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Kim M. Pepin

Publications and source records attributed to Kim M. Pepin.

11 recordsLinked to original sources

Viral outbreak dynamics and evolution in wildlife at the interface with humans

In this study, we used a multi-faceted approach to understand patterns of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) transmission and persistence in a wild white-tailed deer ( Odocoileus virginianus ) population. Serology data indicated transmission of SARS-CoV-2 and persistence during the seven-month sampling period. Traditional disease modelling based on deer-to-deer transmission indicated relatively low prevalence with an R 0 of 1.9 and recovery period of 7 days; however, individual-based modelling informed by GPS tracked-movement data captured a potential transmission event. Phylogenetic analyses revealed a recurring pattern of divergent groups of deer-derived sequences with human-derived sequences falling close to each deer-derived cluster. Further, human-derived sequences were frequently sampled months prior to the deer-derived sequences, indicating repeated human to deer spillover. Using multiple types of data as well as both fine and broad scale analyses, we have characterized a pattern of localized outbreaks of SARS-CoV-2 within white-tailed deer populations that are likely recurring due to frequent spillover events. Our results suggest that while deer-to-deer transmission occurs over small spatiotemporal scales, SARS-CoV-2 persistence over longer periods and across larger regions is likely driven by repeated spillover from human populations.

Pennsylvania

Expanding national-scale wildlife disease surveillance systems with research networks

Efficient learning about disease dynamics in free-ranging wildlife systems can benefit from active surveillance that is standardized across different ecological contexts. For example, active surveillance that targets specific individuals and populations with standardized sampling across ecological contexts (landscape-scale targeted surveillance) is important for developing a mechanistic understanding of disease emergence, which is the foundation for improving risk assessment of zoonotic or wildlife-livestock disease outbreaks and predicting hotspots of disease emergence. However, landscape-scale targeted surveillance systems are rare and challenging to implement. Increasing experience and infrastructure for landscape-scale targeted surveillance will improve readiness for rapid deployment of this type of surveillance in response to new disease emergence events. Here, we describe our experience developing and rapidly deploying a landscape-scale targeted surveillance system for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in two free-ranging deer species across their ranges in the United States. Our surveillance system was designed to collect data across individual, population, and landscape scales for future analyses aimed at understanding mechanisms and risk factors of SARS-CoV-2 transmission, evolution, and persistence. Our approach leveraged partnerships between state and federal public service sectors and academic researchers in a landscape-scale targeted surveillance research network. Methods describe our approach to developing the surveillance network and sampling design. Results report challenges with implementing our intended sampling design, specifically how the design was adapted as different challenges arose and summarize the sampling design that has been implemented thus far. In the discussion, we describe strategies that were important for the successful deployment of landscape-scale targeted surveillance, development and operation of the research network, construction of similar networks in the future, and analytical approaches for the data based on the sampling design.

Ecology and Evolution

Evaluation of SARS-CoV-2 antibody detection methods for wild Cervidae

Wildlife surveillance programs often use serological data to monitor exposure to pathogens. Diagnostic sensitivity and specificity of a serological assay quantify the true positive and negative rates of the diagnostic assay, respectively. However, an assay’s accuracy can be affected by wild animals’ pathogen exposure history and quality of the sample collected, requiring separate estimates of an assay’s detection ability for wild-sampled animals where an animal’s true disease status is unknown (referred to hereafter as sampling sensitivity and specificity). We assessed the sampling sensitivity and specificity of a Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) surrogate virus neutralization test (sVNT) and conventional virus neutralization tests (cVNT) to detect antibodies for ancestral and Omicron B.1.1.529 variants of SARS-CoV-2 in wild white-tailed deer ( Odocoileus virginianus ) and mule deer ( Odocoileus hemionus ). We studied the influence of sample collection method using paired blood samples collected in serum separator tubes and on Nobuto strips from the same animal. Mean estimates of sampling sensitivity and specificity ranged from 0.21–0.95 and 0.94–1.00, respectively, varying by sample collection method, host species, and SARS-CoV-2 variant targeted by the assay. Broadly, sampling sensitivity was estimated to be higher for 1) sera collected in tubes, 2) detecting pre-Omicron SARS-CoV-2 variants, and 3) sVNT relative to cVNT assays. Sampling specificity tended to be high for all tests. We augmented our study with SARS-CoV-2 spike protein sequences derived from sampling locations and times coincident with white-tailed deer captures, finding common amino acid mutations relative to the sVNT Omicron antigen variant. The mutations may indicate that the SARS-CoV-2 variants circulating in cervids from 2021 through 2024 may be better adapted to cervid hosts and more closely related to variants that circulated in humans prior to Omicron variants. We conclude our study with an inter-test comparison of sVNT results, revealing that 40 % inhibition is an optimal threshold for test positivity when testing deer sera for responses to Omicron variant B.1.1.529, compared to the 30 % inhibition recommended for ancestral variants.

