Infectious disease contributed to historical declines and extirpations of bighorn sheep (Ovis canadensis) in North America and continues to impede population restoration and management. Reports of pneumonia outbreaks in freeranging bighorn sheep following contact with domestic sheep have been validated by the results of 13 captive commingling experiments. However, ecological and etiological complexities still hinder our understanding and control of respiratory disease in wild sheep. In this paper, we review the literature and summarize recent data to present an overview of the biology and management of pneumonia in bighorn sheep. Many factors contribute to this population-limiting disease, but a bacterium (Mycoplasma ovipneumoniae) host-specific to Caprinae and commonly carried by healthy domestic sheep and goats, appears to be a primary agent necessary for initiating epizootics. All-age epizootics are usually associated with significant population declines, but mortality rates vary widely and factors influencing disease severity are not well understood. Once introduced, M. ovipneumoniae can persist in bighorn sheep populations for decades. Carrier females may transmit the pathogen to their susceptible lambs, triggering fatal pneumonia outbreaks in nursery groups, which limit recruitment and slow or prevent population recovery. The demographic costs of disease persistence can be equal to or greater than the impacts of the initial epizootic. Strain typing suggests that spillover of M. ovipneumoniae into bighorn sheep populations from domestic small ruminants is ongoing and that consequences of spillover are amplified by movements of infected bighorn sheep across populations. Therefore, current disease management strategies focus on reducing risk of spillover from reservoir populations of domestic sheep and goats and on limiting transmission among bighorn sheep.
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. This article is part of the theme issue ‘Dynamic and integrative approaches to understanding pathogen spillover’.
Summary1. 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 na€ ıve 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 pneumoniainduced 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.
Transmission of pathogens commonly carried by domestic sheep and goats poses a serious threat to bighorn sheep (Ovis canadensis) populations. All‐age pneumonia die‐offs usually ensue, followed by asymptomatic carriage of Mycoplasma ovipneumoniae by some of the survivors. Lambs born into these chronically infected populations often succumb to pneumonia, but adults are usually healthy. Surprisingly, we found that introduction of a new genotype (strain) of M. ovipneumoniae into a chronically infected bighorn sheep population in the Hells Canyon region of Washington and Oregon was accompanied by adult morbidity (100%) and pneumonia‐induced mortality (33%) similar to that reported in epizootics following exposure of naïve bighorn sheep. This suggests an immune mismatch occurred that led to ineffective cross‐strain protection. To understand the broader context surrounding this event, we conducted a retrospective analysis of M. ovipneumoniae strains detected in 14 interconnected populations in Hells Canyon over nearly 3 decades. We used multi‐locus sequence typing of DNA extracts from 123 upper respiratory tract and fresh, frozen, and formalin‐fixed lung samples to identify 5 distinct strains of M. ovipneumoniae associated with all‐age disease outbreaks between 1986 and 2014, a pattern consistent with repeated transmission events (spillover) from reservoir hosts. Phylogenetic analysis showed that the strain associated with the outbreak observed in this study was likely of domestic goat origin, whereas strains from other recent disease outbreaks probably originated in domestic sheep. Some strains persisted and spread across populations, whereas others faded out or were replaced. Lack of cross‐strain immunity in the face of recurrent spillovers from reservoir hosts may account for a significant proportion of the disease outbreaks in bighorn sheep that continue to happen regularly despite a century of exposure to domestic sheep and goats. Strain‐specific immunity could also complicate efforts to develop vaccines. The results of our study support existing management direction to prevent contacts that could lead to pathogen transmission from domestic small ruminants to wild sheep, even if the wild sheep have previously been exposed. Our data also show that under current management, spillover is continuing to occur, suggesting that enhanced efforts are indicated to avoid introducing new strains of M. ovipneumoniae into wild sheep populations. We recommend looking for new management approaches, such as clearing M. ovipneumoniae infection from domestic animal reservoirs in bighorn sheep range, and placing greater emphasis on existing strategies to elicit more active cooperation by the public and to increase vigilance on the part of resource managers. © 2016 The Wildlife Society.
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