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Kezia R. Manlove

Publications and source records attributed to Kezia R. Manlove.

17 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

The influence of human presence and footprint on animal space use in US national parks

Given the importance of protected areas for biodiversity, the growth of visitation to many areas has raised concerns about the effects of humans on wildlife. In 2020, the COVID-19 pandemic led to temporary closure of national parks in the United States, offering a pseudonatural experiment to tease apart the effects of permanent infrastructure and transient human presence on animals. We compiled GPS tracking data from 229 individuals of 10 mammal species in 14 parks and used third-order hierarchical resource selection functions to evaluate the influence of the human footprint on animal space use in 2019 and 2020. Averaged across all parks and species, animals avoided the human footprint, whether the park was open or closed. However, although animals in remote areas showed consistent avoidance, on average those in more developed areas switched from avoidance to selection when protected areas were closed. Findings varied across species: some responded consistently negatively to the footprint (wolves, mountain goats), some positively (mule deer, red fox) and others had a strong exposure-mediated response (elk, mountain lion). Furthermore, some species responded more strongly to the park closure (black bear, moose). This study advances our understanding of complex interactions between recreation and wildlife in protected areas.

western United States

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

Evaluating mountain lion diet before and after a removal of feral horses in a semiarid environment

Non-native species can affect ecosystems by influencing native predator-prey dynamics. Therefore, management interventions designed to remove non-natives may inadvertently lead to increased predation on native species. Feral horses are widely distributed throughout the arid parts of western North America. A growing body of research indicates that horses can be an important prey species to mountain lions in ecosystems where they overlap. In December 2020, the Bureau of Land Management removed 455 horses from the Delamar Mountains, Nevada, USA. We leveraged this management intervention to implement a before–after–control–impact study to test hypotheses about predation on horses and native ungulates. We predicted (1) that horses would comprise an important part of the diet in this mixed-prey community, (2) following removal, the proportion of horses in the diet would decrease and native ungulates would increase, and (3) mountain lion home ranges overlapping the treatment areas would increase in response to decreased prey availability. From 2018 to 2022, we investigated 1360 clusters from 29 GPS-collared lions and identified 1056 prey items. To model the probability of a predation event (a kill), we fit a mixed-effects logistic regression model for ungulate prey as a function of lion sex, treatment area (in/out), and treatment period (pre-/post-removal). We used a log-linear regression model to evaluate changes in home range size. The most common prey were mule deer (55%), feral horses (32%), and coyotes (4%). Twenty-two of 29 lions consumed horses, although the rate of horse consumption was highly variable across individuals. Horses of both sexes and all age classes were predated. In contrast to predictions, our models detected no effect of removals on diet composition (β interaction = 0.30 ± 1.1), nor did the removal influence home range size (β interaction = 0.02 ± 0.02). Despite a 46% reduction in horse abundance, we found no evidence for prey-switching following the horse removal treatment. Removal magnitude, rapid horse immigration, and/or behavioral specialization of individual mountain lions may help explain these results. Our findings have important implications for mountain lion and feral horse management in arid environments characterized by high prey diversity, but low prey abundance.

Nevada

Defining an epidemiological landscape that connects movement ecology to pathogen transmission and pace-of-life

Pathogen transmission depends on host density, mobility and contact. These components emerge from host and pathogen movements that themselves arise through interactions with the surrounding environment. The environment, the emergent host and pathogen movements, and the subsequent patterns of density, mobility and contact form an ‘epidemiological landscape’ connecting the environment to specific locations where transmissions occur. Conventionally, the epidemiological landscape has been described in terms of the geographical coordinates where hosts or pathogens are located. We advocate for an alternative approach that relates those locations to attributes of the local environment. Environmental descriptions can strengthen epidemiological forecasts by allowing for predictions even when local geographical data are not available. Environmental predictions are more accessible than ever thanks to new tools from movement ecology, and we introduce a ‘movement-pathogen pace of life’ heuristic to help identify aspects of movement that have the most influence on spatial epidemiology. By linking pathogen transmission directly to the environment, the epidemiological landscape offers an efficient path for using environmental information to inform models describing when and where transmission will occur.

