Injecting epidemiology into population viability analysis: avian cholera transmission dynamics at an arctic seabird colony

Abstract

Infectious diseases have the potential to spread rapidly and cause high mortality within populations of immunologically naïve hosts. The recent appearance of avian cholera, a highly virulent disease of birds caused by the bacterium Pasteurella multocida, at remote Arctic seabird colonies is an emerging conservation concern. Determining disease risk to population viability requires a quantitative understanding of transmission potential and the factors that regulate epidemic persistence. Estimates of the basic (R ) and real-time (R ) reproductive number are critical in this regard - enumerating the number of secondary infections caused by each primary infection in a newly invaded host population and the decline in transmission rate as susceptible individuals are removed via mortality or immunized recovery. Here, we use data collected at a closely monitored common eider (Somateria mollissima) breeding colony located in the Canadian Arctic to examine transmission and host population dynamics. Specifically, we infer epidemic curves from daily mortality observations and use a likelihood-based procedure to estimate changes in the reproductive number over a series of annual outbreaks. These data are interpreted in relation to concurrent changes in host numbers to assess local extinction risk. Consistent with expectations for a novel pathogen invasion, case incidence increased exponentially during the initial wave of exposure (R = 2·5; generation time = 6·5 days ± 1·1 SD). Disease conditions gradually abated, but only after several years of smouldering infection (R ≈ 1). In total, 6194 eider deaths were recorded during outbreaks spanning eight consecutive breeding seasons. Breeding pair abundance declined by 56% from the pre-outbreak peak; however, a robust population of >4000 pairs remained intact upon epidemic fade-out. Overall, outbreak patterns were consistent with herd immunity acting as a mitigating factor governing in the extent and duration of mortality. Disease mortality is frequently modelled as a form of stochastic catastrophe in wildlife population assessments, whereas our approach gives shape to the functional response between transmission and host population dynamics. We conclude that increased emphasis on integrating epidemiological and population processes is essential to predicting the conservation impact of emerging infectious diseases in wildlife.

Avian Cholera emergence in Arctic-nesting northern Common Eiders: using community-based, participatory surveillance to delineate disease outbreak patterns and predict transmission risk

“…Although outbreaks have caused high mortality at some locations, the outbreaks that we detected in the Hudson Strait have so far been localized and short in duration. This pattern stands in contrast to what has been observed at Mitivik Island, Nunavut (Descamps et al 2012, Iverson et al 2016, and several Common Eider breeding colonies in the St. Lawrence estuary of southern Québec, where recurrent outbreaks have been observed (The Joint Working Group on the Management of the Common Eider 2004). Moreover, outbreak occurrence has been temporally sporadic, suggesting that the pathogen is not readily maintained within the Northern Common Eider subpopulation across seasons, but rather requires periodic reintroduction to result in detectable outbreaks at breeding sites.…”

“…It is also worth considering that disease mortality is a part of the ecology of host populations, and the available evidence suggests at least some Common Eiders infected by Avian Cholera survive and develop immunity (Korschgen et al 1978, Iverson et al 2016). …”

“…One of these breeding colonies was at a long-term bird monitoring station administered by Environment and Climate Change Canada, located off the eastern coast of Southampton Island,Nunavut (Mitivik Island: 64.030 N,81.789 W). Avian Cholera outbreaks on Mitivik Island occurred annually from 2005 to 2012 (Iverson et al 2016). The other three locations were on the northern coastline of Québec in Nunavik, where mortality events were detected by Inuit eider http://www.ecologyandsociety.org/vol21/iss4/art12/ down collectors from the communities of Ivujivik, Kangiqsujuaq, andAupaluk in 2004 and2006.…”

Vaccination protects endangered albatross chicks against avian cholera

“…Finally, avian cholera affects wild bird populations in other very remote areas (Iverson et al, 2016;Leotta, Chinen, Vigo, Pecoraro, & Rivas, 2006). The presence of such infections in these isolated systems raises the question of their origin.…”

Exposure of breeding albatrosses to the agent of avian cholera: dynamics of antibody levels and ecological implications

“…An often neglected but critical compartment of the host population is thus the proportion of individuals surviving infection. These individuals may, for instance, constitute a reservoir compartment (Viana et al 2014) or limit transmission through a herd immunity effect (Iverson et al 2016). For instance, breeding females can mount a protective immune response and passively transmit it to their offspring (Boulinier and Staszewski 2008).…”