Risks of avian influenza transmission in areas of intensive free-ranging duck production with wild waterfowl

Abstract

For decades, southern China has been considered to be an important source for emerging influenza viruses since key hosts live together in high densities in areas with intensive agriculture. However, the underlying conditions of emergence and spread of avian influenza viruses (AIV) have not been studied in detail, particularly the complex spatiotemporal interplay of viral transmission between wild and domestic ducks, two major actors of AIV epidemiology. In this synthesis, we examine the risks of avian influenza spread in Poyang Lake, an area of intensive free-ranging duck production and large numbers of wild waterfowl. Our synthesis shows that farming of free-grazing domestic ducks is intensive in this area and synchronized with wild duck migration. The presence of juvenile domestic ducks in harvested paddy fields prior to the arrival and departure of migrant ducks in the same fields may amplify the risk of AIV circulation and facilitate the transmission between wild and domestic populations. We provide evidence associating wild ducks migration with the spread of H5N1 in the spring of 2008 from southern China to South Korea, Russia, and Japan, supported by documented wild duck movements and phylogenetic analyses of highly pathogenic avian influenza H5N1 sequences. We suggest that prevention measures based on a modification of agricultural practices may be implemented in these areas to reduce the intensity of AIV transmission between wild and domestic ducks. This would require involving all local stakeholders to discuss feasible and acceptable solutions.

Fig. 1. Conceptual model of integrated study components

The original analyses integrated here rely on original and historic agricultural and ecological field studies conducted in Poyang Lake and on original and historic epidemiological and virological analyses.

Fig. 2. Free-grazing-duck farms investigated within the study area

This map shows results from the survey of duck shelters conducted in October 2007. We estimated number of ducks per farm by counting the number of duck shelters per farm and estimated 1500 ducks per shelter. The grey lines delineate county boundaries.

Fig. 3. Seasonal fluctuations of the potential indirect contacts between wild and domestic ducks in rice paddy fields surrounding Poyang Lake, China

Rice production systems influence periods when domestic ducks are free-grazing and in indirect contact with wild ducks sharing the same paddy fields. Illustrations include a) the double crop rice production calendar. A single crop system also occurs in the area, although the double crop system is predominant in the vicinity of Poyang Lake (Li et al. 2012); b) free-grazing periods for domestic ducks in two cycles from March to April before planting of early rice and from October to February after harvesting of late rice(red arrows show the two yearly pulses of juvenile ducks in the paddy fields); c) wild duck presence in rice paddy fields estimated for resident and migratory ducks by the percentage of monthly satellite locations (95% binomial confidence interval was calculated with the binom.test function in R.); d) timing of wild duck departure and arrival for the wintering period.

Fig. 4. Locations of wild ducks at Poyang Lake

This figure shows the best Argos locations (classes 1 to 3) of migratory birds and GPS locations of resident wild birds in the Poyang Lake area for two periods of the year. Resident species included spot-billed ducks and mallards. Migratory species included Baikal teal, common teal, Eurasian wigeon, falcated teal, garganey and northern pintail (Supporting Table 1).

Fig. 5. Potential spread of highly pathogenic H5N1 strains by wild migratory ducks

H5N1 strains isolated from outbreaks in South Korea, Russia and Japan from April to May 2008 were closely related to each other and to strains isolated from Dongting Lake in March 2008 from domestic chickens, ducks, and water.