Ecology Letters

Using transcriptomics to predict and visualize disease status in bighorn sheep (Ovis canadensis)

Increasing risk of pathogen spillover coupled with overall declines in wildlife population abundance in the Anthropocene make infectious disease a relevant concern for species conservation worldwide. While emerging molecular tools could improve our diagnostic capabilities and give insight into mechanisms underlying wildlife disease risk, they have rarely been applied in practice. Here, employing a previously reported gene transcription panel of common immune markers to track physiological changes, we present a detailed analysis over the course of both acute and chronic infection in one wildlife species where disease plays a critical role in conservation, bighorn sheep ( Ovis canadensis ). Differential gene transcription patterns distinguished between infection statuses over the course of acute infection and differential correlation (DC) analyses identified clear changes in gene co-transcription patterns over the early stages of infection, with transcription of four genes—TGFb, AHR, IL1b and MX1—continuing to increase even as transcription of other immune-associated genes waned. In a separate analysis, we considered the capacity of the same gene transcription panel to aid in differentiating between chronically infected animals and animals in other disease states outside of acute disease events (an immediate priority for wildlife management in this system). We found that this transcription panel was capable of accurately identifying chronically infected animals in the test dataset, though additional data will be required to determine how far this ability extends. Taken together, our results showcase the successful proof of concept and breadth of potential utilities that gene transcription might provide to wildlife disease management, from direct insight into mechanisms associated with differential disease response to improved diagnostic capacity in the field.

Conservation Physiology

Disease and secondary sexual traits: Effects of pneumonia on horn size of bighorn sheep

Secondary sexual traits (e.g., horns and antlers) have ecological and evolutionary importance and are of management interest for game species. Yet, how these traits respond to emerging threats like infectious disease remains underexplored. Infectious pneumonia threatens bighorn sheep ( Ovis canadensis ) populations across North America and we hypothesized it may also reduce horn growth in male sheep. We assess the effect of pneumonia on horn size in male bighorn sheep using 12 herd datasets from across the western United States that had horn growth and disease data. Disease resulted in 12–35% reduction in increment (yearly) length and 3–13% reduction in total horn length in exposed individuals. The disease effect was prolonged when pathogens continued to circulate in sheep populations. Further, disease likely delays the age at which horns reach ¾-curl and prevents achievement of full-curl. This is further evidenced with 6 of the 12 herds experiencing an increase in average age at harvest following die-off events.

Colorado, Idaho, Montana, Utah, Washington, Wyomin

Natural history of a bighorn sheep pneumonia epizootic: Source of infection, course of disease, and pathogen clearance

A respiratory disease epizootic at the National Bison Range (NBR) in Montana in 2016–2017 caused an 85% decline in the bighorn sheep population, documented by observations of its unmarked but individually identifiable members, the subjects of an ongoing long-term study. The index case was likely one of a small group of young bighorn sheep on a short-term exploratory foray in early summer of 2016. Disease subsequently spread through the population, with peak mortality in September and October and continuing signs of respiratory disease and sporadic mortality of all age classes through early July 2017. Body condition scores and clinical signs suggested that the disease affected ewe groups before rams, although by the end of the epizootic, ram mortality (90% of 71) exceeded ewe mortality (79% of 84). Microbiological sampling 10 years to 3 months prior to the epizootic had documented no evidence of infection or exposure to Mycoplasma ovipneumoniae at NBR, but during the epizootic, a single genetic strain of M. ovipneumoniae was detected in affected animals. Retrospective screening of domestic sheep flocks near the NBR identified the same genetic strain in one flock, presumptively the source of the epizootic infection. Evidence of fatal lamb pneumonia was observed during the first two lambing seasons following the epizootic but was absent during the third season following the death of the last identified M. ovipneumoniae carrier ewe. Monitoring of life-history traits prior to the epizootic provided no evidence that environmentally and/or demographically induced nutritional or other stress contributed to the epizootic. Furthermore, the epizootic occurred despite proactive management actions undertaken to reduce risk of disease and increase resilience in this population. This closely observed bighorn sheep epizootic uniquely illustrates the natural history of the disease including the (presumptive) source of spillover, course, severity, and eventual pathogen clearance.

