Migration of whooper swans and outbreaks of highly pathogenic avian influenza H5N1 virus in eastern Asia

Abstract

Evaluating the potential involvement of wild avifauna in the emergence of highly pathogenic avian influenza H5N1 (hereafter H5N1) requires detailed analyses of temporal and spatial relationships between wild bird movements and disease emergence. The death of wild swans (Cygnus spp.) has been the first indicator of the presence of H5N1 in various Asian and European countries; however their role in the geographic spread of the disease remains poorly understood. We marked 10 whooper swans (Cygnus cygnus) with GPS transmitters in northeastern Mongolia during autumn 2006 and tracked their migratory movements in relation to H5N1 outbreaks. The prevalence of H5N1 outbreaks among poultry in eastern Asia during 2003-2007 peaked during winter, concurrent with whooper swan movements into regions of high poultry density. However outbreaks involving poultry were detected year round, indicating disease perpetuation independent of migratory waterbird presence. In contrast, H5N1 outbreaks involving whooper swans, as well as other migratory waterbirds that succumbed to the disease in eastern Asia, tended to occur during seasons (late spring and summer) and in habitats (areas of natural vegetation) where their potential for contact with poultry is very low to nonexistent. Given what is known about the susceptibility of swans to H5N1, and on the basis of the chronology and rates of whooper swan migration movements, we conclude that although there is broad spatial overlap between whooper swan distributions and H5N1 outbreak locations in eastern Asia, the likelihood of direct transmission between these groups is extremely low. Thus, our data support the hypothesis that swans are best viewed as sentinel species, and moreover, that in eastern Asia, it is most likely that their infections occurred through contact with asymptomatic migratory hosts (e.g., wild ducks) at or near their breeding grounds.

Figure 1. Map of the study area including satellite transmitter-marked whooper swan migratory routes.

Figure 2. Poultry density and H5N1 outbreak locations [circles (poultry), diamonds (migratory waterbirds), and triangles (wild non-waterbirds)] in eastern Asia (2003–2007).

Figure 3. Whooper swan movements (2006–2007) and proximity to HPAI outbreak locations (2003–2007) affecting poultry (circles) and wild non-waterbirds (triangles) in (a) northeastern China and (b) the Korea Peninsula.

Figure 4. Frequency of poultry and wild bird H5N1 outbreak events in relation to season as determined by whooper swan annual cycle stage.

Circles, squares, diamonds, and triangles represent the expected number of outbreaks in each of bird sector, bars represent the actual number of outbreaks, and arrows up/down indicate if there were greater than or less than expected numbers of outbreaks, respectively.

Figure 5. Relationships among migratory whooper swan movements, the timing of H5N1 outbreaks, and the density of poultry in eastern Asia.

Solid line represents mean poultry density at whooper swan locations through the annual cycle. Circles (poultry), diamonds (migratory waterbirds), and triangles (wild non-waterbirds) indicate the timing and underlying poultry density at each H5N1 outbreak event.