Infection And Immiunity in Bighorn Sheep Metapopulations: Dynamics of Pneumonia

It is widely accepted that reducing contact between domestic and wild sheep limits pneumonia introduction, where domestic sheep transmit pathogens to bighorns. However, in some places, pneumonia persists for many years, even as local domestic in holding decline. We focused on one such system, the Hells Canyon region. We used an extensive long-term dataset to assess the evidence that pneumonia-causing pathogens induce an acquired immune response in bighorn sheep by reconstructing pneumonia exposure histories, and evaluating the impact an individual’s exposure history has on its survival. We found evidence of protective immunity lasting approximately two years, and saw that translocated individuals suffered much higher pneumonia risk than residents. Surviving many past pneumonia events decreased an adult’s risk in future events, although lambs born to ewes with many past exposures were at higher risk than their peers. These results are consistent with a disease that produces some chronic carriers that shed to their lambs for many years. Interestingly, while we might expect that the impact of chronic carriage on a population should decline over time and allow for population recovery (through senescence of carriers), we instead saw a trend of increasing lamb pneumonia mortality. Our findings corroborate long-held hypotheses about the presence of a chronic carrier state, and suggest that better understanding specific mechanisms leading to chronic carriage will help clarify the costs and benefits surrounding various management strategies

Modeling Management Strategies for the Control of Bighorn Sheep Respiratory Disease

Infectious pneumonia has plagued bighorn sheep populations and stymied recovery efforts across the western United States for decades.  Here we present a simple, non-spatial, stochastic, discrete-time model that captures basic bighorn sheep demographics and in which we simulate the dynamics of Mycoplasma ovipneumoniae, the suspected primary causative agent in bighorn sheep respiratory disease. We then use the model to explore the impacts of management approaches, including augmentation, depopulation and reintroduction, density reduction, and test-and-cull, aimed at reducing or eliminating the pathogen, its transmission, or associated infection costs. Results suggest that test-and-cull (testing 95% of a herd and removing PCR-positive individuals) and depopulation and reintroduction (assuming ability to only depopulate 95% of the herd) offer the best probability of eliminating the pathogen, although neither are expected to be 100% successful. Augmentation (adding 30 adult ewes) does not increase the probability of pathogen extinction, and in some cases may prolong pathogen persistence and diminish herd recovery.  Density reduction (randomly removing 25-50% of the herd) only modestly increases the probability of stochastic pathogen extinction and herd recovery.  Stochastic pathogen extinction and herd recovery is predicted to occur on occasion without any management intervention. Ultimately, decisions to manage respiratory disease in wild sheep must weigh the predicted success of the management tool against financial, logistical, ethical, and value-based considerations. Here, we aim to supply mechanistic-based predictions of the relative efficacy of currently employed or proposed tools, as well as characterize the sensitivity of these predictions to our assumptions about how the disease process works

Contact Networks and Mortality Patterns Suggest Pneumonia-Causing Pathogens may Persist in Wild Bighorn Sheep

Efficacy of disease control efforts is often contingent on whether the disease persists locally in the host population or is repeatedly introduced from an alternative host species. Local persistence is partially determined by the interaction between host contact structure and disease transmission rates: relatively isolated host groups facilitate pathogen persistence by slowing the rate at which highly transmissible pathogens access new susceptibles; alternatively, isolated host groups impede persistence for pathogens with low transmission rates by limiting the number of available hosts and forcing premature fade-out. Here, we use long-term data from the Hells Canyon region to investigate whether variable host contact patterns are associated with survival outcomes for 46 cohorts of bighorn sheep (Ovis canadensis) lambs subject to recurrent pneumonia outbreaks. We build social contact networks for each lamb cohort, and quantify variation in lamb mortality attributable to populations, years, and groups. We then refine estimates of chronic carriage rates in ewes, and disease-induced mortality rates in lambs, by finding parameters for the disease process that produce lamb morality rates similar to those observed when simulated on the observed host contact networks. Our results suggest that summer lamb hazards are spatially structured at the subpopulation level: 92.5 percent of the variation in lamb hazards during pneumonia outbreak years was attributable to sub-population-level groups, whereas 1.7 percent and 5.6 percent were attributable to year and population, respectively.  Additionally, the posterior distribution generated by our disease transmission model suggests that pneumonia-causing pathogens may persist locally in bighorn sheep populations, even during apparently healthy years

Cross-species pathogen spillover across ecosystem boundaries: mechanisms and theory

Pathogen spillover between different host species is the trigger for many infectious disease outbreaks and emergence events, and ecosystem boundary areas have been suggested as spatial hotspots of spillover. This hypothesis is largely based on suspected higher rates of zoonotic disease spillover and emergence in fragmented landscapes and other areas where humans live in close vicinity to wildlife. For example, Ebola virus outbreaks have been linked to contacts between humans and infected wildlife at the rural-forest border, and spillover of yellow fever via mosquito vectors happens at the interface between forest and human settlements. Because spillover involves complex interactions between multiple species and is difficult to observe directly, empirical studies are scarce, particularly those that quantify underlying mechanisms. In this review, we identify and explore potential ecological mechanisms affecting spillover of pathogens (and parasites in general) at ecosystem boundaries. We borrow the concept of ‘permeability’ from animal movement ecology as a measure of the likelihood that hosts and parasites are present in an ecosystem boundary region. We then discuss how different mechanisms operating at the levels of organisms and ecosystems might affect permeability and spillover. This review is a step towards developing a general theory of cross-species parasite spillover across ecosystem boundaries with the eventual aim of improving predictions of spillover risk in heterogeneous landscapes