Montana

Ecological interventions to prevent and manage zoonotic pathogen spillover

Spillover of a pathogen from a wildlife reservoir into a human or livestock host requires the pathogen to overcome a hierarchical series of barriers. Interventions aimed at one or more of these barriers may be able to prevent the occurrence of spillover. Here, we demonstrate how interventions that target the ecological context in which spillover occurs (i.e. ecological interventions) can complement conventional approaches like vaccination, treatment, disinfection and chemical control. Accelerating spillover owing to environmental change requires effective, affordable, durable and scalable solutions that fully harness the complex processes involved in cross-species pathogen spillover.

Philosophical Transactions of the Royal Society B:

Risk factors and productivity losses associated with Mycoplasma ovipneumoniae infection in United States domestic sheep operations

Association of Mycoplasma ovipneumoniae with pneumonia in domestic small ruminants has been described in Europe, Asia, and New Zealand but has received less attention in the United States. In 2011, the US Department of Agriculture’s National Animal Health Monitoring Survey detected M. ovipneumoniae shedding in 88% of 453 domestic sheep operations tested in 22 states that accounted for 85.5% of US ewe inventory in 2001. We evaluated factors associated with M. ovipneumoniae infection presence and prevalence, and we compared health, lamb production, and ewe losses in in-fected and uninfected operations. M. ovipneumoniae detection was more common in larger opera-tions than in smaller operations. Both likelihood of detection (at the operation level) and within-operation prevalence were higher in operations with more open management practices than in oper-ations with more closed management practices. M. ovipneumoniae-positive operations showed sig-nificantly lower lambing rates and lower rates of lamb survival to weaning after accounting for dif-ferences in operation size and management practice. While its effect on any single rate was not par-ticularly large, in aggregate we estimated that M. ovipneumoniae presence was associated with an approximately 4.3% reduction in annual lamb production.

Preventive Veterinary Medicine

The ecology of movement and behaviour: a saturated tripartite network for describing animal contacts

Ecologists regularly use animal contact networks to describe interactions underlying pathogen transmission, gene flow, and information transfer. However, empirical descriptions of contact often overlook some features of individual movement, and decisions about what kind of network to use in a particular setting are commonly ad hoc . Here, we relate individual movement trajectories to contact networks through a tripartite network model of individual, space, and time nodes. Most networks used in animal contact studies (e.g. individual association networks, home range overlap networks, and spatial networks) are simplifications of this tripartite model. The tripartite structure can incorporate a broad suite of alternative ecological metrics like home range sizes and patch occupancy patterns into inferences about contact network metrics such as modularity and degree distribution. We demonstrate the model's utility with two simulation studies using alternative forms of ecological data to constrain the tripartite network's structure and inform expectations about the harder-to-measure metrics related to contact.