Colorado, Illinois, Minnesota, New York, Pennsylva

Optimizing management of invasions in an uncertain world using dynamic spatial models

Dispersal drives invasion dynamics of nonnative species and pathogens. Applying knowledge of dispersal to optimize the management of invasions can mean the difference between a failed and a successful control program and dramatically improve the return on investment of control efforts. A common approach to identifying optimal management solutions for invasions is to optimize dynamic spatial models that incorporate dispersal. Optimizing these spatial models can be very challenging because the interaction of time, space, and uncertainty rapidly amplifies the number of dimensions being considered. Addressing such problems requires advances in and the integration of techniques from multiple fields, including ecology, decision analysis, bioeconomics, natural resource management, and optimization. By synthesizing recent advances from these diverse fields, we provide a workflow for applying ecological theory to advance optimal management science and highlight priorities for optimizing the control of invasions. One of the striking gaps we identify is the extremely limited consideration of dispersal uncertainty in optimal management frameworks, even though dispersal estimates are highly uncertain and greatly influence invasion outcomes. In addition, optimization frameworks rarely consider multiple types of uncertainty (we describe five major types) and their interrelationships. Thus, feedbacks from management or other sources that could magnify uncertainty in dispersal are rarely considered. Incorporating uncertainty is crucial for improving transparency in decision risks and identifying optimal management strategies. We discuss gaps and solutions to the challenges of optimization using dynamic spatial models to increase the practical application of these important tools and improve the consistency and robustness of management recommendations for invasions.

Ecological Applications

Strategic testing approaches for targeted disease monitoring can be used to inform pandemic decision-making

More than 1.6 million Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) tests were administered daily in the United States at the peak of the epidemic, with a significant focus on individual treatment. Here, we show that objective-driven, strategic sampling designs and analyses can maximize information gain at the population level, which is necessary to increase situational awareness and predict, prepare for, and respond to a pandemic, while also continuing to inform individual treatment. By focusing on specific objectives such as individual treatment or disease prediction and control (e.g., via the collection of population-level statistics to inform lockdown measures or vaccine rollout) and drawing from the literature on capture–recapture methods to deal with nonrandom sampling and testing errors, we illustrate how public health objectives can be achieved even with limited test availability when testing programs are designed a priori to meet those objectives.

PLoS Biology

Linking mosquito surveillance to dengue fever through Bayesian mechanistic modeling

Our ability to effectively prevent the transmission of the dengue virus through targeted control of its vector, Aedes aegypti , depends critically on our understanding of the link between mosquito abundance and human disease risk. Mosquito and clinical surveillance data are widely collected, but linking them requires a modeling framework that accounts for the complex non-linear mechanisms involved in transmission. Most critical are the bottleneck in transmission imposed by mosquito lifespan relative to the virus’ extrinsic incubation period, and the dynamics of human immunity. We developed a differential equation model of dengue transmission and embedded it in a Bayesian hierarchical framework that allowed us to estimate latent time series of mosquito demographic rates from mosquito trap counts and dengue case reports from the city of Vitória, Brazil. We used the fitted model to explore how the timing of a pulse of adult mosquito control influences its effect on the human disease burden in the following year. We found that control was generally more effective when implemented in periods of relatively low mosquito mortality (when mosquito abundance was also generally low). In particular, control implemented in early September (week 34 of the year) produced the largest reduction in predicted human case reports over the following year. This highlights the potential long-term utility of broad, off-peak-season mosquito control in addition to existing, locally targeted within-season efforts. Further, uncertainty in the effectiveness of control interventions was driven largely by posterior variation in the average mosquito mortality rate (closely tied to total mosquito abundance) with lower mosquito mortality generating systems more vulnerable to control. Broadly, these correlations suggest that mosquito control is most effective in situations in which transmission is already limited by mosquito abundance.