Disease Introduction Is Associated With a Phase Transition in Bighorn Sheep Demographics

Ecological theory suggests that pathogens are capable of regulating or limiting host population dynamics, and this relationship has been empirically established in several settings. However, although studies of childhood diseases were integral to the development of disease ecology, few studies show population limitation by a disease affecting juveniles. Here, we present empirical evidence that disease in lambs constrains population growth in bighorn sheep (Ovis canadensis) based on 45 years of population‐level and 18 years of individual‐level monitoring across 12 populations. While populations generally increased (λ = 1.11) prior to disease introduction, most of these same populations experienced an abrupt change in trajectory at the time of disease invasion, usually followed by stagnant‐to‐declining growth rates (λ = 0.98) over the next 20 years. Disease‐induced juvenile mortality imposed strong constraints on population growth that were not observed prior to disease introduction, even as adult survival returned to pre‐invasion levels. Simulations suggested that models including persistent disease‐induced mortality in juveniles qualitatively matched observed population trajectories, whereas models that only incorporated all‐age disease events did not. We use these results to argue that pathogen persistence may pose a lasting, but under‐recognized, threat to host populations, particularly in cases where clinical disease manifests primarily in juveniles

A Pilot Study of the Effects of Mycoplasma ovipneumoniae Exposure on Domestic Lamb Growth and Performance

Mycoplasma ovipneumoniae is a globally distributed pathogen that has been associated with pneumonia in both domestic and wild Caprinae. It is closely related to M. hyopneumoniae, a respiratory pathogen of swine that is associated with decreased growth rates of pigs as well as clinical respiratory disease. In order to assess the effects of M. ovipneumoniae on lamb performance, we generated a cohort of lambs free of M. ovipneumoniae by segregation of test negative ewes after lambing, then compared the growth and carcass quality traits of M. ovipneumoniae-free and -colonized lambs from weaning to harvest. Some signs of respiratory disease were observed during the feeding trial in both lamb groups, but the M. ovipneumoniae-exposed group included more affected lambs and higher average disease scores. At harvest, lungs of lambs in both groups showed few grossly visible lesions, although the M. ovipneumoniae-exposed group did exhibit increased microscopic lung lesions (P\u3c0.05). In addition, M. ovipneumoniae exposed lambs produced lower average daily gains (P\u3c0.05), and lower yield grade carcasses (P\u3c0.05) compared to those of non-exposed lambs. The results demonstrated the feasibility of test and segregation for elimination of M. ovipneumoniae from groups of sheep and suggested that this pathogen may impair lamb growth and productivity even in the absence of overt respiratory disease

A model for leveraging animal movement to understand spatio-temporal disease dynamics

The ongoing explosion of fine-resolution movement data in animal systems provides a unique opportunity to empirically quantify spatial, temporal and individual variation in transmission risk and improve our ability to forecast disease outbreaks. However, we lack a generalizable model that can leverage movement data to quantify transmission risk and how it affects pathogen invasion and persistence on heterogeneous landscapes. We developed a flexible model ‘Movement-driven modelling of spatio-temporal infection risk’ (MoveSTIR) that leverages diverse data on animal movement to derive metrics of direct and indirect contact by decomposing transmission into constituent processes of contact formation and duration and pathogen deposition and acquisition. We use MoveSTIR to demonstrate that ignoring fine-scale animal movements on actual landscapes can mis-characterize transmission risk and epidemiological dynamics. MoveSTIR unifies previous work on epidemiological contact networks and can address applied and theoretical questions at the nexus of movement and disease ecology

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.The Nevada Department of Wildlife, the Utah Division of Wildlife Resources and New Mexico Department of Game and Fish.https://academic.oup.com/conphysam2023Centre for Veterinary Wildlife Studie

Epidemic growth rates and host movement patterns shape management performance for pathogen spillover at the wildlife–livestock interface

Managing pathogen spillover at the wildlife–livestock interface is a key step towards improving global animal health, food security and wildlife conservation. However, predicting the effectiveness of management actions across host–pathogen systems with different life histories is an on-going challenge since data on intervention effectiveness are expensive to collect and results are system-specific.We developed a simulation model to explore how the efficacies of different management strategies vary according to host movement patterns and epidemic growth rates. The model suggested that fast-growing, fast-moving epidemics like avian influenza were best-managed with actions like biosecurity or containment, which limited and localized overall spillover risk. For fast-growing, slower-moving diseases like foot-and-mouth disease, depopulation or prophylactic vaccination were competitive management options. Many actions performed competitively when epidemics grew slowly and host movements were limited, and how management efficacy related to epidemic growth rate or host movement propensity depended on what objectivewas used to evaluatemanagement performance. This framework offers one means of classifying and prioritizing responses to novel pathogen spillover threats, and evaluating current management actions for pathogens emerging at the wildlife–livestock interface. This article is part of the theme issue ‘Dynamic and integrative approaches to understanding pathogen spillover’