Proceedings of the Royal Society B: Biological Sci

Pneumonia in bighorn sheep: Risk and resilience

Infectious disease was an important driver of historic declines and extirpations of bighorn sheep (Ovis canadensis) in North America and continues to impede population restoration and management. Domestic sheep have long been linked to pneumonia outbreaks in bighorn sheep and this association has now been confirmed in 13 captive commingling experiments. However, ecological and etiological complexities still hinder our understanding and control of the disease. We provide an overview of the current state of knowledge about the biology and management of respiratory disease in bighorn sheep and propose strategies for moving forward. Epizootic pneumonia in bighorn sheep is polymicrobial. Mycoplasma ovipneumoniae, a bacterium host-specific to Caprinae and commonly carried by healthy domestic sheep and goats appears to be a necessary primary agent. All-age epizootics following introduction of M. ovipneumoniae along with other pathogens into bighorn sheep populations are usually severe (median mortality 47%) but fatality rates vary widely, from 15 – 100%. Disease severity may be influenced by the strain of M. ovipneumoniae, by secondary bacterial and viral pathogens, and by factors affecting transmission and host immunity. Once introduced, M. ovipneumoniae can persist in bighorn sheep populations for decades. Carrier dams transmit the pathogen to their susceptible lambs, triggering fatal pneumonia outbreaks in nursery groups, which limits recruitment and slows or prevents population recovery. The result is that demographic costs of pathogen persistence often outweigh the impacts of the initial invasion and die-off. There is currently no effective vaccine or antibiotic for domestic or wild sheep and to date, no management actions have been successful in reducing morbidity, mortality, or disease spread once pathogen invasion has occurred. Molecular-based strain typing suggests that spillover of M. ovipneumoniae into bighorn sheep populations from domestic small ruminants is ongoing, and that consequences of pathogen invasion are amplified by movements of infected bighorn sheep. Therefore, current disease management strategies focus on reducing risk of spillover from reservoir populations of domestic small ruminants and on limiting transmission among bighorn sheep. A broad array of approaches has been tried and more are needed to prevent pathogen introduction, induce disease fadeout in persistently infected populations, and promote population resilience across the diverse landscapes bighorn sheep inhabit. A comprehensive examination of disease dynamics across populations could help elucidate how disease fades out naturally and if population resilience can be increased in the face of infection. Cross-jurisdictional adaptive management experiments and transdisciplinary collaboration, including partnerships with members of the domestic sheep and goat community, are needed to facilitate innovation and speed progress towards sustainable solutions for managing pneumonia to protect and restore bighorn sheep populations.

California, Idaho, Nevada, Oregon, Utah, Washingto

Contact and contagion: Probability of transmission given contact varies with demographic state in bighorn sheep

Understanding both contact and probability of transmission given contact are key to managing wildlife disease. However, wildlife disease research tends to focus on contact heterogeneity, in part because the probability of transmission given contact is notoriously difficult to measure. Here, we present a first step towards empirically investigating the probability of transmission given contact in free-ranging wildlife. We used measured contact networks to test whether bighorn sheep demographic states vary systematically in infectiousness or susceptibility to Mycoplasma ovipneumoniae , an agent responsible for bighorn sheep pneumonia. We built covariates using contact network metrics, demographic information and infection status, and used logistic regression to relate those covariates to lamb survival. The covariate set contained degree, a classic network metric describing node centrality, but also included covariates breaking the network metrics into subsets that differentiated between contacts with yearlings, ewes with lambs, and ewes without lambs, and animals with and without active infections. Yearlings, ewes with lambs, and ewes without lambs showed similar group membership patterns, but direct interactions involving touch occurred at a rate two orders of magnitude higher between lambs and reproductive ewes than between any classes of adults or yearlings, and one order of magnitude higher than direct interactions between multiple lambs. Although yearlings and non-reproductive bighorn ewes regularly carried M. ovipneumoniae , our models suggest that a contact with an infected reproductive ewe had approximately five times the odds of producing a lamb mortality event of an identical contact with an infected dry ewe or yearling. Consequently, management actions targeting infected animals might lead to unnecessary removal of young animals that carry pathogens but rarely transmit. This analysis demonstrates a simple logistic regression approach for testing a priori hypotheses about variation in the odds of transmission given contact for free-ranging hosts, and may be broadly applicable for investigations in wildlife disease ecology.