Espírito Santo

Optimal spatial prioritization of control resources for elimination of invasive species under demographic uncertainty

Populations of invasive species often spread heterogeneously across a landscape, consisting of local populations that cluster in space but are connected by dispersal. A fundamental dilemma for invasive species control is how to optimally allocate limited fiscal resources across local populations. Theoretical work based on perfect knowledge of demographic connectivity suggests that targeting local populations from which migrants originate (sources) can be optimal. However, demographic processes such as abundance and dispersal can be highly uncertain, and the relationship between local population density and damage costs (damage function) is rarely known. We used a metapopulation model to understand how budget and uncertainty in abundance, connectivity, and the damage function, together impact return on investment (ROI) for optimal control strategies. Budget, observational uncertainty, and the damage function had strong effects on the optimal resource allocation strategy. Uncertainty in dispersal probability was the least important determinant of ROI. The damage function determined which resource prioritization strategy was optimal when connectivity was symmetric but not when it was asymmetric. When connectivity was asymmetric, prioritizing source populations had a higher ROI than allocating effort equally across local populations, regardless of the damage function, but uncertainty in connectivity structure and abundance reduced ROI of the optimal prioritization strategy by 57% on average depending on the control budget. With low budgets (monthly removal rate of 6.7% of population), there was little advantage to prioritizing resources, especially when connectivity was high or symmetric, and observational uncertainty had only minor effects on ROI. Allotting funding for improved monitoring appeared to be most important when budgets were moderate (monthly removal of 13–20% of the population). Our result showed that multiple sources of observational uncertainty should be considered concurrently for optimizing ROI. Accurate estimates of connectivity direction and abundance were more important than accurate estimates of dispersal rates. Developing cost-effective surveillance methods to reduce observational uncertainties, and quantitative frameworks for determining how resources should be spatially apportioned to multiple monitoring and control activities are important and challenging future directions for optimizing ROI for invasive species control programs.

Ecological Applications

Predicting functional responses in agro-ecosystems from animal movement data to improve management of invasive pests

Functional responses describe how changing resource availability affects consumer resource use, thus providing a mechanistic approach to prediction of the invasibility and potential damage of invasive alien species (IAS). However, functional responses can be context dependent, varying with resource characteristics and availability, consumer attributes, and environmental variables. Identifying context dependencies can allow invasion and damage risk to be predicted across different ecoregions. Understanding how ecological factors shape the functional response in agro‐ecosystems can improve predictions of hotspots of highest impact and inform strategies to mitigate damage across locations with varying crop types and availability. We linked heterogeneous movement data across different agro‐ecosystems to predict ecologically driven variability in the functional responses. We applied our approach to wild pigs ( Sus scrofa ), one of the most successful and detrimental IAS worldwide where agricultural resource depredation is an important driver of spread and establishment. We used continental‐scale movement data within agro‐ecosystems to quantify the functional response of agricultural resources relative to availability of crops and natural forage. We hypothesized that wild pigs would selectively use crops more often when natural forage resources were low. We also examined how individual attributes such as sex, crop type, and resource stimulus such as distance to crops altered the magnitude of the functional response. There was a strong agricultural functional response where crop use was an accelerating function of crop availability at low density (Type III) and was highly context dependent. As hypothesized, there was a reduced response of crop use with increasing crop availability when non‐agricultural resources were more available, emphasizing that crop damage levels are likely to be highly heterogeneous depending on surrounding natural resources and temporal availability of crops. We found significant effects of crop type and sex, with males spending 20% more time and visiting crops 58% more often than females, and both sexes showing different functional responses depending on crop type. Our application demonstrates how commonly collected animal movement data can be used to understand context dependencies in resource use to improve our understanding of pest foraging behavior, with implications for prioritizing spatiotemporal hotspots of potential economic loss in agro‐ecosystems.

