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Removal of chronic Mycoplasma ovipneumoniae carrier ewes eliminates pneumonia in a bighorn sheep population.

ABSTRACT: Chronic pathogen carriage is one mechanism that allows diseases to persist in populations. We hypothesized that persistent or recurrent pneumonia in bighorn sheep (Ovis canadensis) populations may be caused by chronic carriers of Mycoplasma ovipneumoniae (Mo). Our experimental approach allowed us to address a conservation need while investigating the role of chronic carriage in disease persistence.We tested our hypothesis in two bighorn sheep populations in South Dakota, USA. We identified and removed Mo chronic carriers from the Custer State Park (treatment) population. Simultaneously, we identified carriers but did not remove them from the Rapid City population (control). We predicted removal would result in decreased pneumonia, mortality, and Mo prevalence. Both population ranges had similar habitat and predator communities but were sufficiently isolated to preclude intermixing.We classified chronic carriers as adults that consistently tested positive for Mo carriage over a 20-month sampling period (n = 2 in the treatment population; n = 2 in control population).We failed to detect Mo or pneumonia in the treatment population after chronic carrier removal, while both remained in the control. Mortality hazard for lambs was reduced by 72% in the treatment population relative to the control (CI = 36%, 91%). There was also a 41% reduction in adult mortality hazard attributable to the treatment, although this was not statistically significant (CI = 82% reduction, 34% increase). Synthesis and Applications: These results support the hypothesis that Mo is a primary causative agent of persistent or recurrent respiratory disease in bighorn sheep populations and can be maintained by a few chronic carriers. Our findings provide direction for future research and management actions aimed at controlling pneumonia in wild sheep and may apply to other diseases.

SUBMITTER: Garwood TJ

PROVIDER: S-EPMC7141075 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Removal of chronic Mycoplasma ovipneumoniae carrier ewes eliminates pneumonia in a bighorn sheep population.

Garwood Tyler J TJ Lehman Chadwick P CP Walsh Daniel P DP Cassirer E Frances EF Besser Thomas E TE Jenks Jonathan A JA

Ecology and evolution 20200305 7

Chronic pathogen carriage is one mechanism that allows diseases to persist in populations. We hypothesized that persistent or recurrent pneumonia in bighorn sheep (Ovis canadensis) populations may be caused by chronic carriers of Mycoplasma ovipneumoniae (Mo). Our experimental approach allowed us to address a conservation need while investigating the role of chronic carriage in disease persistence.We tested our hypothesis in two bighorn sheep populations in South Dakota, USA ...[more]

PMID: 32274004

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Project description:BackgroundBronchopneumonia is a population limiting disease of bighorn sheep (Ovis canadensis) that has been associated with contact with domestic Caprinae. The disease is polymicrobial but is initiated by Mycoplasma ovipneumoniae, which is commonly carried by both domestic sheep (O. aries) and goats (Capra aegagrus hircus). However, while previous bighorn sheep comingling studies with domestic sheep have resulted in nearly 100% pneumonia mortality, only sporadic occurrence of fatal pneumonia was reported from previous comingling studies with domestic goats. Here, we evaluated the ability of domestic goats of defined M. ovipneumoniae carriage status to induce pneumonia in comingled bighorn sheep.Methodology/principal findingsIn experiment 1, three bighorn sheep naïve to M. ovipneumoniae developed non-fatal respiratory disease (coughing, nasal discharge) following comingling with three naturally M. ovipneumoniae-colonized domestic goats. Gross and histological lesions of pneumonia, limited to small areas on the ventral and lateral edges of the anterior and middle lung lobes, were observed at necropsies conducted at the end of the experiment. A control group of three bighorn sheep from the same source housed in isolation during experiment 1 remained free of observed respiratory disease. In experiment 2, three bighorn sheep remained free of observed respiratory disease while comingled with three M. ovipneumoniae-free domestic goats. In experiment 3, introduction of a domestic goat-origin strain of M. ovipneumoniae to the same comingled goats and bighorn sheep used in experiment 2 resulted in clinical signs of respiratory disease (coughing, nasal discharge) in both host species. At the end of experiment 3, gross and histological evidence of pneumonia similar to that observed in experiment 1 bighorn sheep was observed in both affected bighorn sheep and domestic goats.Conclusions/significanceM. ovipneumoniae strains carried by domestic goats were transmitted to comingled bighorn sheep, triggering development of pneumonia. However, the severity of the disease was markedly milder than that seen in similar experiments with domestic sheep strains of the bacterium.