Journal of Animal Ecology

Costs and benefits of group living with disease: a case study of pneumonia in bighorn lambs ( Ovis canadensis )

Group living facilitates pathogen transmission among social hosts, yet temporally stable host social organizations can actually limit transmission of some pathogens. When there are few between-subpopulation contacts for the duration of a disease event, transmission becomes localized to subpopulations. The number of per capita infectious contacts approaches the subpopulation size as pathogen infectiousness increases. Here, we illustrate that this is the case during epidemics of highly infectious pneumonia in bighorn lambs ( Ovis canadensis ). We classified individually marked bighorn ewes into disjoint seasonal subpopulations, and decomposed the variance in lamb survival to weaning into components associated with individual ewes, subpopulations, populations and years. During epidemics, lamb survival varied substantially more between ewe-subpopulations than across populations or years, suggesting localized pathogen transmission. This pattern of lamb survival was not observed during years when disease was absent. Additionally, group sizes in ewe-subpopulations were independent of population size, but the number of ewe-subpopulations increased with population size. Consequently, although one might reasonably assume that force of infection for this highly communicable disease scales with population size, in fact, host social behaviour modulates transmission such that disease is frequency-dependent within populations, and some groups remain protected during epidemic events.

Proceedings of the Royal Society B

Spatio-temporal dynamics of pneumonia in bighorn sheep

Bighorn sheep mortality related to pneumonia is a primary factor limiting population recovery across western North America, but management has been constrained by an incomplete understanding of the disease. We analysed patterns of pneumonia-caused mortality over 14 years in 16 interconnected bighorn sheep populations to gain insights into underlying disease processes. 2. We observed four age-structured classes of annual pneumonia mortality patterns: all-age, lamb-only, secondary all-age and adult-only. Although there was considerable variability within classes, overall they differed in persistence within and impact on populations. Years with pneumonia-induced mortality occurring simultaneously across age classes (i.e. all-age) appeared to be a consequence of pathogen invasion into a naïve population and resulted in immediate population declines. Subsequently, low recruitment due to frequent high mortality outbreaks in lambs, probably due to association with chronically infected ewes, posed a significant obstacle to population recovery. Secondary all-age events occurred in previously exposed populations when outbreaks in lambs were followed by lower rates of pneumonia-induced mortality in adults. Infrequent pneumonia events restricted to adults were usually of short duration with low mortality. 3. Acute pneumonia-induced mortality in adults was concentrated in fall and early winter around the breeding season when rams are more mobile and the sexes commingle. In contrast, mortality restricted to lambs peaked in summer when ewes and lambs were concentrated in nursery groups. 4. We detected weak synchrony in adult pneumonia between adjacent populations, but found no evidence for landscape-scale extrinsic variables as drivers of disease. 5. We demonstrate that there was a >60% probability of a disease event each year following pneumonia invasion into bighorn sheep populations. Healthy years also occurred periodically, and understanding the factors driving these apparent fade-out events may be the key to managing this disease. Our data and modelling indicate that pneumonia can have greater impacts on bighorn sheep populations than previously reported, and we present hypotheses about processes involved for testing in future investigations and management.

Journal of Animal Ecology

Female elk contacts are neither frequency nor density dependent

Identifying drivers of contact rates among individuals is critical to understanding disease dynamics and implementing targeted control measures. We studied the interaction patterns of 149 female elk ( Cervus canadensis ) distributed across five different regions of western Wyoming over three years, defining a contact as an approach within one body length (∼2 m). Using hierarchical models that account for correlations within individuals, pairs, and groups, we found that pairwise contact rates within a group declined by a factor of three as group sizes increased 33-fold. Per capita contact rates, however, increased with group size according to a power function, such that female elk contact rates fell in between the predictions of density- or frequency-dependent disease models. We found similar patterns for the duration of contacts. Our results suggest that larger elk groups are likely to play a disproportionate role in the disease dynamics of directly transmitted infections in elk. Supplemental feeding of elk had a limited impact on pairwise interaction rates and durations, but per capita rates were more than two times higher on feeding grounds. Our statistical approach decomposes the variation in contact rate into individual, dyadic, and environmental effects, and provides insight into factors that may be targeted by disease control programs. In particular, female elk contact patterns were driven more by environmental factors such as group size than by either individual or dyad effects.

Wyoming