are only starting to understand how host and environmental factors shape these communities for amphibians. In this study, we examined whether amphibian skin bacterial communities differ among host species, host infection status, host developmental stage, and host habitat. We collected skin swabs from tadpoles and adults of three Ranid frog species ( spp.) at the Mianus River Gorge Preserve in Bedford, New York, USA, and used 16S rRNA gene amplicon sequencing to determine bacterial community composition. Our analysis suggests amphibian skin bacterial communities change across host developmental stages, as has been documented previously. Additionally, we found that skin bacterial communities differed among Ranid species, with skin communities on the host species captured in streams or bogs differing from the communities of the species captured on land. Thus, habitat use of different species may drive differences in host-associated microbial communities for closely-related host species.

Skin bacterial community differences among three species of co-occurring Ranid frogs.

Wildlife must adapt to human presence to survive in the Anthropocene, so it is critical to understand species responses to humans in different contexts. We used camera trapping as a lens to view mammal responses to changes in human activity during the COVID-19 pandemic. Across 163 species sampled in 102 projects around the world, changes in the amount and timing of animal activity varied widely. Under higher human activity, mammals were less active in undeveloped areas but unexpectedly more active in developed areas while exhibiting greater nocturnality. Carnivores were most sensitive, showing the strongest decreases in activity and greatest increases in nocturnality. Wildlife managers must consider how habituation and uneven sensitivity across species may cause fundamental differences in human-wildlife interactions along gradients of human influence.

Mammal responses to global changes in human activity vary by trophic group and landscape.

SNAPSHOT USA is a multicontributor, long-term camera trap survey designed to survey mammals across the United States. Participants are recruited through community networks and directly through a website application (https://www.snapshot-usa.org/). The growing Snapshot dataset is useful, for example, for tracking wildlife population responses to land use, land cover, and climate changes across spatial and temporal scales. Here we present the SNAPSHOT USA 2021 dataset, the third national camera trap survey across the US. Data were collected across 109 camera trap arrays and included 1711 camera sites. The total effort equaled 71,519 camera trap nights and resulted in 172,507 sequences of animal observations. Sampling effort varied among camera trap arrays, with a minimum of 126 camera trap nights, a maximum of 3355 nights, a median 546 nights, and a mean 656 ± 431 nights. This third dataset comprises 51 camera trap arrays that were surveyed during 2019, 2020, and 2021, along with 71 camera trap arrays that were surveyed in 2020 and 2021. All raw data and accompanying metadata are stored on Wildlife Insights (https://www.wildlifeinsights.org/), and are publicly available upon acceptance of the data papers. SNAPSHOT USA aims to sample multiple ecoregions in the United States with adequate representation of each ecoregion according to its relative size. Currently, the relative density of camera trap arrays varies by an order of magnitude for the various ecoregions (0.22-5.9 arrays per 100,000 km), emphasizing the need to increase sampling effort by further recruiting and retaining contributors. There are no copyright restrictions on these data. We request that authors cite this paper when using these data, or a subset of these data, for publication. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government.

SNAPSHOT USA 2021: A third coordinated national camera trap survey of the United States.

As cities seek to provide more habitat for wildlife, there may be unintended consequences of increasing tick-borne disease hazards. In the United States, the Northeast is both highly urban and a hotspot for blacklegged ticks () and tick-borne disease emergence. Though tick-borne disease was once considered a suburban and rural problem, tick-borne hazards in urban landscapes are increasing.

Functional connectivity for white-tailed deer drives the distribution of tick-borne pathogens in a highly urbanized setting.

Carnivores must navigate the complexities of human modifications to their environment. Natural resources and biodiversity decline in urban areas, while people in rural areas often pose greater direct risk through actions such as hunting. To evaluate if carnivore populations adapt their behavior to local risks in rural and urban environments, we compared behavioral responses to novel objects in coyotes (Canis latrans). We placed an attractant at arrays of 30 camera-trap stations at 16 pairs of urban and rural field sites across the USA, with a novel object placed at half of the stations. Coyotes exhibited more cautious behavior and remained farther from the attractant at all sites with the novel object; however, urban coyotes got closer to the attractant than rural coyotes. There were few behavioral differences between urban and rural coyotes and none between eastern and western coyotes. Coyotes across the USA exhibit neophobic behavior but urban coyotes, especially western coyotes, are willing to take more risk (i.e., be closer to the attractant). The consistency in most metrics of coyote behavior suggest that solutions developed in one area could be universally useful. This study also demonstrates the effectiveness of a large, collaborative approach to studying broad-scale patterns in behavioral traits.

Article	Year
Urban park characteristics, genetic variation, and historical demography of white-footed mouse (Peromyscus leucopus) populations in New York City. PeerJ\| PubMed ID: 24688884	2014
SNAPSHOT USA 2019: a coordinated national camera trap survey of the United States. Ecology\| PubMed ID: 33793977	2021
SNAPSHOT USA 2020: A second coordinated national camera trap survey of the United States during the COVID-19 pandemic. Ecology\| PubMed ID: 35661139	2022
Coyotes in New York City Carry Variable Genomic Dog Ancestry and Influence Their Interactions with Humans. Genes\| PubMed ID: 36140828	2022
DNA metabarcoding reveals that coyotes in New York City consume wide variety of native prey species and human food. PeerJ\| PubMed ID: 36164598	2022
Skin bacterial community differences among three species of co-occurring Ranid frogs. PeerJ\| PubMed ID: 37465150	2023
Mammal responses to global changes in human activity vary by trophic group and landscape. Nature ecology & evolution\| PubMed ID: 38499871	2024
SNAPSHOT USA 2021: A third coordinated national camera trap survey of the United States. Ecology\| PubMed ID: 38693703	2024
Functional connectivity for white-tailed deer drives the distribution of tick-borne pathogens in a highly urbanized setting. Landscape ecology\| PubMed ID: 40270782	2025
Large-scale experimental assessment of coyote behavior across urban and rural landscapes. Scientific reports\| PubMed ID: 41407910	2025

Christopher Nagy

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