California. Florida, Georgia, Louisiana, Missouri,

Confronting models with data: The challenges of estimating disease spillover

For pathogens known to transmit across host species, strategic investment in disease control requires knowledge about where and when spillover transmission is likely. One approach to estimating spillover is to directly correlate observed spillover events with covariates. An alternative is to mechanistically combine information on host density, distribution, and pathogen prevalence to predict where and when spillover events are expected to occur. We use several case studies at the wildlife-livestock disease interface to highlight the challenges, and potential solutions, to estimating spatio-temporal variation in spillover risk. Datasets on multiple host species often do not align in space, time or resolution, and may have no estimates of observation error. Linking these datasets requires they be related to a common spatial and temporal resolution and appropriately propagating errors in predictions can be difficult. Hierarchical models are one potential solution, but for fine-resolution predictions at broad spatial scales many models become computationally challenging. Despite these limitations, the confrontation of mechanistic predictions with observed events is an important avenue for developing a better understanding of pathogen spillover. Systems where data have been collected at all levels in the spillover process are rare, or non-existent, and require investment and sustained effort across disciplines.

Philosophical Transactions of the Royal Society B:

Inferring infection hazard in wildlife populations by linking data across individual and population scales

Our ability to infer unobservable disease-dynamic processes such as force of infection (infection hazard for susceptible hosts) has transformed our understanding of disease transmission mechanisms and capacity to predict disease dynamics. Conventional methods for inferring FOI estimate a time-averaged value and are based on population-level processes. Because many pathogens exhibit epidemic cycling and FOI is the result of processes acting across the scales of individuals and populations, a flexible framework that extends to epidemic dynamics and links within-host processes to FOI is needed. Specifically, within-host antibody kinetics in wildlife hosts can be short-lived and produce patterns that are repeatable across individuals, suggesting individual-level antibody concentrations could be used to infer time since infection and hence FOI. Using simulations and case studies (influenza A in lesser snow geese and Yersinia pestis in coyotes), we argue that with careful experimental and surveillance design, the population-level FOI signal can be recovered from individual-level antibody kinetics, despite substantial individual-level variation. In addition to improving inference, the cross-scale quantitative antibody approach we describe can reveal insights into drivers of individual-based variation in disease response, and the role of poorly understood processes such as secondary infections, in population-level dynamics of disease.

Ecology Letters

Inferring invasive species abundance using removal data from management actions

Evaluation of the progress of management programs for invasive species is crucial for demonstrating impacts to stakeholders and strategic planning of resource allocation. Estimates of abundance before and after management activities can serve as a useful metric of population management programs. However, many methods of estimating population size are too labor intensive and costly to implement, posing restrictive levels of burden on operational programs. Removal models are a reliable method for estimating abundance before and after management using data from the removal activities exclusively, thus requiring no work in addition to management. We developed a Bayesian hierarchical model to estimate abundance from removal data accounting for varying levels of effort, and used simulations to assess the conditions under which reliable population estimates are obtained. We applied this model to estimate site-specific abundance of an invasive species, feral swine ( Sus scrofa ), using removal data from aerial gunning in 59 site/time-frame combinations (480–19,600 acres) throughout Oklahoma and Texas, USA. Simulations showed that abundance estimates were generally accurate when effective removal rates (removal rate accounting for total effort) were above 0.40. However, when abundances were small (<50) the effective removal rate needed to accurately estimates abundances was considerably higher (0.70). Based on our post-validation method, 78% of our site/time frame estimates were accurate. To use this modeling framework it is important to have multiple removals (more than three) within a time frame during which demographic changes are minimized (i.e., a closed population; ≤3 months for feral swine). Our results show that the probability of accurately estimating abundance from this model improves with increased sampling effort (8+ flight hours across the 3-month window is best) and increased removal rate. Based on the inverse relationship between inaccurate abundances and inaccurate removal rates, we suggest auxiliary information that could be collected and included in the model as covariates (e.g., habitat effects, differences between pilots) to improve accuracy of removal rates and hence abundance estimates.

Ecological Applications