Project description:Determining the demographic impacts of wildlife disease is complex because extrinsic and intrinsic drivers of survival, reproduction, body condition, and other factors that may interact with disease vary widely. Mycoplasma ovipneumoniae infection has been linked to persistent mortality in juvenile bighorn sheep (Ovis canadensis), although mortality appears to vary widely across subspecies, populations, and outbreaks. Hypotheses for that variation range from interactions with nutrition, population density, genetic variation in the pathogen, genetic variation in the host, and other factors. We investigated factors related to survival of juvenile bighorn sheep in reestablished populations in the northern Basin and Range ecosystem, managed as the formerly-recognized California subspecies (hereafter, "California lineage"). We investigated whether survival probability of 4-month juveniles would vary by (1) presence of M. ovipneumoniae-infected or exposed individuals in populations, (2) population genetic diversity, and (3) an index of forage suitability. We monitored 121 juveniles across a 3-year period in 13 populations in southeastern Oregon and northern Nevada. We observed each juvenile and GPS-collared mother semi-monthly and established 4-month capture histories for the juvenile to estimate survival. All collared adult females were PCR-tested at least once for M. ovipneumoniae infection. The presence of M. ovipneumoniae-infected juveniles was determined by observing juvenile behavior and PCR-testing dead juveniles. We used a known-fate model with different time effects to determine if the probability of survival to 4 months varied temporally or was influenced by disease or other factors. We detected dead juveniles infected with M. ovipneumoniae in only two populations. Derived juvenile survival probability at four months in populations where infected juveniles were not detected was more than 20 times higher. Detection of infected adults or adults with antibody levels suggesting prior exposure was less predictive of juvenile survival. Survival varied temporally but was not strongly influenced by population genetic diversity or nutrition, although genetic diversity within most study area populations was very low. We conclude that the presence of M. ovipneumoniae can cause extremely low juvenile survival probability in translocated bighorn populations of the California lineage, but found little influence that genetic diversity or nutrition affect juvenile survival. Yet, after the PCR+ adult female in one population died, subsequent observations found 11 of 14 ( 79%) collared adult females had surviving juveniles at 4-months, suggesting that targeted removals of infected adults should be evaluated as a management strategy.

Project description:The Norwegian muskox (Ovibos moschatus) population lives on the high mountain plateau of Dovre and originates from animals introduced from Greenland. In the late summers of 2006 and 2012, severe outbreaks of pneumonia with mortality rates of 25-30% occurred. During the 2012 epidemic high quality samples from culled sick animals were obtained for microbiological and pathological examinations. High throughput sequencing (pyrosequencing) of pneumonic lung tissue revealed high concentrations of Mycoplasma ovipneumoniae in all six animals examined by this method and Pasteurella multocida subsp. multocida in four animals, whereas no virus sequences could be identified. Mycoplasma ovipneumoniae and P. multocida multocida were also isolated by culture. Using real time PCR on lung swabs, M. ovipneumoniae was detected in all of the 19 pneumonic lungs examined. Gross pathological examination revealed heavy consolidations primarily in the cranial parts of the lungs and it also identified one case of otitis media. Histologically, lung lesions were characterized as acute to subacute mixed exudative and moderately proliferative bronchoalveolar pneumonia. Immunohistochemical (IHC) examination revealed high load of M. ovipneumoniae antigens within lung lesions, with particularly intensive staining in the neutrophils. Similar IHC finding were observed in archived lung tissue blocks from animals examined during the 2006 epidemic. An M. ovipneumoniae specific ELISA was applied on bio-banked muskox sera from stray muskoxen killed in the period 2004-2013 and sick muskoxen culled, as well as sera from wild reindeer (Rangifer tarandus tarandus) on Dovre and muskoxen from Greenland. Serology and mycoplasma culturing was also carried out on sheep that had been on pasture in the muskox area during the outbreak in 2012. Our findings indicated separate introductions of M. ovipneumoniae infection in 2006 and 2012 from infected co-grazing sheep. Salt licks shared by the two species were a possible route of transmitting infection.

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Removal of chronic Mycoplasma ovipneumoniae carrier ewes eliminates pneumonia in a bighorn sheep population.

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Removal of chronic <i>Mycoplasma ovipneumoniae</i> carrier ewes eliminates pneumonia in a bighorn sheep population.

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